Sunday, May 16, 2010

Human Sexual Dimorphism in Biology, Neurology, Morphology, Development, and Behavior

Eliyahu N. Kassorla
Dr. D. Dunlop
Human Peacocks:
Human Sexual Dimorphism in Biology, Neurology, Morphology, Development, and Behavior

            It is a truth, universally acknowledged, that recombinant genetics creates genetic diversity. The creation and elimination of organisms less adapted to their environment is a process known as natural selection. Sexual selection, a second process, describes the competition within species for access to mates. Most sexually reproducing species have a sex-determining system, and this system codes for different traits. In humans, the sex-determination systems are the sex chromosomes, named “X” and “Y”. Since any human will receive a copy of the X-chromosome from their mother, the Y-chromosome differentially codes for male, and thus sexually dimorphic, traits. Evolution has shaped the key differences between human males and females, and these differences will be examined through a literature review of biological, neurological, morphological, behavioral, and developmental human sexual dimorphism.

Biology: Hormones, Sex and Gender
            The first piece of sexual dimorphism is biological and endocrinological. The article Hormones, Sex, and Gender (1995) by C. Worthman, discusses the effects of endogenous hormones on the human body, on gender-specific traits. The author defines hormones as “chemicals secreted into the blood stream at one body site that exert effects at a remote site” (Worthman, 1995, 594). Worthman relates the complexity of hormones, because “different functional domains of the body may make competing physiologic demands that are mediated through hierarchies of physiologic regulation largely negotiated by endocrine action. Worthman also states that not only does the endocrine system respond to genetic levels, according to natural variation, but that the endocrine system responses are experientially responsive. The author discusses the adaptive role of gender, stating that “sexual reproduction enhances genetic variability among progeny and thus their ability to meet variable selection pressures”, compared to asexual reproduction. The author states the evolution of gender has been successful, considering it exists in almost all higher organisms, and that gender must confer some fitness advantage (602).
The author describes three categories of sex difference, as proposed by Darwin. The first category is the primary sex features, or the features that are involved in reproductive acts, such as genital size or the length of the reproductive tract. The second category is the secondary sex features that enhance mating success, such as displays of fitness, like peacock feathers, bird songs, or moose antlers. The third categories are the ecological features, which are related to “sex-differentiated ‘habits of life’”, such as access to food, clothing, and shelter in humans (602).
The author also describes the interactional mechanisms of action of sex differentiation in response to hormones, primarily estrogen and testosterone. A gene, known as TDF, or testis determining factor, is on the Y-chromosome, and this gene is responsible for triggering the testosterone cascade and masculinizing the embryo (604). The TDF gene is counterbalanced by the estrogen produced by the placenta, which explains the need for males to produce testosterone in amounts similar to an adult level, both in-utero as well as during the twelve weeks after birth (605). The next time the male child produces large amounts of testosterone is in the puberty phase, which is responsible for inducing male primary sex differences (605). In female fetuses, as well as recently born female babies, there is a similarly high level of estrogen, in cooperation with the mother’s placental estrogen (605). The authors summarize that “the [sex differentiation] process involves prolonged, complex developmental sequences coordinated among multiple axes… [and the] action of any hormone is variable and mediated, not intrinsic” (606).

Neurology: Associated Cortical Regions Are Proportionally Larger…
            The second component of human sexual dimorphism is neurological. In an article by Harasty, et al., Language-Associated Cortical Regions Are Proportionally Larger in the Female Brain (1997), the authors assess the brains of 21 subjects free of neuropathology. This included a sample of ten males and eleven females. The brains were weighed at autopsy, fixed in formaldehyde, and sliced in coronal slices. The authors specifically discuss the findings as they relate to the areas known for language acquisition, production, and meaning. They find that female speech is “less dependent of the left hemisphere” and female visuospatial functions are “less dependent on the right hemisphere” (Harasty, et al., 1997, 171). The authors compare these findings to previous findings that females perform significantly better on tasks of verbal fluency and verbal memory.
The authors also report that the mean female brain has larger proportions of grey matter in the dorsolateral prefrontal cortex, known is neuroscience as Broca’s area, which is responsible for speech production (172). Females also have more grey matter in the superior temporal gyrus, an area known as Wernickie’s area, which is responsible for language understanding (172). The authors note that both this morphological study as well as previous fMRI studies reveal that females are also extremely bilateral in these areas; the extent of male bilateralism are very small areas in the non-dominant hemisphere, opposite the normal sized area in the dominant hemisphere (174). The authors state that, relative to weight and size, females have 20.4% larger Broca’s areas than males, as well as 13% larger Wernickie’s area (174).

Morphological: Waist-To-Hip Ratio across Cultures
The third component of human sexual dimorphism is morphological. In an article by Cashdan, Waist-To-Hip Ratio across Cultures: Trade-Offs between Androgen- and Estrogen-Dependent Traits (2008), the author describes the female waist-to-hip ratio (WHR). The author states that previous studies have declared a WHR of 0.7 as ideal “or even lower”, because of the low risk of cardiovascular disease and high probability of conception (Cashdan, 2008, 1099). The author notes that “low WHR signals both fertility and good health” (1099). Across human cultures, however, this ratio varies, but not because of modern diets or obesity. Rather, it is an interaction between genetics and environmental pressures that interact and influence the WHR.
The author uses compiled data from the World Health Organization, and analyzes the body mass index, WHR, ethnicity, and geographic location to analyze the scarcity of food. The author found no significant correlation between WHR and BMI. The question the author asks is: what are the advantages of a high WHR to the success of mating or producing healthy offspring. The author proposes that there are reproductive benefits in a high WHR, despite the negative health effects (1099).  The authors propose several hypothesis, the first being a “better adaptation to cold”, as well as protection against fluctuating food sources (1101). The author notes that in societies with unstable food sources, and where females need to do most of the food procurement and child supporting, a high WHR is beneficial. In these societies, “women must work hard to support their children, compete directly for resources with them, and cope with resource scarcity”, and that “rarely can a woman depend solely on an investing man or even other allomothers to do this for her; she must also depend heavily on her own competitive efforts” (1101). The author describes these reasons why a higher than optimal WHR may be advantageous, and her hypothesis is:
In societies where women are expected to provide most of the food, through hard physical work and in difficult environmental conditions, the balance should be tipped in toward a hormonal profile consistent with a high WHR. In more benign conditions, where women are sedentary and get most of their resources from investing men, a hormonal profile consistent with a low WHR may be adaptive. (1102).
Cashdan discusses key hormones involved with the WHR, which are cortisol, androgens, and estrogens. The author states that approximately 70% of these hormone effects are environmentally dependant (1102). The author discusses the physiological effects of each hormone. Cortisol, a key stress hormone, decreases the levels of leg and thigh fat, and increases the level of visceral fat (1102). This is adaptive because it shifts energy from storage sites to the bloodstream; it moves fat deposits away from a position ready to support a growing fetus to a source that is more easily used for the mother. “The accumulation of visceral fat under stress, therefore, is likely to be adaptive in stressful, dangerous environments and in environments where food abundance is variable” (1102). Further, when all of a mother’s offspring are outside of her body, but still needing care, the success and survivability of her offspring are dependent on her continued maternal care. The hypothesis here is that increased levels of visceral fat, and thus cortisol, increases survivability in societies with variable levels of food or high amounts of environmental stressors and environmental pressures.
Androgen effects, Cashdan describes, are the increase in competitive behaviors, drive, motivation, and energy. The author notes that women with high WHR have “more free testosterone” and “less sex hormone-binding globulin (SHBG) the protein that binds to testosterone [in females] and keeps it biologically inactive” (1102). The hypothesis proposed here is that a higher WHR, and thus higher amounts of androgens, is an adaptive trait that is useful “when a woman  must depend on her own resources to support herself and her children” (1102). Additionally, androgens promote visceral fat storage in females, lending weight to the previous two hypotheses taken together.
The effect of estrogen on the female body decreases visceral fat, increases leg and thigh fat, and prepares the female body for carrying a child. Estrogen levels facultatively decrease in response to “negative energy balance, physical activity and stress [which are] circumstances that favor deferring fertility” (1103). The hypothesis stated here is that when there are environmental stressors or extreme environmental pressures, the ability to conceive and bear offspring is reduced. The fact that females are disproportionately invested in their offspring indicates that this process is evolutionarily adaptive in increasing maternal survivability and, by extension, her current offspring.

Behavioral: An Evolutionary Perspective of Sex-Typed Toy Preferences
            The fourth component of human sexual dimorphism is behavioral. Behavior, however, operates within a biological framework, and so must be explained with biology and evolution. In An Evolutionary Perspective of Sex-Typed Toy Preferences: Pink, Blue, and the Brain (2003), G. Alexander discusses the retinal ganglion cells, their relation to gender, and the types of toys children play with. Alexander rejects social learning theories, and instead describes the effects of hormones on physiological systems (Alexander, 2003, 8). Alexander states that the processes of sex-differentiation creates sexually dimorphic behaviors, and that “experimental manipulation of gonadal hormones [by castration or injection] during nonhuman development shows unequivocally that hormone-dependent masculinization of the brain increases the frequency of subsequent rough and tumble play” (8). Alexander furthers this statement by noting that girls with congenital adrenal hyperplasia, a disorder characterized by increased levels of androgens, show greater levels of aggression, enhanced visuospatial abilities, increased male-typical occupations, and a greater tendency toward “bisexual or homosexual orientations in fantasy and/or behavior” (8).
Alexander describes female-typical drawings: form, color detail, and faces; and relates them to toy preferences. Females, Alexander states, prefer toys that embody these four things (9). Male-typical drawings include motion, movement, and spatial orientation (9). Alexander relates these dichotomous features to neurological and physiological pathways in the brain and how information is processed. There are two main types of retinal ganglion cells, the cells that combine and send stimulation from rods and cones to the visual cortex, and these two types have direct connections to the processing areas.
The first pathway is the M-Cell pathway, which corresponds to the magnocellular retinal ganglion cells. The M-Cell pathway codes for spatial location and visual scenes, and testosterone is implicated in increasing the proportion of M-Cells in the male retina (10). Males, along with androgenized females, have more M-Cells, have more matter in the dorsal parietal lobe, which is responsible for the processing of M-Cell input, and do better on motion and visual tasks (10).
Females, comparatively, have more of the other main type of retinal ganglion cell, the parvocellular cells. The P-Cells code for object recognition, detail, and color, and are processed in the inferior temporal lobe. Females, as well as estrogenized males, have a greater proportion of P-Cells compared to M-Cells, and thus have more brain matter and regions associated with this function (9).
Alexander relates previous comparative genetic studies indicating that the genes that code for the M-Cell pathway is evolutionarily older, and also codes for the colors blue and yellow (9). Further, Alexander notes that genetic analysis has shown that the M-Cell pathway is carried on an autosomal gene, and is thus not sex-linked (11). This corresponds to the sun and the sky, an important distinction in a diurnal species. Alexander also notes that the P-Cell pathway is newer, codes for the colors red and green, and its presence in humans and nonhuman Old World monkeys implicates its role in finding ripe fruit in a dense layer of foliage (10). However, the P-Cell pathway is carried on the X-chromosome, giving females two copies of this color coding gene. The implications of this finding is also addressed, finding that males are more likely to have color-blindness, and that the continued existence of this defective X-chromosome may have adaptive significance (11). The conclusion Alexander draws is that color-blindness is adaptive for detecting “texture and color camouflaged objects” and “evading predation” (11). A crucial tenant of evolution is that natural selection eliminates unfit individuals, or organisms poorly adapted to their environment, so any conservation of a trait in the genome must have adaptive value (11). Since males, in evolutionary history, tended to be hunters rather than detail oriented foragers, color blindness and visuospatial acuity is beneficial; likewise, for females, who tended to be foragers rather than hunters, the ability to distinguish subtle shade variations in berries, tubers, and plants provided protection against toxicity (11). Further, females’ ability to distinguish subtle differences in color, shade, and hue may have also been beneficial in detecting the health of their offspring (11).
Clearly the effects of androgens, which are produced in the gonads, are not confined to genitalia, but also have effects on the physiology and neurology of the brain and sensory systems. Alexander notes that the retina has estrogen receptors, and the post-natal surge of androgens is implicated heavily in the more masculine-typical visual abilities. The testosterone surge nurtures the M-Cell pathways and primes the male or androgenized female for motion and movement.  A female post-natal surge of estrogen is implicated in the increase in the ratio of P-Cells, which prime the female infant, or feminized males, to be more receptive to color, detail, and form (9). Alexander states that “this visual bias at birth ensures that developing cortical circuits are preferentially exposed to faces, which provides the necessary learning experiences that shape the further development of cortical brain areas specialized for face-identification” (10). Alexander is stating a well known principle of human development: the structures already exist in the brain, but are experientially-dependant for the proper functioning in the brain. The brain is born with more circuits than necessary, and a pruning process takes effect to eliminate redundant pathways, as well as make the pathways more specialized. Infants just a few weeks old move their entire body when trying to move their hands, but proprioception develops quickly as the specialized pathways are laid down; by six months an infant can move their limbs independently. This is credited to the strengthening and specialization of pathways from the motor cortex to spinal cord, and then to the correct muscle.
Alexander states, “sex-dimorphic visual preferences consistent with M-Cell or P-Cell processing efficiencies precede experience with gender linked preferences” (10). Further, Alexander states that “neonatal visual preferences support the hypothesis that androgens may initiate the specialization of visual pathways that contribute to visual biases for object movement or form/color” (10).  Alexander seems to be indicating that social learning theories are likely incomplete or wrong. Alexander infers that biological fact is more parsimonious than the contrived social learning theories, and that biology has more explanatory power (12). This model is consistent with both human infant studies, especially using the preferential looking technique, as well as nonhuman primate toy play (12). 

Developmental: Evolution and Developmental Sex Differences
The last piece of the sexual dimorphism puzzle is the development of sexual characteristics. In an article by D. Geary, Evolution and Developmental Sex Differences (1999), Geary explains how sex-specific traits develop. Geary states that childhood is the time when future adult behaviors are refined (Geary, 1999, 115). Geary, like Alexander, rejects the social learning theories, and instead supports an evolutionary explanation. “From an evolutionary perspective, cultural and ecological factors are expected to influence the expression of developmental sex differences” (115). Geary compares human childhood to animal maturation periods. “Females typically choose mates on the basis of indicators of physical, genetic, or behavioral fitness … on the basis of traits that signal a benefit to them” (116). Geary uses the example of the “long and symmetric male hummingbird” as a trait that advertises genetic and reproductive health. Geary compares childhood to the period that juvenile male Bower birds spend observing older males building their bowers, learning how to attract females from the previous generation (117). This is a nonhuman example of how culture is acted upon by evolution and natural selection.
Geary compares the competitive nature of both males and females. Males compete over resources: food, money, status, and property. Females tend to compete with each other for paternal investment, and do so by “relational aggression. They [females] gossip, shun, and backbite their competitors” (117). This is inferentially related to the bilateral female language areas. Curiously, when females fight over a potential male, they utilize terms and phrases that indicate that a male should be wary of assured paternity; when men verbally compete for the affections of a female they question the ability of their competitor to provide resources (117-118).  Geary notes that males by the age of three are already engaged in “rough-and-tumble play … six times more frequently than groups of girls do” (119). Geary also describes the group-level cooperation play that male children engage in, known as team sports. Geary hypothesizes that these are evolved tendencies to engage in male-male competition, as well as group hunting tendencies (118). Differences in the social development of males and females, Geary notes, are also seen in chimpanzees, and is very likely that “these are indeed evolved tendencies in humans” (118). In female group interactions, females show “greater empathy; more concern for the wellbeing of other girls; and more nurturing, intimacy, and social and emotional support” (118). Geary states that the social behavior of men is “focused on achieving status and dominance and developing coalitions for competing against other groups of boys”, while females behavior is “focused on developing and maintain a network of personal relationships and social support” (118). Geary’s conclusion is that childhood is the time where children practice their competition and cooperation (118).
Geary further notes that the aggressive play that male children engage in increases their endurance while decreasing their sensitivity to pain (119). Cultural norms discourage males from expressing pain, which is likely an evolved tendency that increases the ability of males to be better hunters (119). In cultures where there is no limit to harem size, male competitive behavior increases and becomes more aggressive (119). The reverse is also true, that the more monogamy is encouraged, the more the competition takes on token or symbolic meaning (119). In females, there is also a divide based on cultural factors: in cultures where females can hold power and are encouraged to be independent and self-reliant, the less “obedient, more aggressive, and more achievement oriented” the females become.

Testosterone: Testosterone and Men’s Depression, Influences of Serotonin and Testosterone
            The primary male hormone is testosterone, with males producing seven times more testosterone than females (Booth, 1999, 130). Booth, et al. in Testosterone and Men’s Depression: The Role of Social Behavior (1999), the authors describe the relationship to losing struggles for dominance and the decrease in testosterone levels (138). This article studies the association between testosterone levels and depression levels (132). . The authors utilized a sample of 4393 males who performed only one term in the Army, with a mean age of 37. The sample was drawn on the inference that men who served in the military already had higher testosterone levels, and that the higher levels would display a larger effect size. The authors discovered a significant effect size (137). Lower levels of testosterone are implicated with higher levels of depression, while high testosterone males had reduced levels of depression. Average level testosterone males had the largest effect size, which the authors link to the increased antisocial and risk taking behaviors of the males with increased levels of aggression (138). One of the authors, Booth, cites his previous study relating testosterone and aggression levels, along with his findings that lower status individuals show more signs of stress and lower serum testosterone levels (139).
            Further, an article by P. Bernhardt, Influences of Serotonin and Testosterone in Aggression and Dominance: Convergence with Social Psychology (1997), discusses the role of testosterone and serotonin in mediating aggression. Bernhardt extricates aggression from hostility and anger (Bernhardt, 1997, 45). Aggression, Bernhardt states, is a tool used to attain dominance (45). In this article, Bernhardt quotes his almost impossible to get article, Testosterone changes during vicarious experiences of victory and defeat in spectators of sporting events (1997), by noting the “connection of testosterone to status (and presumable feelings of dominance) without  the presence of aggressive acts can also be seen in studies of [sports] fans” (46). The evolutionary explanation predicts correctly the findings that levels of serum testosterone in males are higher when the supported team won, and lower when the supporting team lost (46). The visual system evolved before sociality, and before sports, and thus the prediction is that when seeing aggressive acts take place, there is a neural mechanism that primes the individual for engaging in aggression (46).
            Bernhardt quotes a rat study where dominance behavior was elicited with intramuscular injections of testosterone and serotonin, while an injection of serotonin agonists mitigated the effects of the injected testosterone – “returning the rats to a non-dominant status” (46).
Bernhardt hypothesizes, and correctly since the 13 years since publication, that the responsible structures in the brain are the amygdala and hypothalamus (47). The amygdala responds to testosterone by increasing activation, which increases aggressive output (48). The hypothalamus mediates the activity of the amygdala, preferentially responding to serotonin to lower aggressive output (48). Further, studies with low serotonin animals have shown them to be “hyperresponsive to aversive stimuli”, reinforcing the connection of testosterone with aggression (48).

Human sexual dimorphism is expressed more complexly than in other animals. The many gender specific attributes are interactional. Many of them have implications on human culture and human behavior, but their value is in understanding their root cause. Human behavior, in order to make sense, must be examined in light of evolution and biology. Evolution has created and forged the gender differences to what we see today, and society is a construct of our biology. Without our biology, our adaptations through hundreds of thousands of years of natural selection, sociality could not be possible. The way humans express their behavior today is a direct reflection on environmental and selection pressures in the past. The male advantage in visual acuity, the high rate of color blindness in men, and the role of aggression and male-typical behaviors all have added to the survival of the human species, Homo sapiens sapiens. Hunting, killing, fighting, these are all things that have fitness advantages for males. Common features in most sports that are male-dominated involve acts that rely on physicality and motion. Baseball, basketball, football, lacrosse, and soccer all rely on individuals on opposite teams competing, individuals on the same team cooperating, and one team emerging victorious. Studies in psycho-endocrinology have revealed that males who engage in sports have higher serum testosterone, and increases when they win (Bernhardt, 1997, 46). Combined with the Alexander article, the inference that can be drawn is that male play styles mimic hunting, using the weapons of the day – whether it is an arrow or a gun is irrelevant, what is important is the child understands what the object does – practicing for killing their food, and that evolution forged these activities to be fun for children. These play styles activate and strengthen the pathways that code for motion and spatial arrangement so that through play, the child practices the activities that his ancestors needed to be good at for survival.
Females, as evolution has forged them, are typically weaker, physically, than males. Their contributions, from an evolutionary standpoint, are the typical home and hearth cultural norms. Females raise children, rear them, and give them the best chance of survival that they possibly can. The female advantage in color, object perception, and sociality are also reflections of our evolutionary past. According to Alexander (2003), the early role of females tended to be in foraging nuts, berries, tubers, herbs, plants, and child rearing (Alexander, 2003, 11). Because of the need to discriminate between toxic plants and non-toxic food, females have evolved the neuronal and physiological structures associated with object discrimination and color perception. Additionally, while males were on hunting parties, females tended to stay at the campsite together, where their cooking and child-rearing took place. Because of the need for cooperation and coordination required for communal living, females have undergone selection pressure to increase their ability to produce and understand complex social language, as well as non-verbal behaviors (Harasty, et al, 1997, 175). Further, the female infant preference for faces strengthens the area in the fusifom facial area, allowing females to discriminate subtle differences in facial expression. In combination with the enhanced female perception of color, females are regarded as superior in understanding and empathizing with other’s emotional states (Alexander, 11-12). . Alexander also reveals that female children also play with their toys as if they were offspring. In combination with studies that reveal that female monkeys who engage in this type of play have lower infant mortality rates, this play is interpreted as practice for future offspring.
The complex interaction between biological, neurological, and evolutionary forces maintains the differences in males and females. While not as striking as a peacocks tail, the male and female differences all contribute to survival and reproductive advantages. No doubt exists that natural selection and sexual selection together have equipped each gender with the tools they need to be successful. In an evolutionary perspective, success is not measured by survival and offspring. Rather success is measured in grandchildren – because your experiment, the F2 generation, was adapted well enough to survive and pass down their genes. That is the goal of every organism.

Alexander, G. M. (2003). An evolutionary perspective of sex-typed toy preferences: pink, blue, and the brain. Archives of Sexual Behavior, 32, 7-17.
Bernhardt, P. C. (1997). Influences of serotonin and testosterone in aggression and dominance: Convergence with social psychology. Current Directions in Psychological Science. 6:2, 44-48.
Booth, A., Johnson, D., Granger, D. (1999). Testosterone and men’s depression: The role of social behavior. Journal of Health and Social Behavior. 40:2, 130-140.
Cashdan, E. (2008). Waist-to-hip ratio across cultures: trade-offs between androgen- and estrogen-dependent traits. Current Anthropology, 49(6), 1099-1107.
Geary, D. (1999). Evolution and developmental sex differences. Current Directions in Psychological Science (Wiley-Blackwell), 8(4), 115-120.
Harasty J., Double, K. L., Halliday, G. M., Kril, J. J., McRitchie, D. A. (1997). Language-associated cortical regions are proportionally larger in the female brain. Archives of Neurology, 54:171–176.
Worthman, C. M. Hormones, sex and gender. Annual Review of Anthropology. 24, 593-617.

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