Biology ETDs

Publication Date



Theorists and researchers who examine the evolutionary ecology of mating dynamics consider two primary forces, intrasexual and intersexual, as important pressures of selection. Bilateral symmetry and, more controversially, hormone markers in many species, impart information that has been found to influence some aspects of intersexual selection. Both symmetry, as a sign of developmental stability, and hormone markers (i.e., testosteronized traits as cues of immunocompetence) have been classically treated as signals of genetic fitness (Moller & Swaddle, 1997; Hamilton & Zuk, 1982), although neither are consistently shown to correlate with increased mating success. Indeed, results between studies on either trait independently are famously incompatible, but all agree that both of these physical cues result from indirect selection for high genetic quality of offspring. However, there is a growing body of research that has characterized testosterone as key to the calibration of mating and parental efforts, two forms of direct selection. Hence, as with any complete model of mating dynamics, the theory quickly finds itself appealing to both indirect and direct forces of selection. This dissertation is the first study that simultaneously considers the effects of both, using the two cues of testosterone and symmetry. The studies that comprise this dissertation are designed to discover whether symmetry and testosteronized traits communicate the same (e.g., genetic integrity) or different (e.g., behavioral propensity) information or perhaps some mix of content under variant conditions. Homo sapiens, an altricial species with a biparental mating system, is the chosen species of focus.\xa0These studies yield a new organizing framework for a theory of social systems that encompass but are not exclusive to mating systems. Focusing on the nature of the human mating system, this dissertation was a study of female preferences, including behavioral associations with hormone markers, specifically physical cues in the face that reflected 1200 experimental gradations of gender-typical ratios of testosterone to estrogen. As well, experimental stimuli were presented that systematically varied in level of both testosteronize and symmetry. Finally, detailed questionnaires were administered to gather information about the personal traits of all female participants viewing the experimental stimuli. For some studies, this included calculation of the risk of conception for each females ovulatory cycle. Results of the hormone marker studies indicate that females (1) associate extremely testosteronized faces with physical and behavioral traits well-designed for both physical and social competition, (2) significantly associate a lack of testosteronization with pro-sociality, (3) exhibit a tiny but strongly statistically significant shift (p < .0001) toward a more testosteronized male when choosing the most attractive face during high risk of conception, (4) appear to be maximizing a tradeoff within a compete-cooperate continuum when choosing their most attractive faces, and (5) choose an attractive male as a function of personal psychometrics and hormonal state.\xa0 As expected, another finding (6) showed that symmetry is significantly and consistently preferred by females for attractiveness across all combinations of testosterone and symmetry, while testosterone preferences vary widely and in conjunction with traits of the female viewers. (7) Most pertinent to revision of mating theory, this is the first study to independently test for effects of testosterone and symmetry, and their interaction. Speaking to the large and confusing literature, testosteronization is only preferred for attractiveness when combined with symmetry. That is, symmetry and testosteronization appear to convey separate information that significantly interacts to yield a powerful combination cue. Only when high symmetry and mild-to-moderate levels of testosterone occur together is the male considered attractive, probably because this is the strongest cue of somatic condition as expected from immunocompetence theory (Zahavi, 1975; Hamilton & Zuk, 1982) and maintenance of developmental stability (Thornhill, 1980). It would appear that symmetry may be a more pure marker of genetic integrity while testosteronization cues competitive ability beyond immunocompetence, that varies as a function of female condition. In sum, these findings are consistent with the assumption that what the male is perceived to offer in both direct behavioral and indirect genetic form as reflected by current condition, is bartered for by the female with her own behavioral and genetic traits, and her condition. In caveat, genetic competence and behavioral predictors cannot be treated wholly separate as purely indirect or direct selection, respectively, since both have heritable components. Kokko et al. (2002) developed a working mathematical model that replaces a Fisherian runaway-good genes dichotomy with a sexual selection continuum, carrying 'cheap' choice at one end and costly choice at the other. As long as variation in males continues, female preferences evolve as a response to the genetic correlation between level of male display and breeding value to the female. In this way, female choice is self-reinforcing, allowing for preferences and 'sexiness' of sons to build-up genetic correlations (Lande, 1981) at the cheap end of choice, while mounting costliness of traits eventually halts runaway at the opposite end of the continuum. Regarding the results of this dissertation, the same continuum could be used with condition dictating under-developed testosterone and asymmetry for individuals in poor energetic state and only those in good condition or perhaps of highest genetic integrity affording high levels of testosterone while maintaining symmetry. In this way, displays would be an honest indication of traits desirable for offspring. Another continuum developed in this dissertation involves a novel theoretical framework described as a compete-cooperate continuum, defined as follows. At the compete end of the continuum are those traits specific to individual challenges, whether it be intrasexual competition with conspecifics over resources or mate access, or competition in attracting the opposite sex. In contrast, traits for cooperation are defined as those traits for joining in purpose with one or more conspecifics, such as in parenting effort or group coalitions that may or may not engage in inter-group competition. There is much evidence from the fields of evolutionary development and neuroendocrinology that the social environment of the mother during fetal and infant stages as well as during childhood influence the setpoints for investment of testosterone-driven competitive traits (Kuzawa, 2009), with cooperation as the default, less expensive state. Re-interpreting evidence at the broad level of bi-directional selection in a compete-cooperate continuum lends insight to understanding highly social species, particularly in the area of mating dynamics but extending to same-sex coalitions, lengthy juvenile periods and variation in life span. These dissertation findings appeal for a revision to theories of mating systems as co-evolution with general social challenges during life history. Many knowns have been established in the area of overall sociality. (1) Intrasexual conflict in the classic view is solvable by selection for traits that can deal with both same-sex antagonism and same-sex coalition (Ladd et al, 2008). (2) Intersexual conflict is expected to exist to some extent but is not addressed directly by this dissertation (Morrow, Stewart, Rice, 2008). (3) Finally, it is expected that both intrasexual and intersexual pressures select for cooperation in social alliances. In this dissertation, findings support special attention to those of high genetic integrity as capable allies. Specifically, a basis for symmetry as a cue of developmental stability and a signal of genetic fitness is supported, and when symmetry is combined with mild to moderate levels of testosterone the two are significant to female choice, especially for short-term matings at high risk of conception, probably as a signal of current condition reflecting immunocompetence in the current environment. Much progress in the understanding of mating systems has been made by asking whether overall 'genetic quality' is being used in mating decisions. However, in purest hypothetical form, generic 'good genes' per se are expected to have small influence, expressly in altricial species, since traits that serve the opposite sex in a more explicit and specific manner will subsume any presumption of nonspecific generic quality. While all traits under selection must have some heritable component, it is not expected that all traits will be selected for simultaneously, under the same directional selection pressures. A more precise approach to traits reflecting genetic fitness is to consider the domain of selection. In this dissertation, developmental stability and immunocompetence were handled as reflections of somatic effort, having both genetic and condition related components that result from indirect selection (Kokko, 2002). Given this, testosteronization was treated primarily as a result of direct selection in the area of reproductive effort, afforded only when immunocompetence is high enough and developmental stability has been maintained as it trades off with another area, that of somatic effort. Lastly, it is integral to life history theory that both somatic effort and reproductive effort are sensitive to the changing social domain and are expected to tradeoff in a manner that maximizes lifetime reproductive success. In this dissertation, it was found that females exposed in utero to high androgens in the blood of their mothers who were in uncertain social environments behave differently than those females who have not been exposed in utero. Considered altogether, these factors lead me to propose a general compete-cooperate tradeoff theory of social systems, encompassing mating systems and probably cross species communication (Navara, 2009). There is gaining evidence that testosterone (via inhibin, its controlling factor) directs mating and parenting effort (Gray, 2006). Testosterone, especially in conjunction with low cortisol, is associated with increased aggressive behavior with conspecifics, mates and offspring (Daly & Wilson, 1988) while lower testosterone (especially in concert with elevated prolactin and oxytocin, and lowered vasopressin) is found in pair bonded males, fathers and group coalitions (Kuzawa, 2004; Gray, 2009; Mehta et al., 2009) and is sensitive to changes in cortisol that result from social challenges but not physical challenges (Flinn, 2005). The existence of individual challenges (i.e., social competition) in tradeoff with alignment-seeking with positive fitness correlates through cooperation (i.e., group formation, mate bonding, offspring care) are two basic economic problems that an adult in any social species must solve. A compete-cooperate spectrum provides a more focused theoretical framework that may unify and illuminate the current profusion of pertinent studies across many disciplines (i.e., development, psychology, psychiatry, policy-making, biology, anthropology, neurology, endocrinology, immunology, computational mathematics, and so on).\xa0 In conclusion, the novel aspect of the theoretical framework developed by this dissertation arises largely from the perceived cues of both competition and cooperation in the human, backed by large areas of literature from diverse scientific fields and across many species, particularly mammals. A preference for cooperation is viewed as a result of both intersexual and intrasexual preferences that are in a direct continuum with contrasting design selecting primarily for male physical competitive capacities. Furthermore, this competition-cooperation continuum may even be the greater evolutionary force in species where female parental care is vulnerable to exploitation (Trivers & Willard, 1973). Females of such species will prize males who signal cooperation in addition to genetic integrity and the physical capacity to protect. A preference for those individuals signaling good somatic condition (e.g., reflected by developmentally stability either alone or in conjunction with immunocompetence) is also supported by these data. What an individual has to offer in the way of cooperation, competitive abilities, and somatic condition is as important as those same qualities in the perceiver. This dissertation does not ignore or discount theories of 'good genes', but makes explicit when and what components of 'good genes' may be of priority.




compete, cooperate

Document Type


Degree Name


Level of Degree


Department Name

UNM Biology Department

First Advisor

Charnov, Eric L.

First Committee Member (Chair)

Watson, Paul J.

Second Committee Member

Brown, Angela

Third Committee Member

Alcock, Joe