Chapter 8: Individuals on the Autism Spectrum Represent Solitary Foragers
Grammarly
| Down Syndrome Defined: |
| Autism is a developmental disorder characterized by communication, social, and behavior challenges. The condition is lifelong and symptoms can vary considerably from one person to the next. Symptoms involve challenges or differences in motor skills and both intellectual and social abilities. Behavioral therapy can help children with autism develop social and communication skills. Here are some defining elements of autism: Communication difficulties Social challenges Behavioral differences Problems with empathy |
Chapter Summary
This chapter reviews etiological and comparative evidence supporting the hypothesis that some genes associated with the autism spectrum were naturally selected and represent the adaptive benefits of being cognitively suited for solitary foraging. The systemizing theory of autism is extended here, and people on the autism spectrum are conceptualized as ecologically competent individuals that could have been adept at learning and implementing hunting and gathering skills in the ancestral environment. Upon independence from their mothers, young individuals on the autism spectrum may have been psychologically predisposed toward a different life-history strategy, common among mammals and even some primates, to hunt and gather primarily on their own.
Many of the behavioral and cognitive tendencies that autistic individuals exhibit are viewed here as adaptations that would have complemented a solitary lifestyle. For example, the obsessive, repetitive, and systemizing tendencies in autism, which can be mistakenly applied toward activities such as block stacking today, may have been focused by hunger and thirst toward successful food procurement in the ancestral past.
Individuals on the autism spectrum share various behavioral traits with solitary species. Both solitary mammals and autistic individuals are low on measures of gregariousness, socialization, direct gazing, eye contact, facial expression, facial recognition, emotional engagement, affiliative need, and other social behaviors. The evolution of the neurological tendencies in solitary species that predispose them toward being introverted and reclusive may hold important clues for the evolution of the autism spectrum and the natural selection of autism genes.
Solitary animals are thought to eschew unnecessary social contact as part of a foraging strategy, often due to scarcity and wide food dispersal in their native environments. It is thought that the human ancestral environment was often nutritionally sparse as well, which may have driven human parties to disband periodically. Inconsistencies in group size must have led to inconsistencies in the manner in which natural selection fashioned the social minds of humans, which in turn may well be responsible for the large variation in social abilities seen in human populations.
This chapter emphasizes that individuals on the autism spectrum may have only been partially solitary, that natural selection may have only favored subclinical autistic traits and that the most severe cases of autism may be due to assortative mating. This solitary forager hypothesis of autism is explored in the context of anthropology, comparative neuroscience, epidemiology, neuroethology, and primatology.
Autism and its Place in Evolution, Natural History, and the Wild
Autism is a condition that affects individuals from infancy and is diagnosed based on three primary symptoms: social deficits, impaired communication, and stereotyped and repetitive behaviors (Piven, 2000). People with autism largely withdraw from social contact and become absorbed in private worlds of obsessive interests and repetitive activities (Kelly et al., 2008). Autism is highly heritable and associated with genetic and environmental risk factors (Cantor, 2009). It is thought that the genes associated with autism create very selective abnormalities that tend to affect brain regions associated with social cognition (Amaral, Schumann & Nordahl, 2008). Unfortunately, the genetics, molecular biology, and neuroscience of autism are still, relative to many other neurological disorders, shrouded with uncertainty due to their highly complex nature (O’Roak & State, 2008).
A portion of this complexity arises from the relatively large number of distinct susceptibility genes that have been identified, many of which can be completely absent even in pronounced autism (Freitag, 2007). This genetic diversity may be responsible for the clinical diversity, which ranges from debilitating social deficits to minor personality traits (Caronna, Milunsky & Tager-Flusberg, 2008). Medical science recognizes that autism is a continuum often referred to as the autism spectrum disorders (ASD). Of these disorders, the DSM recognizes autistic disorder (Kanner’s autism), childhood disintegrative disorder, and pervasive developmental disorder not otherwise specified (PDD-NOS or atypical autism) (Piven, 2000). Autistic disorder itself has also been broken into four subgroups: Asperger syndrome, the highest-functioning form (Asperger, 1944; Frith, 1991), autism, high-functioning, and low-functioning autism (Kanner, 1943; Baron-Cohen, 2006). Geneticists report that although the clinical distinctions do not map neatly onto specific genes or patterns of genes, lower-functioning individuals may have a higher total number of susceptibility alleles (Abrahams & Geschwind, 2008). For this reason, this chapter will not make evolutionary distinctions between individual autistic disorders but will focus on the autism spectrum and the range of related genes as a whole.
Several very different theories about the causes of autism have attempted to explain the scattered facts. It has been difficult for theorists to create a grand synthesis, and autism has been reconceptualized many times. At one point, it was thought that autistic children were purely a result of poor parenting, an idea that was once widely embraced but is now utterly rejected (Baron-Cohen, 1993). Autism is now known to be a biological phenomenon in which a genetic diathesis or susceptibility may interact with early environmental circumstances to determine the severity (Kumar et al., 2009). However, why this genetic susceptibility to autism is so prevalent and how the genes persisted despite the perceived adverse effects is unclear. It is the author’s view that conceptualizing autism in terms of evolutionary biology offers may help us make sense of its seemingly incongruous characteristics.
The risk of developing autism approaches .5 percent in the general population, making it a highly prevalent “disorder” from an evolutionary perspective (Gluckman, Beedle & Hanson, 2009). In the past two decades alone, the incidence of ASD has increased from 2-5 to 15-70 per 10,000 children, a dramatic increase which is attributed to heightened attention by the medical community as well as the broadening of diagnostic criteria (King & Bearman, 2009; Fombonne, 2009). Disorders like autism that are so prevalent that they exceed typical mutation rates are thought to have persisted because the genes responsible for them conferred some advantage in the ancestral environment (Nesse & Williams, 1998). To begin conceptualizing the evolutionary provenance of such a syndrome, it is essential to attain a rough date of its origins in natural history.
For years autism was thought to be a disorder that affected Caucasians exclusively. If this had been the case, an evolutionary explanation would have to explain why autism originated and spread in Europe over the last 20 to 40 thousand years. It is now known, however, that autism affects all human populations (Szatmari & Goldberg, 2000). In fact, autism presents with very similar prevalence rates worldwide in all studied races and ethnic groups (Fombonne, 2002). It has a very moderate association with immigrant status or socioeconomic status (Morrier et al., 2008). That autism has a similar prevalence in all studied populations suggests that it existed in a fully developed form before the first humans left Africa. Autism appears very ancient, yet how were the responsible genes selected and maintained over tens or hundreds of millennia?
This chapter will delineate the “solitary forager” hypothesis of autism which proposes that some genes contributing to autism were selected and maintained because they facilitated solitary subsistence. Low group number, population dispersion, band fission or dissolution, estrangement, separation, and the condition of being lost were probably infrequent but unavoidably reoccurring conditions that may have impacted the human genome during evolution. Individuals on the autism spectrum are described here as having had the potential to be self-sufficient and capable foragers in scenarios marked by diminished social contact. In other words, unlike neurotypical humans, these individuals would not have been obligately social and may have been predisposed toward a relatively solitary lifestyle.
The psychological characteristics of autism are taken here as a suite of cognitive adaptations that would have facilitated lone foraging. Like other solitary mammals with similar cognitive adaptations, they were probably not completely solitary; rather, they may have done some of their foraging alone and reconvened intermittently with familiar individuals. The chapter will use perspectives from evolutionary medicine to expound on this hypothesis in a conjectural and exploratory manner.
The Application of Evolutionary Medicine to Autism
Several sensible evolutionary theories of autism have been put forth. Autism has been conceptualized as a low-fitness extreme of a parentally-selected fitness indicator (Shaner et al., 2008). The authors have advanced that variation in the ability to connect socially to one’s parents, an adaptive trait, may have a maladaptive, extreme form that results in autism. Other researchers have envisioned autism as a consequence of paternally imprinted genes (Badcock & Crespi, 2006). This idea has been taken further, and autistic-like traits have been envisioned as constituting a male-typical strategy geared toward parental investment, low-mating effort, high partner-specific investment, and long-term resource allocation (Del Giudice et al., 2010).
These and other theories of autism are well-supported and plausible. None of these are directly compatible with the present hypothesis, but neither are they directly contradictory. Like the present hypothesis, they view autism as an extreme end of a continuum constituted by adaptive traits. Unlike these, though, the present hypothesis attempts to explain autism in terms of the behavioral ecology of hunting and gathering. This chapter will argue that autism represents “a lone forager in a social world.”
Importantly, social and asocial tendencies have neurological bases and vary widely between species (Robinson, Fernald, & Clayton, 2008). Innate predispositions toward sociality are also thought to vary within species (Brune & Brune-Cohrs, 2006), and it is thought that these predispositions, like the severity of autism, can be shown to exist on a continuum. Perhaps a large proportion of the autism spectrum, maybe even pronounced cases of autism, may reflect normal variation. The autism spectrum will be conceptualized as representing naturally occurring variation, at one end of the sociality continuum.
The Solitary Forager Hypothesis of Autism
Today, the cognitive disabilities associated with the autism spectrum are clear and well documented; however, modern social, occupational, and mating practices may conceal the evolutionary or adaptive benefits. From an anthropological perspective, our society is very different from the ancestral environment. Because of the large group sizes seen in modern-day cities and the very social nature of modern employment, social abilities such as congeniality, extraversion, and savoir-faire are highly regarded. Even minimal social dysfunction or awkwardness can be professionally and socially problematic. In fact, the DSM considers social ability as a critical component of psychological health (APA, 1994).
Social ability may have been less critical in the prehistoric past, especially in specific contexts. During the six million years since our branch diverged from that of chimpanzees, our ancestors lived in relatively small groups that probably fluctuated greatly in size (Nesse & Williams, 1995). Under these conditions, the abilities to relate effortlessly to a stranger, to display affection in a demonstrative manner, or to charm a foraging companion were probably exposed to inconsistent selective pressures. Inconsistencies in the level of social ability that our environment demanded may well be responsible for the considerable variation in social abilities seen in human populations and the extremes of social “dysfunction.”
The adaptive value of social ability may have been inconsistent in the ancestral past for many reasons. Depending on the period of human evolution, the geographical location, the ecological setting, and the cultural habits of the group in question, ancestral foragers may have foraged intimately with others throughout the day, may have spent weeks foraging alone, or anything between these two extremes. Humans are a highly social species, and this tells us that, like chimpanzees, we must have spent much of our formative years congregating together (Byrne & Bates, 2007). However, just as our social tendencies are a testament to our social past, our asocial tendencies may indicate the opposite. In other words, during prehistoric times, a certain proportion of breeding individuals may have adapted neurologically to living under conditions where group size was very small or social contact was attenuated. This may have led to the numerous autism genes found in the modern-day gene pool. It is unclear which phenotypes on the autism spectrum might have been selected for in the ancestral environment. Surely, it is most conservative and parsimonious, though, to assume that high-functioning or subclinical phenotypes were the substrate for selection.
Certain eccentricities or impediments peculiar to autism may have precluded past researchers from considering that individuals on the autism spectrum may have survived well during prehistoric times. As with neurotypical people, behavior in autism can vary markedly from individual to individual. Some individuals with autism are awkward and unwieldy, while others are graceful and nimble. Some are gentle and kind, while others can become angry and violent. Some are severely mentally disabled, whereas others are cognitively gifted. These extremes, often barely tempered by social constraints, might make these individuals appear dangerously unnatural. Given this, and given that a proportion of individuals with autism cannot be mainstreamed comfortably in elementary school, it may appear that autism would have been maladaptive.
Although some individuals on the autism spectrum have grave social deficits, many may have been able to survive and prosper as effectively as other solitary mammals in their natural environment. A great deal of new research supports this line of reasoning by illustrating that autistic individuals may have great trouble with social cognition, but their other cognitive abilities are primarily intact (Baron-Cohen, 2003). The following section will consider some of the findings in the literature on autistic intelligence, supporting the notion that autistic individuals can be very competent in areas that do not require social cognition.
Systemizing vs Empathizing
Simon Baron-Cohen and others have changed how many researchers think about autism by pointing out that a social deficit alone may account for most of the symptoms. Previous theories of autism characterized autistics as cognitively confused, disorganized, or incoherent. On the other hand, Baron-Cohen has characterized autistics as having profound social disabilities but otherwise being coherent and able-minded. His theories of autism emphasize that the central deficit is in the social domain, specifically in the inability to empathize with and model the minds of others (Baron-Cohen, 1994).
A large number of subsequent studies have substantiated that “theory of mind,” or the ability to empathize with others, is impaired in autism (Colle, Baron-Cohen & Hill, 2007). Baron-Cohen and others have argued persuasively that impaired theory of mind in autism can be independent of learning ability and general intelligence. Furthermore, he has documented that some autistic individuals can have superior technical understanding of physical systems (sometimes referred to as folk physics as opposed to folk psychology) compared to their age-matched peers. He has termed this ability “systemizing.”
Baron-Cohen has demonstrated that even though individuals with autism are poor at empathizing, they are good at systemizing. Systemizing is the ability to observe a physical system and make inferences or conclusions about how it works and what causes it to work the way it does. He explains that systemizing works well for phenomena that are lawful and deterministic, but that systemizing is much less useful when it comes to predicting moment-by-moment changes in a person’s behavior. Empathizing and forming theories about the other person’s mind are required for the latter task (Baron-Cohen et al., 2009).
According to Baron-Cohen, abilities associated with empathizing include responding empathetically to distress, intuiting another’s emotional state, being sensitive to facial expressions, and demonstrating ability with language. On the other hand, systemizing is associated with ability in domains such as map reading, mental rotation, physics, mathematics, and motoric systems (Baron-Cohen, 1995). People who are good at empathizing are thought to lean toward jobs like social work, psychology, and nursing. High systemizing is thought to lead to jobs in engineering, construction, and science.
Unlike autism, empathizing seems unimpaired in individuals with Down syndrome, William’s syndrome, and some other forms of intellectual disability, despite their decreased ability to systemize and lower general intelligence (Baron-Cohen et al., 1986; Karmiloff-Smith et al., 1995). This dissociation between intelligence and empathy indicates a genetic and cognitive difference between the two disorders. Many children with autism have IQs well below the average for their age; however, the intelligence tests that correct for social disability have shown that many individuals with autism may not be intellectually impaired at all (Scheuffgen et al., 2000). Contrary to speculations, researchers have found little evidence of a deficit of executive function in autistic children younger than four years of age. This suggests that the mild executive function deficits seen after age 4 are not primary to the disorder but may arise later because of the absence of social learning (Griffith et al., 1999). In fact, several “less learned, more innate” executive functions, including inhibition and visual working memory, appear to be spared in autism (Russell, 1997).
Baron-Cohen, and those who have followed him, have performed a great deal of research showing that systemizing is part of the genetic profile of autism and that the autistic spectrum is continuous with normal human variation. He has demonstrated that the parents and relatives of people with autism tend to be good at systemizing but not as good at empathizing. He has compiled data showing that fathers and grandfathers of males with autism are twice as likely to be engineers compared to males in the general population (Baron-Cohen, 2006). He has also shown that students in the natural sciences have more relatives with autism than students in the humanities (Baron-Cohen, 2006).
Baron-Cohen and others have also shown that in Asperger’s syndrome and high-functioning autism, individuals can perform at average or often superior levels in tasks requiring the systemization of information. People with Asperger’s scored higher on his Systemizing Quotient (SQ) (Baron-Cohen et al., 2003), performed better on tests of intuitive physics (Lawson et al., 2004), and can reach extremely high levels of achievement in systemizing domains, such as mathematics, physics, and computer science (Baron-Cohen et al., 1999). This has been called the “autism advantage” in popular autism advocacy. It is thought that these high-functioning autistic individuals may be neurologically well-suited for certain jobs that are detail-oriented, repetitive, and involve the identification of technical errors (Scheuffgen et al., 2000).
A popular conceptualization of this purports the idea that quirky computer specialists working in Silicon Valley, for example, desire jobs allowing them to work alone on computing problems, tend to marry others who are high on systemizing but low on empathy and tend to have the propensity to have children that, like them, are on the autism spectrum. Baron-Cohen pointed out that “If systemizing talent is genetic, such genes appear to co-segregate with genes for autism (Baron-Cohen, 2006).”
Baron-Cohen and others have successfully convinced many researchers that autistic people are intelligent in a different way and very good at systemizing and understanding non-social, natural processes. Baron-Cohen has even posited that evolution may have maintained the genes for autism precisely because of the systemizing ability, also suggesting that many cases of autism may be due to the assortative mating of two high-systemizing parents (Baron-Cohen, 2006). The present paper hopes to extend these arguments by pointing out that these natural systemizing abilities could have predisposed people on the autism spectrum to be able-minded, able-bodied, solitary foragers in the prehistoric past.
Predicted Hunting and Foraging Patterns in Autism
In modern society, due to cultural, historical, and sociological circumstances, many individuals with autism do not learn to become self-sufficient. Hindered by social deficits, many people with autism do not follow their peers toward social and occupational mobility. Today, children must go through a prolonged period of education and socialization to reach a point where they can hold a job and live autonomously. Autonomy and food procurement depend on social abilities and learning that took place in a particularly social setting, the school classroom. Schooling can be arduous for individuals with autism because, as the systemizing theory of autism has demonstrated, individuals with autism have a proclivity to learn things on their own rather than from others (Siegel, 2003).
Unfortunately, the interests chosen, and knowledge acquired by individuals with autism often do not coincide with financial, professional, or social opportunities (Cimera & Cowan, 2009). Even when carefully guided by loving parents, it is difficult for many individuals with autism to teach themselves how to become self-sufficient in today’s world. However, this may have been much more natural in the ancestral environment, particularly considering that merely 10,000 years ago, neither food procurement nor the acquisition of a place to sleep was necessarily contingent on social ability as they are today.
Like mothers in contemporary foraging societies, mothers in the ancestral past would have required their children to learn how to forage for food from an early age (Buss, 2005). Virtually all mammals, whether of social or asocial species, use their systemizing abilities to learn food procurement techniques from their mothers (Krebs & Davies, 1993). The offspring of asocial mammalian species may not be motivated to empathize much with their mother but are nonetheless driven by hunger to attend to her examples and internalize her tactics (Begon et al., 1996). This strategy works well for hundreds of species of asocial mammals (even ones with very small brains and limited systemizing abilities) and presumably would have worked well for individuals with autism.
It would be an immoral experiment to place an autistic toddler and its mother in the wilderness for years in order to see if he or she learns and thrives. However, would such an experiment be needed if it could be shown that autistic behaviors are normal relative to those of other solitary animals taken out of the wild since birth (say, a pet reptile, a domestic cat, or a captive orangutan)? Are there reasons to think that an individual with autism, living in prehistoric times, would not be strongly motivated by thirst, appetite, discomfort, sexual urges, and other innate instincts to become nutritionally independent and to increase its reproductive success?
The behavior of autistic individuals is often seen as bewilderingly inappropriate in a social context because they often become interested in or obsessed with socially meaningless activities (Piven, 2000). In a natural environment, though, it is likely that hunger would have motivated them to redirect their obsessive tendencies toward food procurement. Today, their hunger for food does not drive them to refine food procurement techniques because their parents feed them whenever they are hungry. Modern humans are responsible for social and academic learning and are rarely given a chance to be positively reinforced by successful food acquisition. This temporal or causal pairing between learning and satiety, integral for wild animals (Domjan, 2003), has been artificially taken away from modern children. Because the compelling natural instinct of hunger does not actuate or motivate modern individuals with autism, their efforts and skills are misplaced onto irrelevant stimuli.
Humans habituate to things they are not interested in and systemize things they find rewarding, motivating, or intrinsically interesting. In the ancestral past, activities leading up to the sating of hunger would have been highly reinforced. Thus, food procurement and food processing strategies would have been the primary variables of the reinforcement schedule for individuals with autism. Perhaps, when children with autism ignore their parent’s examples of social behavior today, it is because these examples seem uninteresting and meaningless. In contrast, in the ancestral past, they would have been inspired by their parent’s hunting and gathering activities.
Neurotypical children are highly intrinsically motivated to learn social customs. Theory of mind and empathy play a large role in their motivation. They anticipate what others want them to do and they want to impress or please. They want to delight their parents in the same way a dog wants to appease its owners. Individuals with autism don’t exhibit as much of an innate need to please others. Without it they have trouble adjusting and conforming. The best form of therapy for someone with autism may be found in refocusing their interests and drives, and perhaps the best way to do this is through food. It sounds inhumane to many people to use a meal to shape human behavior. However, trial and error in food acquisition would have been formative for prehistoric children. Creating appropriate protocols to use food to properly reinforce students with autism will be difficult for cognitive/behavioral psychologists but it could work. It may also prove effective for individuals with intellectual disabilities. I have a strong conviction that many neurodevelopmentally challenged people could potentially become high-functioning given the proper incentives, reinforcement histories, and brain training.
Today, because they are not able to forage or to watch their parents forage and because they can obtain food free of effort, the interests of young children with autism are redirected toward nonsocial activities, like stacking blocks, flipping light switches, lining toys up in rows, playing with running water, chasing vacuum cleaners, and collecting bottle tops. This misapplication of an innate tendency is known in human ethology as a type of “vacuum activity (Eibl-Eibesfeldt, 2009).”
The powerful and mobilizing asocial fascinations and preoccupations seen in modern-day autism could have aided their prehistoric counterparts in self-preservation. The interests of autistic individuals often lead to the development of islets of aptitude or competence. Despite apparent deficits, many have refined or even mastered specific skills. These talents are often referred to as splinter skills. They may include eccentric proficiencies, such as penchants for drawing, music, rote memory, or puzzle solving (Treffert, 2009). In extreme cases, these skills might include savant abilities, including counting, hyperlexia, pattern finding, and calendar or mathematical calculation (Treffert, 2000). Some of these skills and abilities in autism were probably acquired because the individual focused intently on a particular type of problem-solving. In the past, these elaborate abilities would probably have mapped onto the acquisition of foraging techniques, which, would have been honed to proficiency through rote repetition and practice.
Many anthropologists report that the hunter-gatherers they study cultivate extraordinary naturalistic abilities and can sense and perceive things to which they are virtually blind (Kaplan et al., 2000). These abilities, like tracking, ranging, stalking, food processing, mapping of terrain, and knowledge of flora and fauna, may be areas through which the potential for autistic or savant-like abilities was channeled in the ancestral past. The same could be said for the deep stores of specialized or technical knowledge exhibited by people on the autism spectrum. This penchant for knowledge about pet interests could have been dedicated to memorizing edible and inedible species, analyzing the habits of prey items, understanding self-protection, maximization of food-collection efficiency, tool fashioning, and shelter procurement.
Aside from their asocial preoccupations, individuals with autism also exhibit stereotyped and repetitive actions (Piven, 2000). Many mammals engage in perseverative or repetitious behaviors, especially when placed into unnatural or confining environments (Lewis et al., 2007). Repetitive, stereotypical behavior (including self-injurious behavior) is very rare in the wild but very common in captive animals as well as in autism (Grandin, 2009). More intelligent animals seem to have an increased capacity for self-injurious behaviors. It has been estimated that 10 to 15 percent of rhesus monkeys living alone in a cage develop self-biting, head-banging, and self-slapping (Lewis et al., 2007). This may indicate that the living conditions that many young individuals with autism experience are artificial and possibly inhumane, as they are not as stimulating or motivating as the wild environment they are born expecting.
The propensity toward strict adherence to routine seen in autism may have close analogs in the “master routines” and “subroutines” of many nonsocial species (e.g., waking, cautious emergence, defecation, grooming, basking, foraging, returning, bedding, sleeping). Although such neurologically mediated rituals can sometimes be repetitive and inflexible in many vertebrate species, they are essential regulators of adaptive behavior (MacLean, 1990). Perhaps the persistent, stereotyped behaviors characteristic of autism had ecological utility in that they allowed structure, order, and self-regulation.
Why is there a tendency toward tedium and invariability, then? Most of the variety in the life of a human hunter-gatherer is probably found in its social interactions. There would probably be much less variety in the life of a secluded hunter-gatherer. A lone forager would be forced to engage in lonely, repetitive, and stereotypic activities, such as repeatedly scanning for threats and items to scavenge, picking and processing fruit, searching for and extracting vegetables, and locating and capturing prey items. An obsessive desire for sameness, repetition, and ritual makes little sense in the context of a social setting but seems applicable in a solo setting. In fact, it might be harmful to expect variability and to thrive on unpredictability in a solitary scenario because of the monotony of living alone.
A mind that is highly geared toward using social cognition and forming emotional relationships would have been disadvantageous in an individual who was forced by circumstance to live companionless. This may help explain why many individuals with autism have an undue preference for their own company, pay attention to the nonsocial aspects of people, and treat others as inanimate objects (Bowler, 2007). Concentrating on empathy or theory of mind would probably have been impractical and counterproductive. Martin Brune (2006) has speculated that theory of mind and social cognition are probably vulnerable to dysfunction. He pointed out that most people, at one time or another have strong desires to ascribe intentions to non-animals. A solitary forager without autism may likely attribute agency or ascribe intentions to inanimate objects, amounting to displaced and confused behavior.
Like other animals that are not obligately social, many individuals with autism avoid close bodily contact and fail to establish emotional relationships. It seems that these tendencies might have facilitated solitary life whereas the inclinations to seek out physical contact and emotional relationships could have made solitary life miserable or unbearable. Classic works of fiction portraying humans abandoned or marooned by others emphasize the human need for companionship. The protagonists in such works frequently have unremitting obsessions with imaginary friends, behavior that would be extraneous and probably maladaptive for a solitary human. People on the autism spectrum would be less likely to yearn for companionship and more likely to focus on survival. Solitary species have minimal abilities for social cognition. This is probably because gregarious predispositions, companionable inclinations, and social instincts, in general, are maladaptive in a solitary context.
Here is a short excerpt from an interesting 2011 news story from Olympia Meola about a boy with autism that was lost in the woods:
“It’s hard to know exactly what was going through 8-year-old Robert Wood Jr.’s mind as he wandered for five days through the woods in Hanover County, but it’s possible that aspects of his autism helped him survive as much as they contributed to his disappearance. Educators familiar with Robert say his quiet determination and lack of self-awareness may have carried him through.”
In her book “Animals Make Us Human” autistic professor Temple Grandin (who herself engaged in repetitive, restricted, and self-injurious behavior at a young age) points out that even though domestic dogs and cats both live comfortably with humans, only cats can leave a human family to live solitarily in the wild (Grandin, 2009). “If you put the family poodle out in the countryside, his chances of surviving are low unless he finds another family to live with. But abandoned cats do fine.” Here she underscores that some animals are obligately social, whereas others can transition between social and solitary lifestyles. Her life story is an attestation to the fact that individuals with severe autism can make this transition while maintaining the “cognitive coherency” to contribute profoundly to both industry and academia (Grandin, 1996).
Why Orangutans Became Solitary Foragers
“To understand a man, look to men; and to understand men, look to the animals.” Jean-Jacques Rousseau
Most animals, many mammals, and several species of primates are solitary and seek food independently. Such a solitary foraging strategy can even be effective for apes. An analysis of the behavior of orangutans in the wild offers valuable insight into the ecology of a reclusive ape. Orangutans, the species third closest to humans, as revealed by molecular studies, live solitarily in the wild. Orangutans eat, sleep, hunt, and forage on their own (Delgado & Van Schaik, 2000). They are often described as cautious and introverted, and it has been estimated that Bornean orangutans spend at least 95% of their time alone (Van Schaik, 1999). Orangutans have low interaction and association rates and only infrequently meet up with conspecifics, often only to mate (Van Schaik & Van Hoof, 1996). They have been reported to congregate in small groups temporarily but only to eat from a particularly fruit-laden tree. Several specialists emphasize that orangutans have limited social aptitude and prefer solitude (Van Schaik, 1999). Van Schaik (1999) has concluded that, unlike all other species of apes, well-defined communities do not appear to exist in any orangutan population studied.
In orangutans, inculcation in infancy and juvenility consists of learning about food procurement from the mother. In stark contrast, chimpanzees are indoctrinated into learning about food procurement and socialization (Delgado & Van Schaik, 2000). Orangutan mothers teach their babies to recognize edible food species, implement foraging techniques, find shelter from the elements, protect themselves from predators, and develop effective ranging capabilities (Noorwijk & Van Schaik, 2005). Compared to chimpanzees, young orangutans do not learn much from their mothers about communication or socialization; however, they do learn everything that they need to survive and reproduce and can reach complete ecological independence before age 10 (Wich, Atmoko & Setia, 2009).
Unlike their orangutan counterparts, chimpanzee adolescents reliably stay with (or at least frequently visit) their mothers for months or years after they have been weaned (Goodall, 1986). Their strong affective ties, emotional attachments, and gregarious nature keep mother and child in contact into adulthood or, at times, throughout life (Galdikas, 1984). Orangutans, on the other hand, exhibit very different behavior. Adolescent orangutans reliably leave their mother and go off on their own to forage very soon after weaning. The bond between the mother and child is mainly based on the provision of milk (Noordwijk & Van Schaik, 2005).
One of the most frequent complaints of parents with autistic children is that they find it difficult to build an emotional bond with the child (Frith, 1991). One might imagine that in an ancestral setting, the bond between a mother and her autistic child could have been as delicate (and yet, at times, as ecologically appropriate) as the bond seen in orangutans. Despite this relative delicacy, the vast majority of babies and children with autism do develop genuine psychological attachments to their caregivers. This attachment would probably have facilitated the acquisition of survival techniques as it does in orangutans.
The ability to make inferences about the mental states of others probably first emerged in a clear form during early primate evolution due to heavy selection from the social environment (Brothers, 1990). However, apes, relative to monkeys, have elaborated extensively upon this ability, presumably because their social environment was even more critical. Aside from orangutans, all apes, including gibbons, gorillas, chimpanzees, and bonobos, are social species, much like humans (Chance & Jolly, 1970). To some degree, orangutans regressed in their social abilities relative to other apes because, as their group size decreased, pressure from the social environment must have decreased along with it.
After orangutans diverged from the common ancestor they shared with gibbons around 18 million years ago, they moved into Southeast Asian rainforests, where they were forced to give up their social lives for solitary ones because of ecological constraints (Sugardjito, te Boekhorst & van Hoof, 1987). Primatologists generally agree that orangutans live solitary lifestyles primarily because the islands of Borneo and Sumatra, where they are found, have poor food density. Relative to the lush African regions that chimpanzees and gorillas inhabit, these islands cannot support large groups of social apes (Delgado & Van Schaik, 1999). If orangutans lived in larger social groups, they would have to travel extremely far (up to 20 miles) each day simply to get enough food to sustain themselves (Sugardijto, te Boekhorst & van Hoof, 1987). Because orangutans are large animals, and because the trees and bushes in their non-seasonal habitat go through various phases of producing buds, shoots, and fruit, the orangutans must forage through many plants daily to ferret out suitable dietary foodstuffs (Delgado & van Schaik, 2000).
Because they must traverse so much land every day to obtain sufficient calories, individual orangutans must define large territories for themselves. It is thought that in Sumatra, each orangutan needs nearly a square kilometer and that in Borneo, each requires an even larger area of spatial isolation (MacKinnon, 1974). Fascinatingly, Borneo is thought to be less food-dense, and Bornean orangutans are thought to be less socially inclined when compared to Sumatran orangutans (Van Schaik, 1999). Food density of the habitat is actually known to be an important determinant of group size in a number of animals (Marler, 1968). In fact, when food becomes scarce, even chimpanzees split up to search for food alone (de Waal, 1982).
Harsh and unpredictable climates marked much of human evolution (Reed, 1997). The Pleistocene and Pliocene ice ages caused frequent aridity of the African plains, which would have dried up many food sources for our foraging ancestors (Ravelo et al., 2004). These conditions would have rendered our habitat nutritionally scarce (Bobe, Behrensmeyer & Chapman, 2002), likely compelling groups of our ancestors to disband. Humans may have been forced to do this habitually in the past, even though we are an inherently social species. In sum, environmental forces prominent during our evolution caused nutritional scarcity that, at least in some geographic regions, may have created the same conditions that selected orangutans to become solitary.
Another condition that influences selection for sociality is the distribution of food resources. It is known that when food is approximately evenly dispersed in an environment, solitary foraging yields higher energy returns, but when food is clumped, group foraging becomes more efficient (Marler, 1968). One may not even need to invoke scarcity or food distribution patterns to conclude that many pre-social species, including humans, may have experienced historical disruptions (either punctuated or gradualistic) in their social continuity that left lasting traces in the genome.
Adaptations particular to orangutans, which are thought to reflect their life-history strategies, may have implications for autism. Orangutans show prominent sexual dimorphism (van Schaik, 2004), which is thought to be due to high testosterone levels in the males. Autistics are also thought to exhibit elevated testosterone levels, which may be associated with increased fetal exposure to testosterone (Knickmeyer et al., 2005). It might make sense that a solitary forager strategy is better suited to males, given that female animals of many species have need for parenting proficiency. Male orangutans spend a greater proportion of their time alone than females (most of the time spent between two males is thought to be attributable to random, unintended encounters) (van Schaik, 1999).
Interestingly, autism is four times more prevalent in men than women, is accompanied by more severe anomalies in brain structure in men, and is known to have a worse prognosis (Bowler, 2007). Higher testosterone levels in autistic males may have increased their sexual aggressiveness and sexual attractiveness. Mating practices of individuals on the autism spectrum may have been similar to those of the orangutan. Females with autism or on the autistic spectrum probably had little difficulty procuring receptive sex partners. Conversely, males could have procured partners using the same tactics used by male orangutans, such as propositioning, perseverative soliciting, provisioning/food sharing, and others.
Fighting and politics take up a large proportion of a chimpanzee’s day. This is just not the case with the solitary orangutan. My previous book, Program Peace, documents the large toll the dominance hierarchy takes on people. Social competition consumes much of our thought and is usually emotionally toxic. It also compels us to use suboptimal, submissive displays which drain us and adversely affect our healthy. Interpersonal conflict, Machiavellian games, plays for superiority, and attempts to dominate others take mental and physical energy. They also waste time. Individuals with autism would likely have been largely immune to this. They are not concerned with fraternizing, gossip, powerplays, bragging, and putting others down. Escaping the pecking order, and its extraneous costs, may have been a large benefit to having autism. This seems to still be true of people with autism today.
It has not yet been made clear how much orangutan neurology has been affected by their recent stint of solitary foraging, which has only gone on for the last 10,000 years (Van Schaik, 1999). Regardless, evolutionary comparisons with solitary primates (e.g., galagos, lorises) and other solitary mammals (e.g., tigers, polar bears, wolverines, moose) that are known to have neurological adaptations causing them to lack biological instincts for gregariousness, affection, and strong social relationships should be informative.
It is vital to affirm that no offense is intended toward autistic individuals in this comparison with orangutans. Only traits related to sociality are compared here, and individuals with autism are not in any way equated with apes in general. In fact, individuals with autism are only compared to orangutans here to the same extent that neurotypical individuals are compared to chimpanzees. Orangutans were selected as a basis of comparison for this chapter simply because they are the species of solitary foragers most closely related to humans.
How Autism Could Have Been Naturally Selected
The evolution of social tendencies in animals is a poorly understood research topic. Even less understood is the evolution of solitary tendencies from social forebears. It is clear that there are costs and benefits to living in groups and that the pressures from the social environment can change abruptly (Perez-Barberia, Shultz & Dunbar, 2007). Surely, in the past, individuals on the autism spectrum were sometimes born into the arms of supportive and cohesive social groups, much like today. If autism does represent a solitary forager strategy then this circumstance could have constituted a mismatch that may have been negatively selected against. However, most adaptations have associated risks, and instead of representing a panacea, they reflect tradeoffs that, over evolutionary time, produce more benefits than costs on average.
This mismatch may not even have decreased fitness. Given the propensities of modern-day people with autism, such individuals might have chosen to journey off alone nomadically or hermitically. Alternatively, they might have chosen to forage alone but return to their group infrequently to interact and travel with group members. This may have depended on “how autistic” the individual was.
Even individuals on the far side of the autism spectrum may not have even been truly solitary during prehistory. Social chess abilities or Machiavellian intelligence are not well developed in people on the autism spectrum. Their speech and mannerisms can be monotonous and mechanical, yet this may not have kept them from offering valuable skills and forming functional relationships with members of their tribe. In many cases, autistic individuals exhibit pragmatic competence that could have made them valuable attributes to their foraging companions. Today, a large proportion of individuals with Asperger’s have been assimilated into elite social and professional spheres even though they are not adroit social conformers (Grandin, Duffy & Attwood, 2008).
It is reasonable to imagine that a proficient hunter with autism could be not only tolerated but highly valued by a small band of hunters who were each eccentric themselves, not having been exposed to our modern, relatively conformist, post-industrial society. This would be akin to today’s situation, where millions of mainstreamed autistic children worldwide have become accepted on the playground, despite their differences. It is well accepted that despite valuing their time alone, many individuals with autism enjoy friendships and have a documented predilection for valuing the quality of friends over quantity (Bauminger et al., 2008). Similarly, when in captivity or when gathering around a large, fertile fruit tree, orangutans can be observed to have social competencies, even if they are not as facile or effusive as chimpanzees.
If autism, in fact evolved, did it do so predominantly among neurotypical humans or within an isolated population of solitary individuals? The autism continuum could represent a remnant of genetic introgression that took place before humans were the only species in our genus. Perhaps some of the genes for autism evolved not in our direct ancestral line but in an isolated subspecies, which later merged genetically with our line of descent through gene flow. Demes or subpopulations of relatively solitary humans adapted to local environmental conditions could have been assimilated into our gene pool after a fair amount of interbreeding following migration. Such solitary subpopulations could have arisen in ecologically or climatologically different geographic regions of Africa during the Plio-Pliestocene.
The evolution of human populations with short stature may shed light on this issue. The pygmy phenotype, characterized by small body size, appears to have evolved independently in South American, African, and Southeast Asian populations in the last 200,000 years. The phenotype is restricted chiefly to rainforest environments and is thought to respond to the selective pressures of living in a tropical rainforest (Migliano, Vinicius & Lahr, 2007). This powerful climatological association has motivated adaptationist hypotheses about how small size would increase reproductive success in a warm, wet environment with dense foliage. Physical anthropologists have hypothesized that short stature may have increased the capacity to cope with one or more of the following: caloric limitations, high temperature, high humidity, extensive forest undergrowth, increased mortality, vitamin deficiencies, or even a combination of these (Migliano, Vinicius & Lahr, 2007). Multiple genetic disruptions of the growth hormone and insulin-like growth factor I pathway are likely to be involved etiologically, but no specific DNA mutations have been uncovered (Cavalli-Sforza, 1986).
It is clear, though, that when pygmies intermarry with non-pygmies, the result is a spectrum; children tend to be intermediate in stature to those of the two parental populations (Cavalli-Sforza, 1986). Pygmy populations show us a few interesting things in the present context: 1. Isolated pockets of humans can remain reproductively insulated for long enough to evolve discrepant ecological strategies; 2. Such populations can quickly (less than 40,000 years in the South American and Asian pygmies (Cavalli-Sforza, 1986)) develop features that vary markedly from the norm; 3. These traits can involve multiple genes at different loci; and 4. Interbreeding can result in either continuous or polymorphic variation in subsequent generations. Interestingly, as these indigenous people become assimilated into other gene pools, the genes for short stature will persist. They may affect phenotypic variability in sporadic and unpredictable ways for a long time.
The genes that make up a polygenic trait usually have different natural histories. They appeared as mutations at different periods and were selected at different times. For example, several different genes, each working through different molecular mechanisms, helped Europeans develop lighter skin as they moved to higher latitudes over the last 60,000 years. Interestingly, an entirely different set of alleles with unique cellular properties helped people in northern Asia develop lighter skin (Norton et al., 2007). Few of these genes have been selected to fixation, and they occur together in different proportions, creating much variability in skin color even within isolated populations. The genes for autism may be similar to these examples because each gene may have a different natural history. Some genes may have been meant to work cooperatively, whereas others not. Each gene predisposing toward autism may represent a different way to make an organism less reliant on sociality.
Like other polygenic, continuous traits, the mutations responsible for autism could have been maintained by “environmental heterogeneity,” a form of balancing selection. In other words, the genes responsible for autism may have remained in our gene pool because as social-environmental conditions fluctuated in the past, discrepant genetic polymorphisms or “multiple alternate alleles” were favored. Currently, it is not possible to scrutinize the natural history of autism genes at this level of analysis because even though over a dozen genes have been implicated, including an oxytocin receptor, a serotonin transporter, and putative language genes, very little agreement exists in the literature over the specifics (Cantor, 2009).
It is currently not possible to tell whether the frequencies of genetic variants responsible for autism are high enough, or in the right proportions, to accommodate a model of past positive selection. The contributions of many relatively rare genes and de novo mutations (Abrahams & Geschwind, 2008) tell us that autism may not have been subject to natural selection for thousands of years and that it may have a large non-evolutionary component as well as an irregular evolutionary signature. The present chapter cannot fully address this issue primarily because of the lack of knowledge about the genetics of autism. It is unclear whether autism can be explained better by rare mutations or combinations of common genetic variants (Muhle, Trentacoste & Rapin, 2004). Future linkage and association studies, though may be able to resolve whether the responsible genes are mutated sequences encoding aberrant gene products or normal polymorphisms acting synergistically (Kumar & Christian, 2009).
It is also clear that a certain proportion of the clinical picture of autism is not representative of adaptation. Some cases of autism are associated with congenital anomalies and physical stigmata that were probably not adaptive. How and why rare comorbidities such as Rett syndrome, tuberous sclerosis, fragile X syndrome, psychomotor epilepsy, and other clinical entities can present with autism is far from apparent (Amaral, Schumann & Nordahl, 2008). It may be the case that several pathological conditions present symptoms that resemble autism (or exacerbate autism). Thus clinicians and epidemiologists have grouped them with autism, obscuring its natural visage and the elements of it that could have been adaptive. This is undoubtedly the case with ADHD and schizophrenia. Many of these unknowns will not become clear until additional genetic, molecular, and pathophysiological research is done.
Another significant criticism of the present argument is that there may be no clearly documented anthropological evidence for solitary foraging in modern humans. This should not be a massive blow to the present hypothesis given that there do not seem to be documented examples of autistic individuals in hunter-gatherer groups either. No one has looked for these things systematically. However, we should expect the prevalence of autism in forager groups to be equivalent to that in the rest of the world, given that epidemiologic studies indicate that environmental factors, such as perinatal insults, prenatal infections, teratogens, and toxins (factors that may be particular to modern life) account for only very few cases of autism (Amaral, Schumann & Nordahl, 2008). In modern society and throughout history, it is apparent that many people intentionally sequester themselves or prefer solitude to different degrees. It is reasonable to expect that this behavior would have existed in the ancestral past and could have been continuous with the autism spectrum.
Even though there seems to be no academic literature on solitary foraging in humans, it is clear that when food is scarce, hunting parties have been seen to disperse for solitary hunting and reconvene at later times (Hill & Kaplan, 1993; Jochim, 1988). When food is not abundant and nutritional intake is low, the optimal foraging strategy is to lower population size and density (Belovsky, 1988). As with other apes, submarginal or impoverished habitats cannot support large groups of humans, and group size diminishes under these circumstances (Mandryk, 1993).
Several substantiated cases of abandoned youths, known as feral or wild children, have survived to adulthood in the wild (Brothers, 1990). Far more children were probably orphaned in the wilderness in ancestral times, which may have contributed to the selective pressures for asocial temperament. Feral children usually have many autistic features in the sense that they are emotionally detached, prefer solitude, and eschew physical contact (Brothers, 1990). These features may constitute protective, adaptive responses to a solitary life, and their resemblance to the symptoms of autism may not be coincidental.
A consistent, predictable proportion of ancestral humans (and ancestral hominins) must have been forced to live alone. From these individuals, the ones with mutations that created disruptive abnormalities in social brain regions may have experienced increased reproductive success. This should not sound like a stretch, considering that this general pattern may have already occurred during the evolution of orangutans. It appears that from the consistency of orangutan behavior in and out of the wild, their solitary tendencies may be instinctual and innate and that selective pressures acted upon their brain. This indicates that it should be informative for autism researchers to compare the brain areas responsible for social cognition across apes.
The Autistic Brain and the Brains of Solitary Mammals
The brain abnormalities in autism do not seem to constitute indiscriminate pathological abnormalities as one might expect if autism were simply a disease. The most conspicuous brain abnormalities seem to consistently and systematically affect the areas of the brain that have been associated with social cognition (Adolfs, 2001). The amygdala, the anterior cingulate cortex, the orbito and medial frontal cortex, and the mirror neuron system have all been strongly associated with social cognition (Dapretto, Davies & Pfeifer, 2006) and also are the same areas that exhibit prominent anomalies in autism (Williams et al., 2001). This selectivity makes it seem that the genes that influence social areas of the brain were affected, and the others were spared (consonant with Baron-Cohen’s psychological theories of autism). According to Gelman and Williams (1998), brains have been evolutionarily organized to acquire and store particular sorts of relevant information and disregard other irrelevant information. In this context, individuals along the autistic spectrum appear to have a neurological propensity to gate out social information and thus gain conscious access to highly processed nonsocial perceptions and schemata. This section will examine how this might be accomplished by focusing on eye contact, facial expression, oxytocin regulation, macrocephaly, amygdala reactivity, and facial recognition in autism.
Studies have shown that autistic individuals are less expressive, especially with respect to facial communication. They make fewer facial expressions and are rated as more flat or neutral in affect by observers (Yirmija et al., 1989). This absence of facial responsiveness is probably due to underlying neuronal mechanisms, and there is evidence that the facial motor nucleus is significantly reduced in size in autism (Rodier et al., 1996). Fascinatingly, the size of the facial motor nucleus is thought to vary predictably in total volume as a function of group size in monkeys and apes. The larger the average group size, the more crucial facial expressiveness is, and the larger the facial motor nucleus must be (Sherwood, 2005). It should be informative to analyze the anatomical organization of the autistic facial motor nucleus taking note of the general size, the placement of motor neurons, the distribution of neuron types, and the general topography of muscle representation. Experts in neurological/phylogenetic specialization might be able to perceive social or ecological traits in the distinctive anatomical organization of the facial motor nucleus in autism. Analyzing it relative to the orangutan facial motor nucleus should also be informative, as it is known that orangutans are much less facially expressive than other apes (Liebal, Pika & Tomasello, 2006).
Oxytocin, a neuropeptide thought to enhance social learning, social expressiveness, direct eye gaze, and the ability to remember faces (Scaskan et al., 2008), is reduced in autism subjects. Diminished peripheral oxytocin levels may play a prominent role in retuning social brain modules in autism (Green et al., 2001). It has been shown that intravenous oxytocin significantly reduces stereotypic behaviors in adult autism subjects and increases empathy in people without autism (Hollander et al., 2003). Variation in oxytocin levels in mammals reflects adaptations to the social environment, just as it may in the case of autism. Animals that rely on pair bonds and social attachment have higher plasma oxytocin levels, especially when it is behaviorally relevant, like during childbirth or monogamous sex (Campbell, 2007).
Comparing prairie voles to montane voles, two very closely related rodent species is interesting in this context because the two differ widely in bonding behavior. The montane vole, relative to the prairie vole, has a much smaller number of receptors in the brain for oxytocin, and unlike the amorous prairie voles, they do not form pair bonds (Marler, 1968). The montane voles have fewer receptors and thus are less responsive to oxytocin, making them warier, suspicious, and more easily frightened of other members of their species. This ensures that they do not allow themselves to become vulnerable (Marler, 1968). It is thought that the wide discrepancy in social behavior between these two species reflects adaptation to two very different physical and social environments (Adolfs, 2001). Not surprisingly, interspecific, seasonal, and reproductive variations in oxytocin concentrations have been attributed ecological and adaptive significance. High levels are associated with trust, love, pair bonding, and generosity in various mammals (Adolfs, 2001). It would be interesting to compare the details of oxytocin action- such as receptor number and distribution- in solitary animals with that of people with autism.
Diminished peripheral levels of oxytocin may cause individuals with autism to be born “expecting” or prepared for a socially impoverished environment. Natural selection cannot act on behavior directly but instead acts on the neural substrates that generate the psychological mechanisms that create the behavior. Evolved psychological mechanisms, such as cognitive modules, are generally understood in terms of specific inputs, decision rules, and outputs (Buss, 1995). Most of these mechanisms were naturally selected to be sensitive to a narrow range of perceptual information. In other words, they are biologically prepared to learn about or solve particular adaptive problems. Some mechanisms are known to be domain-specific, and many of these are assumed to exhibit variation in humans causing some people to attend to perceptual cues that others might miss entirely. Tuning differences in domain-specific mechanisms or modules, especially those involving oxytocin, serotonin, and adrenaline, may underlie differences in autistic cognition and, like other differences seen in nature, may have been created by natural selection to help solitary foragers face their particular set of recurrent or ecologically relevant threats and opportunities.
It has been shown that one or both hippocampi are often significantly larger in autism (Amaral, Schumann & Nordahl, 2008). The hippocampus is a convergence zone integral to spatial ability, and perhaps the large hippocampus in autism has neuroecological relevance. The study of neuroecology focuses heavily on the relationships between ecological hardships, the necessity for spatial ability, and the size of the hippocampus (Garamszegi & Eens, 2004). It might make sense that a solitary forager would have to compensate for the fact that it could not rely on the spatial abilities of its companions. Individuals with autism have also been shown to excel at the block design subtest of the Wechsler intelligence scales, evidence of high visuospatial abilities (Bolte, Dziobek & Poustka, 2009). It may be possible that such abilities are indicative of the visuospatial or mnemonic rigors particular to a solitary existence.
Brain growth is accelerated in early autism, which may have been adaptive for a youngster preparing to become a solitary forager. Individuals with autism have been known for years to exhibit increased head circumference and increased brain size (two highly correlated traits) during infancy (Dementieva et al., 2005). Macrocephaly (head circumference higher than the 97th percentile), one of the most consistently encountered traits seen in autism, is known to affect between 14% and 34% of all autistic infants (Fidler, Bailey & Smalley, 2000). As revealed by MRI, total brain size is, on average, 5-10% bigger in autism between 18 and 48 months of age (Mraz et al., 2007). Neonates who will develop autism and macrocephaly exhibit normal head circumference at birth, but their head growth accelerates during the first year of life. This growth continues until at least four years of age, slows, and then decelerates prematurely (Dementieva et al., 2005). This increased brain maturation and growth rate slows early, well before nonautistic brains start to slow, resulting in very similar head sizes between those with autism and those without in both adolescence and adulthood (Fidler, Bailey, & Smalley, 2000).
A large contributor to increased brain size in youth is myelination, and it is thought that different areas of the brain myelinate differentially according to an ecological program seen in all mammals where primary sensory areas begin to myelinate first well before association cortices. The dramatic increase in head circumference from birth until four may be evidence that the learning arc for a solitary forager is not as protracted as it is for other children. Hunter-gatherer children need to laboriously learn a language along with social customs. This is a time-consuming process (Kaplan et al., 2000). Researchers have concluded that learning during human childhood takes so long because social interactions are more variable and relatively less frequent than other forms of ecological learning (Greenough, Black & Wallace, 1987). The fact that individuals with autism show this increase in head and brain size between birth and age four may indicate that they are programmed to learn more about their environment, faster, at an earlier age. This may also suggest that autism represents a precocial (“out of the nest early”) strategy where learning takes place very early so that the animal can become independent of its mother quickly, a characteristic observed in countless precocial animals that do not have complex social lives. Consistent with this conclusion are data evincing that many males with autism exhibit precocious puberty (Tordjman, 1997), further evidence of a precocial as opposed to an altricial strategy.
Other neurological differences particular to autism may hold neuroecological significance. Individuals with autism have been widely reported to have increased fear activity in the amygdale and high levels of anxiety (Baron-Cohen et al., 2000), which might act to increase vigilance, caution, and a healthy fear of strangers. It seems reasonable to assume that a solitary forager would benefit more from such caution than an individual who must learn to embrace companions. Some frequently reported but only preliminarily researched eccentricities in autism include acute and perceptive hearing and increased frequency of, and interest in, smelling (Leekam et al., 2007), two features that could indeed be interpreted in a neuroethological context. Face processing, a key factor in the development of social perception, is severely impaired in autism (Dalton et al., 2005). The area responsible for face recognition, the fusiform face area, in particular, has demonstrated reduced activation in autism during facial discrimination tasks (Pierce & Redcay, 2008), indicating that in autism, like in many solitary animal species, identity recognition may not be as valuable. These neurological differences may be telling. If autism truly does represent a solitary phenotype, then the brain abnormalities -which are highly consistent across individuals on the spectrum- should furnish theoretically intriguing insights, not only into comparative cognition but also into human evolution.
Implications of the Solitary Forager Hypothesis
This chapter has attempted, in an exploratory manner, to provide a characterization of autism that reconciles known findings with evolutionary theory. In the past, it was not understood how individuals on the autism spectrum might have gotten along during prehistoric times. Yet now, a comparison with solitary species shows that autistic individuals may have mainly lived solitary lives and still have achieved self-sufficiency and reproductive success.
Characteristics of autism that have been interpreted as consistent with the solitary forager hypothesis include the high systemizing abilities, obsessive and perseverative tendencies, repetitious and ritualistic tendencies, splinter skills, deep but narrow stores of knowledge, the parallels with orangutans and montane voles, gaze aversion, absence of eye contact, increased hippocampal size, macrocephaly, precocious puberty, the testosterone effect, reduced fusiform face area and facial motor nucleus activity, reduced oxytocin concentrations and the sex ratio.
Clearly, there are exceptions to each line of evidence offered here. For instance, there are innumerable functional differences between the social mind of an orangutan and that of the average individual with autism. The growing body of experimental literature testing the social-cognitive skills of solitary species may offer important insight into autistic traits and tell us more about the similarities and differences in these domains. It will be challenging to determine irrefutably if what we know as autism today was an adaptive phenotype in the ancestral past and the hypothesis presented here is underspecified and vague. However, the evolutionary perspectives delineated here could potentially provide structure for empirical investigations in animal behavior or cognitive neuroscience.
The case that the autism spectrum represents a solitary forager phenotype is a very top-heavy argument that can and probably should be toned down in numerous ways. First, individuals with autism were probably not totally solitary and may even have been better adapted to very small groups than to a purely solitary existence. Second, it should be emphasized that natural selection may have only been selecting for subclinical autistic traits and that the high-functioning corner of the spectrum was the substrate for natural selection. Third, the most severe cases of autism may have been maladaptive and due to the assortative mating of two individuals that hold a high number of autism susceptibility genes.
A comprehensive solitary forager theory of autism must address these issues and should start by partitioning variation in autism into nosological categories that represent either pathology or nature. This chapter has not clearly committed to delineating which aspects of autism are adaptive and which are not, or even committed to whether the lowest functioning forms could have had a place in nature. It is probably too early to make these discriminations. However, it seems that if the extreme end of the autism spectrum was selected for, that the distribution of autism prevalence relative to severity might be bimodal or have a fattened tail yet this does not seem to be the case.
Other endophenotypes and genetic patterns in autism can probably be analyzed in terms of the present hypothesis to provide convergent evidence. Eventually, genetic hypothesis testing could provide near incontrovertible proof for the present hypothesis. Until then, comparing intron relative to exon mutations in susceptibility genes for autism, mapping gene linkages, analyzing epigenetic patterns, scrutinizing genome-wide microarray analyses, and even looking for inter and intraspecific trends in genographic data may all provide further support.
Further comparative behavioral studies may also be revealing. It will be instructive to look for abilities in autism that more closely resemble foraging activities than the abilities mentioned here. Conversely, we should look for anthropological evidence for autism-like traits among successful foragers. It is also important to question whether the processing deficits in autism might have put a solitary forager at a disadvantage.
To further explicate the evolutionary roots of autism and draw new inferences with the potential to inform medical intervention. I encourage researchers to turn to ethology and Niko Tinbergen’s (1963) “four questions” in understanding the value of behavior: 1) what is the immediate benefit to the organism? 2) What is the immediate consequence? 3) How does it develop in the individual across ontogeny? 4) How did it evolve in species across phylogeny? Knowledge about the costs and benefits of solitary existence may help to guide each of these lines of research.
Oliver Sacks (1970) has formulated an interesting view of autism that appears to be consistent with this. He points out that the perspective of the autistic individual appears aboriginal because they never succumb to our modern societal conventions, but that this does not keep them from perceiving, thinking, and behaving in original, innovative and intelligent ways:
“The autistic by their nature are seldom open to influence. It is their ‘fate’ to be isolated and thus original. Their ‘vision’, if it can be glimpsed, comes from within and appears aboriginal. They seem to me, as I see more of them, to be a strange species in our midst, odd, original, wholly inwardly directed, unlike others (Sacks, 1970).”
Even Hans Asperger wrote about his impression that autism has certain compensating aspects. He noticed a “particular originality of thought and experience which may well lead to exceptional achievements later in life.” In his early writings he called his autistic patients, ‘little professors.’
Studies in behavioral genetics have demonstrated that tendencies for cooperation, temperament, and sociality have biological underpinnings. Furthermore, they show considerable variability within and between animal species (Frank, 1998). Tendencies for independence, reclusiveness, introversion, and other traits characteristic of autism certainly show a great deal of variability between species (Trivers, 1985), but what about within them? Perhaps populations of other social species, such as chimpanzees, have an equally low but consistent prevalence of autistic individuals.
No formal diagnostic criteria are available for psychiatric or even social disabilities in other animals (Wilner, 1991). However, it would be interesting, although difficult, to see if there are analogs or possibly homologs of autism in other species. If there were homologs of autism in species closely related to humans, it would be relatively easy to use molecular techniques to show this, given that the genes responsible could be identified. Looking at the evolutionary signatures in the behavioral genetics of autism might tell us more about our ancestors’ variability in life-history strategies. Many different factors could be invoked in such a discussion, including behavioral neuroscience, cognitive primatology, the importance of group membership to survival, fission-fusion sociality, mating strategies, maverick males, paleoneurology, parenting methods, phenotypic plasticity, sexual selection, social and affective neuroscience, pair bonds, territoriality, social hierarchy, and others.
“Because humans are highly social, we like to think that complex societies represent the crowning achievement of evolution.… Indeed, if group living were the universally superior lifestyle, we would expect social species to outnumber solitary ones, but exactly the opposite is true. Why? Almost certainly because in many environments, the costs of living with others are prohibitively high (Alcock, 2001).”
Humans are an innately social and gregarious species. Like that of chimpanzees, their ancestral environment selected them to be this way (Foley & Gamble, 2009). It is probable that, as with all traits selected for by evolution, there are costs and benefits associated with social predispositions and that the considerable variation in sociability in our species reflects the large variability in selective forces in the past. The relative prevalence of autism is high enough to suggest that it was a phenotype that was naturally selected for but also low enough to suggest that it was rarely preferable to the socially typical alternative.
Perhaps the prevalence of the autism spectrum in modern human populations tells us something profound about the frequency of forced solitude in ancestral times, the adaptive value of social instincts, and the plasticity of human cognitive strategies. Showing that autism had ecological viability and that it exists today because of its success in the past suggests that it should not be considered a disease but a condition. It should not be thought of as something to be ashamed of but as something representing individuality, self-determination, and autonomy.
Individuals with autism, even pronounce autism, are capable of forming lasting monogamous pair bonds as millions of people have witnessed on Netflix’s love on the spectrum.
There are cases of identical, twins where one has autism, and one does not which shows that it is epigenetic. Or at least that there are epigenetic factors.
Simon Baron Cohen has the systemizing mechanism. If and then. Or. Input, operation, output. It, finds confirms and experiments with patterns. If I take a tomato seed and planted in the moist soil, then I get a tomato plant. if I attach an arrow to a stretchy fiber and release the tension in the fiber, then the air will fly. If I take a plow, and I harness it to my arcs, then the plow will move. He maintains that anecdotally a lot of inventors seem to have artistic traits. People who work in stem have more autistic traits. How does society treat Nuro diverse people. Many of them are unemployed and struggle with depression and anxiety, which is partially a result of not getting the right support and being excluded. society should have an obligation to make sure that no one is left out.
Now, one in 48 males has autism. Kids with autism often do better than normal on mechanical reasoning problems. Systemizing is trying to understand lawful relationships between variables.
The term Asperger’s is now outdated and has been replaced by autism spectrum disorder.
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Chapter 10: Technical Comparisons Between Autism and Solitary Mammals
Solitary Mammals Provide an Animal Model for Autism Spectrum Disorders
Grammarly
Chapter Summary
Species of solitary mammals exhibit specialized neurological adaptations that prepare them to focus working memory on food procurement and survival rather than on social interaction. Solitary and nonmonogamous mammals that do not form strong social bonds have been documented to exhibit behaviors and biomarkers that are similar to endophenotypes in autism. Both individuals on the autism spectrum and certain solitary mammals have been reported to be low on measures of affiliative need, bodily expressiveness, bonding and attachment, direct and shared gazing, emotional engagement, conspecific recognition, partner preference, separation distress, and social approach behavior. Solitary mammals also exhibit specific biomarkers characteristic of autism, including diminished oxytocin and vasopressin signaling, dysregulation of the endogenous opioid system, increased HPA activity during social encounters, and reduced HPA activity to separation and isolation. The extent of these similarities suggests that solitary mammals may offer a valuable model of autism spectrum disorders and an opportunity to investigate genetic, epigenetic, and etiological factors. If the brain in autism can be shown to exhibit distinct homologous or homoplastic similarities to the brains of solitary animals, it will reveal that they may be central to the phenotype and should be targeted for further investigation. Research into the neurological, cellular, and molecular basis of these specializations in other mammals may provide insight into behavioral analysis, communication intervention, and psychopharmacology for autism.
Animals Models and Solitary Mammals
Animal models of disease are used to better understand disease processes. Well-defined animal models that can recapitulate core symptoms of autism are essential for research into the nature of the neurological aberrations. Currently, mouse models are the most widely utilized. Rodent models of autism typically involve mice with specific lesions, mice that are genetically engineered to carry certain genes or panels of inbred mouse strains. Some mouse models of autism are capable of reflecting disease symptoms such as impaired social interaction, communication deficits, and repetitive behaviors. Large-scale datasets and biobanks have linked multiple genes to autism spectrum disorders, and genetic linkage and association studies in humans have begun to inform the design of mouse models.
Genetically modified mice with deletions, truncations, and overexpression of these autism candidate genes have helped to model the disorder (Moy & Nadler, 2008). However, the rodents used for these models are primarily social animals that are engineered to have symptoms characteristic of social deficits. The present chapter emphasizes the potential importance of naturally occurring phenotypes found in solitary species in modeling autism. There is an extensive knowledgebase in zoology and behavioral neuroscience of naturally existing variation in social capacities found between mammalian species that can be harnessed as a tool to inform the development of future animal models and to provide insight into the biology of autism.
Most animals, many mammals, and several species of primates are solitary (Alcock, 2001). Solitary species are known to have specialized behavioral adaptations that prepare them mentally to live alone (Decety, 2011). These behavioral adaptations have been shown to have neural underpinnings (Young, 2009). Adjustments to social neural circuits and associated neurotransmitters, neuromodulators, and their receptors fine-tune solitary animals to direct cognition toward foraging and self-preservation rather than on interaction with members of their species (Alcock, 2001). Not all solitary mammals exhibit the same suite of adjustments. This is because individual species respond to diverse social concerns particular to their unique environments. There does, however, seem to be a large amount of convergence in many of these adjustments (Adolfs, 2001). Social neuroscientists have begun to elucidate specific neurological pathways that underlie specializations involved in prosocial behavior, attachment, and bonding. Researchers are also beginning to compare the pathways found in social animals with those in solitary animals (Shapiro & Insel, 1990), and identify traits that correlate with group size and social necessity (Dunbar, 1988; 1998). Even though this research is in its nascent stages and the pathways involved are currently not well-resolved, continued experimental research may have important implications for autism spectrum disorders (ASD) because individuals on the autism spectrum share a variety of traits with solitary species (Reser, 2011a; 2011b). To promote this comparative approach, the present chapter will review literature that points to comparable traits.
Our understanding of the “social nervous system” has been driven by studies analyzing specific biological markers in species that parent, species that are socially monogamous, species capable of developing extended families, and those capable of selective social camaraderie (Porges & Carter, 2010). Comparisons of the species-typical mating and affiliative strategies between the socially monogamous prairie vole (Microtus ochrogaster) and the closely related but nonmonogamous (promiscuous or polygamous) montane vole (Microtus montanus), have served as the primary model for the mapping of the neurocircuitry of social behavior in mammals (Carter et al., 1995). These voles have been closely studied and exhibit divergent traits in the neuroscience of bonding and attachment. These and other closely related but socially discrepant species pairs will be discussed to build a comparative paradigm.
Individuals on the autism spectrum exhibit behaviors and biological markers common in solitary and nonmonogamous mammals (Reser, 2011). Both solitary mammals and autistic individuals have been reported to demonstrate lower measures of affiliative need, bodily expressiveness, bonding and attachment, conspecific recognition, emotional engagement, gregariousness, partner preference, separation distress, and social approach behavior. Individuals with autism also exhibit specific biological markers that are characteristic of solitary mammals, including diminished oxytocin and vasopressin action, dysregulation of the endogenous opioid system, increased HPA activity to social events, and reduced HPA activity to separation owing to anomalies in vagal tone and parasympathetic response. See Tables 1 and 2 below for matched comparisons between A) neurotypical humans and humans with autism; and B) the nonmonogamous montane vole and the monogamous prairie vole. Are the similarities in these shared behaviors sufficient to warrant the pursuit of a solitary mammal model of autism? Before this question can be answered, these purported similarities must be investigated in various species with differing bonding and attachment strategies.
| Behavioral Predispositions in Autism and Montane Voles | ||
| Reduced Behaviors | Humans with Autism Relative to Those Without | Montane Voles Relative to Prairie Voles |
| Affiliative need, gregariousness, and social approach | (Mundy, 1995; Emre et al., 2009; Baron-Cohen et al., 2000) | (Lim et al., 2004; Shapiro & Insel, 1990) |
| Bodily expressiveness and communicativeness | (Yirmija et al., 1989; Begeer et al., 2009; Peppe, 2007) | (Marler, 1968; Hammock and Young, 2006) |
| Bonding and attachment | (Sigman & Ungerer, 1984; Rutgers et al., 2004) | (Marler, 1968; Hammock and Young, 2006) |
| Conspecific recognition | (Dalton et al., 2005; Pierce & Redcay, 2008) | (Lim et al., 2004; Young, 2002) |
| Social preference | (Buitelaar, 1995; Depue & Morrone-Strupinsky, 2005) | (Lim et al., 2004; Young, 2009) |
Table 1
| Neurological Findings in Autism and Montane Voles | ||
| Presentations | Humans with Autism Relative to Those Without | Montane Relative to Prairie Voles |
| Reduced action of oxytocin and vasopressin | (Green et al., 2001; Hollander et al., 2003) | (Marler, 1968; Shapiro and Insel, 1990) |
| Dysregulation of the endogenous opioid system | (Gilberg, 1995; Machin & Dunbar, 2011) | (Shapiro et al., 1989) |
| Anomalies in vagal tone and parasympathetic response | (Porges & Carter, 2010; Porges, 2005) | (Grippo et al., 2007; 2008; Shapiro & Insel, 2004) |
| HPA hyperactivity in social situations | (Baron-Cohen et al., 2000; Sahley & Panksepp, 1986) | (Shapiro and Insel, 1990; Hammock and Young, 2006) |
Table 2
There are currently no animal models that reflect the entire range of behavioral and neurological phenotypes in autism; however, some researchers have advised that studies into the neurobiology of normal social cognition may provide clarification for understanding the mechanisms responsible for autism (Hammock & Young, 2006). This chapter extends this argument, advising that studies into the neurobiology of solitary cognition may provide further insight and clarification. Regardless of whether the similarities between the brains of solitary/nonmonogamous mammals and individuals on the autism spectrum are coincidental or are partly due to adaptive convergence to similar ecological demands (as proposed and outlined in Reser, 2011a), they may help to elucidate the neurobiological and molecular underpinnings of ASD.
Hammock and Young (2006) posit that:
“Basic research into ethologically relevant behavior of the prairie vole has allowed us to gain insight into some of the underlying neural and genetic mechanisms of social-bonding behavior in mammals. Humans may share some of these mechanisms and when these mechanisms are disrupted, either by genetic, environmental or interactive causes, extreme phenotypes such as autism may be revealed. These studies illustrate the power of the comparative neuroethological approach for understanding human neurobiology and suggest that examining the neurobiological bases of complex social behavior in divergent species is a valuable approach to gaining insights into human pathologies.”
The Behavior of Solitary Mammals
Some animal species are obligately social, some are obligately solitary, and others are facultatively social and can transition between social and solitary lifestyles. Species that are obligately social form groups even under very low population densities (Bothman & Walker, 1999). In contrast, some species, like whistling rats (Paratomys brantsii) maintain solitary living even under very high population densities (Jackson, 1999). Obligate solitary living is rare in birds, but common in mammals, reptiles, amphibians, and invertebrates.
Among the many mammals categorized as solitary are well-known animals such as armadillos, opossums, orangutans, red pandas, red squirrels, Tasmanian devils, wolverines, as well as most bears, cougars, tigers, and skunks. See Table 3 below for a more extensive list that includes a diverse assortment of mammals from orders, including: primates, lagomorpha, rodentia, carnivora, ominidaet, artiodactyla, perissodactyla, soricomorpha, xenarthra, and also marsupials and monotremes.
| Abridged List of Solitary Mammals | |
| Armadillo, Baikal seal, Bamboo rat, Bear, Black Rhinoceros, Black-footed Cat, Blind mole rat, Brown-throated Sloth, Bushbuck, Bushy-tailed Opossum, Clouded Leopard, Coast Mole, Cougar, Dusky-Footed Woodrat, Eastern Pygmy Possum, European Mink, European Polecat, Fishing Cat, Four-horned Antelope, Four-toed Hedgehog, Giant Anteater, Grizzly bear, Hog-nosed skunk, Honey Badger, Jaguar, Japanese Hare, Javan Rhinoceros, Lemming Leopard, Maned Sloth, Marbled Polecat, Marten, Mountain Weasel, Montane Vole, Meadow Vole, Musk deer, Neotropical Otter, Northern Bettong, Opossum, Orangutan, Paca, Philippine Mouse-deer, Philippine Tarsier, Polar bear, Pudú, Red Brocket, Red Panda, Red Squirrel, Rhinoceros, Ringed seal, Scaly-tailed Possum, Short-beaked Echidna, Siberian chipmunk, Skunk, Solenodon, Southern Tamandua, Spotted skunk, Steppe Polecat, Striped Hog-nosed Skunk, Striped Polecat, Sumatran Rhinoceros, Tapeti, Tasmanian Devil, Tiger, Vagrant Shrew, Water deer, Zokor | |
Table 3
Sociality is the extent to which members of an animal species tend to associate in social groups (gregariousness) and form cooperative societies. Table 4 below describes some of the forms of sociality recognized by animal behavior experts.
| Types of Sociality in Animals | |||||
| Asocial | Subsocial | Solitary-But-Social | Parasocial | Eusocial | |
| Only socializes during courtship and mating | Cares for its young but shows no other sociality traits | Cares for young, adults forage separately but may sleep together | Cares for young, and adults socialize in a communal dwelling | Overlapping adult generations, cooperative care of young, and division of labor (i.e., ants, bees, and wasps) | |
Table 4
Behavioral genetics has demonstrated that both social and asocial tendencies have genetic and neural underpinnings (Trivers, 1985). Furthermore, these traits can show considerable variability between and within animal species (Frank, 1998). Significant variation within species in social propensities has been observed in more than a hundred vertebrate species (Lott, 1991). It is unclear if the variation within species is due to genetic differences between individuals, differential responses to environmental circumstances, or gene-environment interactions. Likewise, it is not clear why there might be variation in social propensities and abilities within our own species (Baron-Cohen, 1995). However, it is thought that much variation between species is genetic.
Perhaps both intra and interspecific diversity can be utilized to investigate the autism spectrum; however, the data concerning interspecific diversity is currently much stronger. Even closely related species can have vastly divergent social predispositions. In fact, phylogenetic inertia is thought to be strong for general physiology but not for social behavior, i.e., closely related species can have very different social organization if they live in different habitats or eat different foods (Zuk, 2002).
Voles Provide an Animal Model of Autism
Placed together in a large room, several species of rodents, such as nonmonogamous montane voles, are content to be loners and will spread out uniformly, attempting to maximize the distance between themselves and others. Social rodents, like monogamous prairie voles, if placed in the same room, will prefer to huddle together and affiliate in close proximity (Shapiro & Insel, 1990). It is thought that the wide discrepancy in social behavior between these voles reflects adaptation to two very different physical and social environments (Adolfs, 2001). In prairie and pine voles, the males and females form long-term pair bonds, establish a nest site, and rear their offspring together. In contrast, montane and meadow voles do not form pair bonds, and only the females take part in rearing the young. This is true in the wild and in captivity. It is believed that this diversity in behavior is maintained by selection favoring one of two male spatial/paternity strategies: 1) maintain a small home range and actively defend the female that you are monogamous with from other males (breeder); or 2) maximize range by wandering to maximize the rate at which unguarded females are encountered (roamer) (Phelps, 2010).
Nonmonogamous montane and meadow voles do not show partner preferences like prairie and pine voles after experimentally induced pair-bonds are instigated by cohabitation (Lim et al., 2004). This may be likened to the situation in autism, where social bonding and secure attachment behavior are diminished (Sigman & Ungerer, 1984). Pups of the monogamous prairie vole, but not the nonmonogamous montane vole, show a robust stress response to maternal separation along with increased vocalization and increased stress hormone levels (Shapiro & Insel, 1990). This behavioral pattern is highly analogous to the diminished separation distress evident in autistic infants and children. In fact, children with autism show diminished (but existent) preferential proximity seeking and reunion behavior when separated from their mothers under laboratory settings (i.e., Strange Situation Test) (Buitelaar, 1995; Naber et al., 2008).
Because of the animals’ small size and easy maintenance in the laboratory, the neurobiology of the social differences between these two species of vole has been carefully examined. The differences are thought to be primarily governed by the regulation of the neuromodulators oxytocin (OXT) and vasopressin (AVP) (Churchland, 2011). Neuropeptides like oxytocin, vasopressin, and endogenous opioids regulate complex social behaviors (Miller, 2005). Interestingly, the same neuropeptides have been shown to be affected in autism (Gilberg, 1995; Green et al., 2001; Hollander et al., 2003; Machin & Dunbar, 2011). In fact, data suggest that individuals with autism are more likely to have genetic variants of genes necessary for developing parental and affiliative behaviors in other species (especially the genes for the oxytocin and prolactin receptors) (Yrigollen et al., 2008).
It will be interesting to perform further comparative analyses, but it is not completely clear which genes or which brain systems should be interrogated. A relevant model of neurobiological regulation of affiliation in mammals (Depue & Morrone-Strupinsky, 2005) has suggested that dopamine plays an essential role in incentive-reward motivational processes associated with the appetitive phase of affiliation, endogenous opioids are involved in the consummatory phase of socialization, and oxytocin and vasopressin enhance the perception and memory of affiliative stimuli. To make the appropriate comparisons, let us first look at the role of oxytocin signaling in nonmonogamous rodents and in autism.
Oxytocin in Autism and Solitary Mammals
Oxytocin is a peptide hormone and neuromodulator involved in mammalian reproduction, social recognition, and pair bonding. Animal species that rely on pair bonds and social attachment exhibit higher levels of plasma oxytocin, especially when it is behaviorally relevant, like during monogamous sex, childbirth, and lactation (Campbell, 2007). High levels of oxytocin are associated with mating, mating season, continued proximity, trust, and pair bonding in many mammals and these are considered to be adaptive (Adolfs, 2001). Oxytocin can buffer the response to stressors, especially social ones. It is released during positive social interactions and appears to facilitate the capacity for being trusting and socially perceptive (Porges & Carter, 2010). Mice that have had oxytocin knocked out show deficiencies in social recognition, social memory, and the ability to manage emotional reactivity due to stress (Takayanagi et al., 2005; Pederson et al., 2006).
After being synthesized in the hypothalamus, OXT and AVP are released into the extracellular space resulting in both local action and diffusion throughout the brain. OXT and AVP are also sent directly to specific brain areas, including the amygdala, hippocampus, striatum, suprachiasmatic nucleus, bed nucleus of the stria terminalis, and brainstem where they take different actions, depending on the receptors they bind to. It is not clear if the areas that synthesize, process, and distribute OXT and AVP are affected in autism or solitary animals, although this should be a topic of future research. On the other hand, there are significant differences in what brain areas are found to contain oxytocin receptors when comparing monogamous to nonmonogamous mammals.
Prairie voles and montane voles have very different oxytocin receptor profiles. The montane vole, relative to the prairie vole, has a much smaller number of receptors in the brain for oxytocin, and unlike the amorous prairie voles, they do not form pair bonds (Marler, 1968). The montane voles have fewer receptors and thus are less responsive to oxytocin, making them more wary, suspicious, and more easily frightened of other members of their species (Marler, 1968).
When the two are compared, monogamous species have higher densities of oxytocin receptors in the caudate, putamen, amygdala, orbitofrontal cortex, and nucleus accumbens (Hammock & Young, 2006). This may indicate that these brain regions may have fewer receptors in autism and that perhaps treating autism might involve increasing the number of receptors in these areas. The shell region of the nucleus accumbens is especially abundant in oxytocin receptors in socially monogamous species and prairie voles but not in nonmonogamous voles (Insel, 2010). Oxytocin receptor blockers (antagonists) applied directly to the nucleus accumbens of female prairie voles inhibit mating-induced partner preference formation, indicating that activation of oxytocin receptors in this area of the brain is necessary for bonding and attachment (Young et al., 2001).
Other nonmonogamous species such as marmoset monkeys, rhesus monkeys, titi monkeys, the California deer mouse, and the white-footed mouse, have OXT and AVP receptor distributions that are highly similar to that of the montane vole (Bales et al., 2007; Wang et al., 1997). These comparisons suggest that autism research should be focused on the nucleus accumbens and its role in social motivation. It would be interesting to compare the details of oxytocin action, such as receptor type, number, and distribution pattern, in solitary animals with that of people with autism, but again, this research has not been done. The comparable data about receptor density and distribution in humans has not been determined because injection methods to tag receptors cannot be done in living humans for ethical reasons and do not yield results when performed on the brains of cadavers.
Results interpreted as supporting the idea that oxytocin concentrations (in the cerebrospinal fluid (CSF)) are related to species-typical social behavior patterns come from comparisons between bonnet macaques (Macaca radiata) and pigtail macaques (Macaca nemestrina). The bonnet macaques, which have significantly higher levels of oxytocin when laboratory-born than the pigtail macaques, are described as gregarious affiliative and affectively stable, while pigtail macaques are described as socially distant and temperamentally unstable (Rosenblum et al., 2002). Furthermore, the pigtail macaques exhibited elevations in CSF corticotropin releasing factor, elevations of which promote social vigilance in both solitary and territorial mammals. Within a species, the early environment may play a role. When rhesus macaques (Macaca mulatta) are separated from their mothers at birth and reared with peers in a small cage, they develop a wide range of behavioral abnormalities that have been associated with autistic symptoms. These monkeys exhibit low affiliation, high aggression, and high self-directed and repetitive activities. These genetically social monkeys also had a significantly lower concentration of CSF oxytocin (Winslow et al., 2003).
Oxytocin, the neuropeptide thought to enhance social learning, social expressiveness, direct eye gaze, and the ability to remember faces in humans (Savaskan et al., 2008), is reduced in the blood plasma of autism subjects. Diminished circulating levels of oxytocin may play a significant role in retuning multiple social brain modules in autism and increasing fear and avoidance responses to social stimuli (Green et al., 2001). It has been shown that intravenous oxytocin significantly reduces stereotypic behaviors in adult autism subjects and increases empathy and generosity in people without autism (Hollander et al., 2003).
After treatment with intranasally inhaled oxytocin, autistic patients have been reported to exhibit more appropriate social behavior (Andari et al., 2010), increased attention to the eye region of faces (Andari et al., 2010), increased emotion recognition (Guastella et al., 2010), diminished repetitive behavior (Kosfeld et al., 2005), and diminished social fear (Kirsch et al., 2005). Likewise, oxytocin infusions into the brain increase side-by-side contact and decrease aggressive behavior in female prairie voles (Witt et al., 1990), increased social contact in male rats (Witt et al., 1992), and in squirrel monkeys (Winslow & Insel, 1991). While this research is promising, further clinical trials are necessary to demonstrate potential benefits and side effects of oxytocin in the treatment of autism (Bartz & Hollander, 2008).
Humans and all eutherian mammals have only one receptor for oxytocin, OXTR, but humans have several alleles for the receptor, which differ in their binding effectiveness. Individuals homozygous for the “G” allele (which produces the high-affinity receptor), when compared to carriers of the “A” allele, show higher empathy, lower overall stress response, as well as lower prevalence of autism (Rodrigues et al., 2009). Two mutations (single nucleotide polymorphisms in the third intron) of the oxytocin receptor have emerged as candidate genes for autism. In fact, several studies have shown that these versions of the gene were associated with autism (overtransmitted by families to offspring with ASD) (Wu et al., 2005; Wermter et al., 2010). Other genes seem to be involved as well. Recent work on CD38, a transmembrane protein involved in oxytocin secretion in the brain, has shown that several genetic variants of the gene show a significant association with high-functioning autism (Munesue et al., 2010). Although several studies point to the function of the oxytocin receptor (Jacob et al., 2007; Wermter et al., 2009), the underlying problem with oxytocin signaling in autism remains unclear.
Vasopressin in Autism and Solitary Mammals
Arginine vasopressin is a peptide hormone found in most mammals that plays a crucial role in homeostasis and regulating water, glucose, and salts in the blood. Stored in vesicles in the posterior pituitary, most AVP is released into the bloodstream. However, some AVP is released directly into the brain, where it plays a significant role in social behavior and bonding. Humans and all eutherian mammals have three receptors for vasopressin, AVP receptor 1A, AVP receptor 1B, and AVP receptor 2. Experimental studies in several species have indicated that the precise distribution of vasopressin receptors in the brain is associated with species-typical patterns of social behavior. Specifically, there are consistent differences between monogamous and nonmonogamous voles in the distribution of AVP receptors and the distribution of AVP containing axons (Young, 2009).
AVP release during social interaction and mating in prairie voles leads to increased activation of brain areas with high levels of AVP receptors, such as the ventral pallidum. The high density of receptors in the ventral pallidum is also found in the monogamous marmoset, evincing convergent evolution among rodents and primates. Activation of the pallidum, a key area in mammalian reward circuitry, is thought to reinforce affiliative behavior leading to learned partner preferences and the initiation of pair bonding (Pitkow et al., 2001).
In male prairie voles, vasopressin infusions directly into the brain facilitate partner preference formation, and receptor antagonists block it (Winslow et al., 1993). Altering receptor density also makes a difference. Experimentally increasing the vasopressin receptor (V1aR) levels in the ventral pallidum of nonmonogamous meadow voles using the injection of a viral vector directly in the ventral pallidum resulted in the formation of strong partner preferences. Hammock and Young (2006) describe this experiment in the following way: “Therefore, even though these two species diverged long ago, this simple change in the expression of a single gene replicated a hypothetical evolutionary event that may have ultimately led to the development of monogamy.” Thus it is clear that small, easy-to-make changes can result in large psychological differences.
Vasopressin receptors in the lateral septum (which projects directly to the nucleus accumbens) have been shown, by studies using site-specific injections of a V1aR-specific antagonist, to be critical for social recognition in male mice (Bielsky et al., 2005). Further, these authors found that a viral vector causing reexpression of V1aR in the lateral septum of V1aR knockout mice resulted in a complete rescue of social recognition. Knowledge of the role of the ventral pallidum, the lateral septum, and the nucleus accumbens in this circuit offers clues as to where to look and what brain areas to target in autism. In fact, the receptivity of these areas to vasopressin in autism remains undefined. These findings further substantiate the importance of attaining receptor distribution profiles in autism so that specific brain areas and their receptors can be manipulated for therapeutic purposes.
There is also evidence for the role of the gene that codes for the human vasopressin receptor (AVPR1A) in ASD. Fascinatingly, it contains an evolutionary signature (microsatellite repeats) that is also found in voles where its existence is considered to be an example of evolution in action. This evidence comes from genetic studies of the polymorphic microsatellite repeats in the 5’ flanking region of the gene (3,625 base pairs upstream of the transcription start site of AVPR1A). Of these repeats, overtransmission of RS3 and undertransmission of RS1 has been associated with ASD (Yirmiya et al., 2006; Wassink et al., 2004). Fascinatingly, similar microsatellite repeats have also been found in avpr1a in prairie voles and have been viewed as instrumental in regulating social behavior. Some, but not all, studies have found an association of these repeats with social behaviors in voles (Mabry et al., 2011; Hammock & Young, 2005). King (1994) has suggested that the instability of microsatellite sequences serves as a kind of evolutionary tuning knob (King, 1994). Hammock and Young have done extensive experimentation suggesting that the AVPR1A locus may be such a tuning knob while relating their findings to autism (2005).
Endogenous Opioids in Autism and Solitary Mammals
Endogenous opioids are opiate-like peptides that bind to opioid receptors in the nervous system and gastrointestinal tract. In the brain, this binding has a pain-killing (analgesic) effect (like morphine), decreasing the perception of and reaction to pain and increasing pain tolerance. Endogenous opioids are considered heavily involved in social enjoyment (the consummatory phase of affiliation) (Depue & Morrone-Strupinsky, 2005). Their release and action during social intercourse are thought to make social encounters pleasurable and reinforcing. Blockade of endogenous opioid receptors by an opioid antagonist increases the need for social attachment and, therefore, the solicitation of affiliative behavior from social partners (Martel et al., 2004). On the other hand, treatment with nonsedative doses of morphine significantly decreases clinging behavior and grooming solicitations in primates, as well as decreasing grooming performed. Morphine also reduces huddling duration and social activity in prairie voles (Shapiro et al., 1989).
Because low levels of opioids increase seeking affiliative comfort in mammals, and high levels decrease it, it has been suspected that high levels are associated with autism, which seems to be the case (Machin & Dunbar, 2011). Perhaps the presumed high action of opioids in the autistic brain keeps these individuals from seeking social contact, and the presumed absence of phasic opioid release during affiliation keeps social encounters from being rewarding.
In a review on this topic, Sahley and Panksepp (1987) point out that a growing body of evidence points out that: (1) autistic-like symptoms can be induced in animals with the administration of exogenous opioids, (2) human individuals addicted to opiates exhibit autistic-like symptoms, (3) autistic-like symptoms in the severely mentally disabled can be attenuated by opioid blockade, and (4) the many brain areas that have been suggested to be dysfunctional in autism have high concentrations of opioids. These findings suggest that the deficient social bonding in autism might be strengthened by the manipulation of opioid action in the brain.
Autistic children lack the everyday motivation to engage others socially, as indicated by their poor social skills and lack of spontaneous communication. They seem to lack emotional interest in other people, leading to a decreased initiative to affiliate (Sahley & Panksepp, 1986). Autism has been speculated to be associated with higher opioid levels and higher opioid receptor activation, which may underlie the reluctance to engage (Gilberg, 1995), although this has not been clearly demonstrated, and many details remain unclear. Further research into the effects of opioids on social behavior and their role in autism should prove informative. Specific pathways stand out as having promise. Studies in animals indicate that of the different families of opiate receptors, the µ-opiate receptor family seems to be the most directly implicated in regulating social behavior and that the β-endorphin has a high affinity for those receptors.
It is generally thought that interactions between µ-opiate receptors and dopamine neurons in the ventral tegmental area of the hypothalamus produce the experience of reward associated with the appetitive and consummatory phases of social contact (Gilberg, 1995). This pathway should be interrogated by future autism research. Oxytocin and vasopressin also facilitate the effects of endogenous opioids. In rodents, oxytocin neurons in the paraventricular nucleus of the hypothalamus project to the neurons in the arcuate nucleus and temporarily increase the release of opioids there (Csiffary et al., 1992). Endogenous opioids have been shown to play a role in diminishing the release of oxytocin and vasopressin and regulating the hypothalamic pituitary adrenal axis.
There is a close functional relationship between the endogenous opioid and serotonergic systems in the brain. In fact, serotonin pathways modulate both enkephalin and morphine analgesia. Serotonergic input to the hypothalamus via the raphe nuclei may reduce arousal and facilitate opioid-mediated feelings of affiliative gratification (Depue & Morrone-Strupinsky, 2005). Thus, high and dysregulated levels of serotonin observed in autism may also play a role in dampening the need for certain forms of social contact (Anderson, 2005). In fact, the administration of the drug fenfluramine has been shown to lower elevated serotonin levels and partially ameliorate several symptoms in autism (Clineschmidt et al., 1978).
Social network analysis has shown that patterns of grooming and aggressive behavior in rhesus macaques can be partially explained by repeat polymorphisms associated with the serotonin system (Brent et al., 2011). Rhesus macaques that carry a copy of the short allele in the serotonin transporter linked repeat polymorphism direct less attention to the eyes and are less likely to look at a face than a non-face image (Watson et al., 2009). Allelic heterogeneity at the serotonin transporter locus has been similarly implicated in autism as well (Sutcliffe et al., 2005).
Modifications in Amygdalar, Vagus, and Parasympathetic Responses
Highly social animals share with humans the capacity to form long-lasting social relationships and thus provide an opportunity to examine the physiological effects of social isolation. In prairie voles, isolation from a partner for a few days produces behavioral responses that significantly mimic depression and anxiety in humans. The prairie vole, for instance, has an autonomic nervous system that is relatively human-like, with high levels of parasympathetic-vagal activity (Grippo et al., 2007). These animals exhibit decreased heart rate when socializing, but become stressed when socially isolated. Socially isolated prairie voles explore less, become depressed, and are more likely to display immobility in response to a stressor (Grippo et al., 2008), whereas montane voles are not nearly as affected. Like solitary mammals, individuals with autism are less stressed (sympathetically responsive) in response to social separation and isolation (Buitelaar, 1995; Naber et al., 2008).
It is thought that social mammals uniquely have the ability to regulate an autonomic state of calmness while regulating communicative functions, including the musculature of the face and neck necessary to produce prosocial facial expressions, vocalizations, and head gestures (Porges & Carter, 2010). These capacities are limited in autism, suggesting that parasympathetic function may be involved. The primary nerve of the parasympathetic branch of the autonomic nervous system exits the brainstem as the vagus or 10th cranial nerve. This nerve has both motor-efferent and sensory-afferent components. Many of these afferent sensory fibers carry information from the viscera to a brainstem region known as the nucleus tractus solitarius. Stephen Porges (2005) has documented alterations in vagus morphology and parasympathetic tone in autism that are consonant with phenotypes seen in nonsocial species.
He points out that social contact in autism leads to sympathetic activation and fight-flight arousal states that induce a drive to diminish contact or withdraw. Individuals with autism have been widely reported to have increased fear activity in the amygdala and high levels of stress function during social interaction (Baron-Cohen et al., 2000). Autonomic arousal is linked to social stimuli for solitary animals because it is vital that solitary animals protect their foraging space and actively avoid threatening conspecifics. Solitary animals are often territorial and find the presence of another animal in their territory aversive, especially an animal of their own species (Harcourt, 1989).
Modifications in Brain Regions Involved in Social Processing
The brain abnormalities in autism do not seem to constitute indiscriminate pathological abnormalities as one might expect if autism were simply a disease. The most conspicuous brain abnormalities seem to consistently affect the areas of the brain that have been associated with social cognition (Adolfs, 2001). The amygdala, the anterior cingulate cortex, the orbito and medial frontal cortex, and the mirror neuron system have all been strongly associated with social cognition (Dapretto et al., 2006), and also have been shown to be the same areas that exhibit the prominent anomalies in autism (Williams et al., 2001). Unfortunately, despite some promising research (i.e., Bell et al., 2010; Pellis et al., 2006), little is known about the social cortex in mammals, especially solitary ones.
The brain in autism has shown underactivity in nearly every brain region associated with the empathy circuit (Di Martino, 2009). When individuals with autism attempt to make judgments about the intentions, motives, or state of mind of another, they show reduced activity in the dorsomedial prefrontal cortex (dmPFC) (Happe et al., 1996; Wang et al., 2007). When asked to infer emotional state from pictures of people’s faces, they demonstrate underactivity in the frontal operculum (FO), amygdala, and anterior insula (Baron-Cohen & Hammer, 1997; Baron-Cohen et al., 2001). When individuals with autism are asked to rate how they feel after viewing emotionally charged pictures, they show less activity within a number of regions in the empathy circuit, including the dmPFC, the posterior cingulate cortex, and the temporal pole (Silani, 2008).
Not only are areas involved in empathy underactive during empathy tasks, but the dmPFC and ventromedial prefrontal cortex (vmPFC) show atypical baseline activity during rest (Kennedy et al., 2008; Kennedy et al., 2006). In fact, social impairment in autism is correlated positively with the degree of atypical vmPFC response (Lombardo et al., 2007; 2010). The corresponding studies in nonhuman animals have not been performed. However, it might be expected that solitary or nonmonogamous species exhibit the same neuroanatomical irregularities in homologous cortical areas and the motor neuron system. Analogs of the relevant prefrontal areas may not be present in rodents but are in other primates. Limited yet existent empathic abilities have been documented in apes, and cortical regions that correspond to human social cortical regions are thought to be instrumental (Dunbar, 2008; Joffe & Dunbar, 1997; Povinelli, 1994).
It has been suggested that empathizing and systemizing of physical systems are contingent on separate brain modules (Baron-Cohen, 1995). However, both may be made possible by the same architecture for systemizing, namely the pathways involved in working memory. In other words, empathy may involve systemizing another’s perceived mental state using mirror neurons and social schemas. Perhaps social mammals naturally find stimuli from conspecifics captivating and will automatically attempt to systemize this information unless fear sets in first.
Phasic increases in dopamine neurotransmission in the PFC are thought to underlie the ability to internally represent, maintain, and update contextual information about salient external and internal stimuli (Braver & Cohen, 1999). Stimuli that are deemed novel, surprising, or appetitive are given priority. Seamans and Robbins (2010) have proposed that this dopaminergic process regulates the access of salient contextual representations and maintains them online in active memory so that systemization and modeling of these representations can occur.
Perhaps the brains of solitary mammals are fine-tuned to perceive incoming social stimuli as fearful and not appetitive or novel to keep these stimuli from entering working memory. Aberrations in the receptivity of subcortical motivational areas to neurochemicals such as oxytocin and vasopressin are likely to be the prior or proximate causes of altered cognition in autism. These low-level aberrations likely influence and give rise to emergent aberrations in cortical areas, which should be considered the high-level targets for cognitive/behavioral interventions.
Epigenetics, Phenotypic Plasticity, and Autism
Environmental cues encountered early in life are used by the developing organism to fine-tune its body type, above and beyond what its genes have in store for it. As discussed in previous chapters, research in the field of phenotypic plasticity and epigenetics has shown that many organisms demonstrate predictive adaptive responses to environmental stressors (Auld et al., 2010). There are many examples of predictive adaptive responses in nature, and they allow organisms to use specific, early environmental cues to influence their developmental trajectory (Via & Lande, 1985). It may be possible that some social mammals are receptive to specific foreboding environmental cues that give them information about the social environment that they can expect after birth. Cues indicative of social attenuation might be used by developing mammals to alter their social neurochemistry. We have already seen that rats and humans respond similarly to early cues about stress in a behavioral response referred to as “social referencing” (Zhang et al., 2006). This social referencing may program social behaviors not just stress-related ones.
Some mammals have been documented to exhibit adaptive, social flexibility or plasticity to changing social environments. This is called social plasticity, which is the ability to adaptively change the expression of social behavior according to previous experience (Schradin et al., 2011). In mammals, high population density instructs mammals to remain in the place of their birth and to favor group living. On the other hand, reproductive competition, absence of surviving female relatives, high predation pressure, infanticide, and low food availability favor dispersal and solitary living (Schradin et al., 2011; Randall et al., 2005). Ecological constraints in the prevailing environment determine which strategy will contribute the most to evolutionary fitness.
This phenotypic flexibility, in the form of endocrine adjustments, has been documented in the African striped mouse, and it is attributed to epigenetic changes and a broad reaction norm, not to genetics (polymorphism). Ongoing research has shown that specific endocrine changes underlie these proclivities, including higher testosterone, lower prolactin, and lower glucocorticoid levels (Schradin et al., 2011). There are similar findings of social plasticity in fish (Maruska et al., 2019). Interestingly, there is also evidence of aberrations in each of these three hormones in humans with autism. Similar plasticity has been documented in adult male primates. For example, first-time and experienced father marmosets who had spent considerable time carrying infants had more vasopressin V1a receptors in the prefrontal cortex than adult male nonfathers living in similar social conditions (Kozorovitskiy et al., 2006).
Recent research has underscored the large environmental influences in autism. These studies have confirmed that autism is not only driven by genetics but can be strongly associated with particular environmental scenarios. It is known that maternal stress, paternal age, serotonin levels, multiparity and others are risk factors for autism. Could these factors, or some facet of them, offer information to the fetus about the social environment? Are there other cues that the fetus could intercept and respond to that indicate how valuable social cognition has proven to be to their parents? Research has even revealed that autism may be associated with aberrant epigenetic methylation of the oxytocin receptor (Gregory et al., 2009). Autism may be linked with specific environmental cues that are predictive of the quality of the social environment the fetus is “expecting” to be born into.
The questions to ask are: 1) “Could epidemiological factors that predispose to autism, or some facet related to them, offer information to a fetus about the condition of the social environment that its mother is experiencing? 2) Are there other cues that the fetus could intercept and respond to that indicate how valuable social cognition has proven to be to its parents?” This perspective could influence geneticists and epidemiologists to reinterpret the epigenetic contributions to autism, change how they look for environmental effects, and cause them to home in on specific molecular pathways responsible for changes in gene expression.
Solitary Predispositions in Nonhuman Primates
Nonhuman primate models can be preferable to rodent models because primates are more closely related to humans, have complex social structures, rely on vision for social signaling, and have deep homology in brain circuitry mediating the computation of reward sensitivity and social value. On the other hand, they have only infrequently been used to model autism because primates are more expensive to manage than rodents, are not appropriate for invasive studies due to ethical concerns, are “low-throughput” due to much longer gestation times, and are not ideal for gene knock-in/knock-out or optogenetic studies. Primates, and especially apes, are relatively social mammals, but each species can be shown to lie on a spectrum. Nocturnal prosimians, such as mouse lemurs, dwarf lemurs, bushbabies, and lorises, are solitary foragers, do not live in groups, but do exhibit some social networking faculties (Bearder, 1987). Interestingly, these “stem primates” are thought to represent the ancestral pattern of primate social organization (Muller & Thalmann, 2000; Shultz et al., 2011).
Polymorphism in the repetitive microsatellite locus for the vasopressin receptor mentioned above is present in humans and bonobos. Chimpanzees, which are thought to exhibit slightly lower levels of social reciprocity, empathy, and sociosexual bonding relative to bonobos, do not have this microsatellite locus, and Hammock and Young (2005) have suggested that this is reminiscent of the genetic differences between montane and prairie voles at this same locus.
Bonobos are considered more social and easygoing because their foraging territory south of the Congo River is much richer in large fruiting trees than that of chimpanzees north of the Congo. Bonobos have been gathering in friendly groups around stable supplies of fruit for thousands of years. This is why bonobos can live and forage in larger groups and are thought to be more social than chimpanzees (Wrangham, 1986). Thus, reduced foraging competition facilitates social life in bonobos (Wrangham RW, 1986; Hare et al., 2007), and may have resulted in a human-like AVP expression profile. Recall that autism on the other hand, has been strongly associated with a very different AVP expression profile and with overtransmission of specific microsatellite repeats in this same gene (Yirmiya et al., 2006; Wassink et al., 2004).
Pair living is relatively rare in primates, but group living is not. The most common type of social organization in nonhuman primates consists of relatively promiscuous multimale/multifemale social groups, but even though there is no pair bonding, group members bond. There is a paucity of research on this topic though, and the influence of social neuropeptides on primate group structure has been largely neglected. In anthropoid primates, same-sex relationships have much in common with sexual relationships in mammals that form monogamous pairs. They both involve high levels of coordination, behavioral synchronization, and compromise (Machin & Dunbar, 2011), and both involve a central role of oxytocin (Dunbar, 2008). Thus, even though voles provide a strong foundation for social neuroscience, further research into primate social neurochemistry should be highly informative.
Conclusion
This review has attempted, in an exploratory manner, to consider parallels in neurophysiology between ASD and solitary mammals. Preliminary comparative studies juxtaposing the neurobiology of social mammals with that of solitary mammals have been done, but the pertinent comparisons with autism have only begun. Taken as a whole, these studies suggests that basic and translational research into social cognition in solitary mammals, and the brain alterations that underlie it, could lead to advancements in understanding and ultimately treating autism. The pertinent literature also suggests that research into the neurophysiology of solitary mammals may contribute to identifying more specific biomarkers and developing more precise animal models. The similarities noted here may be numerous and fine-grained enough to suggest that they are not superficial or coincidental. The extent to which these animal studies can be directly extrapolated to autism is very unclear, though.
This line of research points to four major dichotomies that might help to model autism, listed in Table 4 below. There is a monogamous/nonmonogamous dichotomy, a group/solitary dichotomy, and a domestic/wild dichotomy. There may also be a relevant female/male dichotomy as well as there is evidence of significant sexual dimorphism in many, if not all, of the neurobiological systems discussed (Hammock & Young, 2006; Baron-Cohen, 2003). The biodiversity underlying these dichotomies should be interrogated from the perspective of comparative psychology.
| Species Whose Social Inclinations can be Meaningfully Compared | ||
| Monogamous vs. Nonmonogamous | Group Adapted vs. Solitary | Domesticated vs. Wild |
| Prairie Voles vs. Montane Voles | Spotted Hyenas vs. Striped Hyenas | Domesticated Dogs vs. Wolves |
| Marten vs. Agouti | Lions vs. Tigers | Domesticated Silver Fox vs. Wild Red Fox |
| California deer mouse vs. white-footed mouse | Pigtail macaque vs. Bonnet macaque | Domesticated Goat vs. Wild Goat |
| Marmoset vs. Rhesus macaque | Chimpanzees vs. Orangutans | Humans vs. Chimps |
| Pine Voles vs. Meadow Voles | Ringtailed lemurs vs. Mongoose lemurs | Chicken vs. Quail |
Table 4
An important question remains: Are the neurobiological mechanisms found in solitary and nonmonogamous mammals sufficient to capture the nuanced social impairments featured in the autism diagnosis? Because of the various genetic and environmental contributions to autism (Cantor, 2009) it is clear that only a fraction of what is known as autism could be accurately modeled by cognitive specializations for solitary living in other mammals. The modern, entity of autism is a mixture of phenotypes with separate causes lumped together by clinicians. A large proportion of it may represent disease that cannot be reliably compared to naturally occurring animal phenotypes. Based on the paucity of basic research and the absence of consensus in the literature, the present line of research necessitates further critical examination, as well as questioning of the structuring assumptions. Ultimately, understanding ASD will probably require synthesis across several different models.
This model, unlike most animal models, does not detail how to alter or program a laboratory animal to mimic aspects of autism. The pronouncements here have not made considerations for immediate application but are much more general and expository. Typically, diseases with discrete, recognized causes, such as Rett syndrome, Down syndrome, and fragile X, are amenable to animal modeling, which may immediately suggest treatment options. Highly polygenic disorders that also involve phenotypic plasticity, and de novo mutations, such as autism, are more challenging to model, and the models are more difficult to assess.
The utility of animal models are commonly assessed using three criteria: (i) face validity (resemblance to human symptoms); (ii) construct validity (similarity to the underlying causes of the disease); and (iii) predictive validity (expected similar responses to treatments). It is currently not possible to meaningfully assess the validity or value of the present model.
Not only could the study of solitary mammals affect the study of autism, but autism research could also help elucidate phenomena in social neuroscience and social psychology. Traits associated with autism, aside from those listed in Tables 1 & 2, should be investigated in a variety of solitary mammals, including joint attention, pretend play, facial expressiveness, communicative intent, empathy, the mirror neuron system, fusiform recognition areas, and other social cortical areas. Also, this research should have implications for understanding other disorders marked by alterations in related social pathways, such as borderline personality disorder, insecure and withdrawn attachment disorders, psychopathy, and William’s syndrome.
Robert Plomin, author of the leading textbook, Behavioral Genetics (2008), writes: “[We predict that] when genes are found for common disorders such as mild mental retardation or learning disabilities, the same genes will be associated with variation throughout the normal distribution of intelligence, including the high end of the distribution (Plomin et al., 2006).” Could something similar be true throughout the normal distribution of sociality, including social deficits, ASDs, and other disorders of bonding, attachment, and empathy?
Convergent evolution is pervasive, and the similarities between autism and solitary animals may extend beyond superficial resemblances. This chapter’s review of comparative evidence supports the hypothesis that some genes associated with the autism spectrum were naturally selected and represent the adaptive benefits of being cognitively suited for solitary foraging. People on the autism spectrum may have been ecologically competent. The chapter suggests that upon independence from their mothers, young individuals on the autism spectrum may have been psychologically predisposed toward a different life-history strategy, common among mammals and even some primates, to hunt and gather primarily on their own. This may have resulted from periodic or geographic disruptions in the efficacy of group foraging in the ancestral past or reduced adaptive value of sociocultural information sharing.
The resulting evolutionary pressures may have driven the selection of genes that created social processing deficits making their bearers resistant to the transference of units of cultural information (memes). Many of the behavioral and cognitive tendencies that autistic individuals exhibit are viewed as adaptations that would have complemented a solitary lifestyle.
Perhaps components of the autism spectrum can be understood in terms of behavioral ecology and evolutionary medicine, but this does not necessarily mean that autism is an ecological anachronism. In other words, autistic people may not be out of place in time. Several scientists and many autism advocacy groups promote the idea that autism has compensatory advantages even in modern society (Grandin & Panek, 2013; Baron Cohen, 2006). Table 5 presents some of these tendencies, their implications for modern individuals, and their implications for prehistoric, solitary foragers.
| Autistic Traits, Then and Now | |||
| Trait or Symptom of Autism | Psychological Consequences | Implications for Moderns | Implications for Solitary Foragers |
| High systemizing ability | A tendency to systematically explore the laws governing nonsocial processes (Baron Cohen, 2003; 2006) | Eccentric or narrow but substantial knowledge and skills (Treffert, 2000) | An impetus guiding the acquisition of food procurement techniques |
| Obsessive, repetitious tendencies | Perseveration in behavior and thought (Piven, 2000) | Repetitious play and need for sameness (Kelly et al., 2008) | Order, structure, and autonomous self-regulation |
| Gaze aversion and absence of shared eye contact | Minimal eye contact and diminished attention to the faces of others (Piven, 2000) | Unfortunate social hurdle (Hutt & Ounsted, 1966) | Instinctually prepared to not focus on eyes or provoke conspecifics |
| Low oxytocin and vasopressin activity | Reduced social interest, learning and expressiveness (Green et al., 2001) | Unfortunately hindered social cognition (Hollander et al., 2003) | Prepared for a socially impoverished environment |
| Anomalies in anterior cingulate cortex, orbito and medial frontal cortex | Reduced social learning, (Adolphs, 2001) | Hindered social cognition, imitation, and empathy (Dapretto et al., 2006) | Decreased reliance on others |
| Amygdala hyperactivity | Potentiation of innate and conditioned fears (Dapretto 2006) | Excessive anxiety and withdrawal from social world (Baron Cohen et al., 2000) | Healthy caution, and fear of unfamiliar conspecifics |
Table 5
The contemporary, postgenomic age allows molecular methods that were practically inconceivable before genome sequencing was possible. The emerging field of “evolutionary cognitive genetics” makes it clear that there can now be confluence and integration between fields such as brain genomics, human population genetics, and molecular anthropology. The methodology of this field may be applicable here. In order to use modern methods to study the present relationships, it might be helpful to A) perform large-scale comparisons of genes across several strategically selected species in a search for social genes with highly elevated rates of evolution in mammals, especially in primates; B) determine if the alleles for these genes are associated with specific social phenotypes using in vitro and in vivo lab studies; and C) subject the candidate genes to polymorphism and association studies in humans.
The analytical tools that neuroscientists use to study social capacity in other vertebrates can, with appropriate caution, be used to study social capability in humans. Other species have found myriad ways to reduce social contact for ecological purposes. Understanding how this is accomplished may provide insight into prosocial pharmacotherapeutics or even gene therapy for autism.
How can the present comparative, neuroethological approach help with autism? In this author’s opinion, the way it can help the most is through comparative neurobiology. It will be interesting to see if neuroanatomical receptor distribution patterns of oxytocin, vasopressin, endogenous opioids, prolactin, serotonin, and dopamine in the brains of solitary mammals resemble those observed in autism. If there are significant resemblances, it will be necessary for scientists to compare the distribution patterns of these receptors in different animals to help determine which areas in the autistic brain feature a paucity of receptor expression so that these specific areas can be targeted. It may be possible to test drugs and even behavioral interventions in solitary or nonmonogamous animals to determine if these can reverse social interaction deficits. The model may allow an alternate vantage point into the autistic brain, which can only be studied in limited ways because of technical limitations and ethical concerns.
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