Robert Cox - Research

Sexual conflict and cryptic female choice

Sexual dimorphism often indicates that natural and/or sexual selection favors different traits in males and females. This can create intra-locus sexual conflict because genes that are beneficial when expressed in males may be detrimental when expressed in females, and vice versa. Ryan Calsbeek’s research on the brown anole (Anolis sagrei) indicates pervasive intra-locus sexual conflict tied to both morphological and physiological correlates of fitness. Interestingly, females may be able to mitigate this conflict via "cryptic" mate choice: females mate with multiple males and then appear to selectively sort their sperm to produce sons and daughters by different sires! Ryan and I are currently investigating both the physiological mechanisms that enable this cryptic choice and the potential adaptive value of "sperm sorting" with respect to offspring fitness.

Evolution of sexual size dimorphism (SSD)

Why are males larger than females in some species, yet females are larger than males in others? This question has intrigued biologists since Charles Darwin, who first proposed that males are larger than females because large body size gives them an advantage in competition with other males for access to mates (sexual selection). By contrast, females may be larger than males when body size strongly influences the number of offspring that a female can produce (fecundity selection). One way to test these hypotheses is to use the evolutionary history of a group of organisms to look for correlated evolutionary changes in sexual selection, fecundity selection, and SSD. For example, the figure on the left shows that the evolution of territoriality in lizards is associated with shifts toward male-larger SSD, while evolutionary increases in fecundity are correlated with shifts toward female-larger SSD. For more details, check out our paper in Evolution ( PDF) and a recent review of SSD in reptiles from the book Sex, Size & Gender Roles: Evolutionary Studies of Sexual Size Dimorphism ( PDF).

Endocrine regulation of sexual size dimorphism

Although many evolutionary studies have focused on why males and females differ in size, relatively few have explored how males and females develop alternative phenotypes in the face of intersexual genetic correlations. Henry John-Alder and I have begun to explore the role of testosterone as a sex-specific epigenetic growth regulator in Sceloporus lizards. Our results indicate that testosterone strongly influences male growth, but that the direction of this effect depends on the direction of sexual size dimorphism. For example, the figure on the left shows that testosterone inhibits growth in a species where males are the smaller sex, but stimulates growth in species where males are the larger sex. Thus, testosterone may act as a ‘bipotential’ regulator that facilitates the development of both male– and female-larger SSD. In collaboration with Emily Taylor at Cal Polytech, we are expanding the scope of this project by studying additional Sceloporus species with alternative patterns of SSD. Check out our papers in PBZ ( PDF), JEB (PDF), Functional Ecology (PDF), and Integrative and Comparative Biology ( PDF) for more details.

Testosterone and coloration

Many organisms exhibit sexual dichromatism, a difference in color between males and females. For example, adult male eastern fence lizards (Sceloporus undulatus) have bright blue and black patches on their throats and bellies, as well as bright dorsal coloration. Males broadcast these social signals by performing "push-up" displays that expose their colorful ventral surfaces. By contrast, females and juveniles have cryptic dorsal coloration and plain white ventral surfaces. The figure on the left shows that the development of coloration in males is strongly dependent upon testosterone. Castrated males are almost indistinguishable from females in both dorsal and ventral coloration, while castrated males that receive testosterone have vibrant colors identical to intact control males. The development of bright blue ventral patches can even be induced in juvenile females by giving them testosterone! For details, check out this paper in Copeia (PDF).

Testosterone and parasitism

Testosterone mediates the seasonal and sex-specific expression of many traits that are important for male reproductive success, but there are also costs associated with elevated testosterone levels. Increased mite parasitism is one such cost that is incurred by male lizards. For example, the figure to the left shows that breeding male striped plateau lizards (Sceloporus virgatus) are more heavily parasitized than females. Parasitism decreases when males are castrated to remove the primary endogenous source of testosterone (CAST), but parasitism increases when castrated males are given exogenous testosterone (TEST). Parasitism and other such costs may help explain why testosterone inhibits growth in this species, since males with higher parasite loads also grow more slowly. Check out these papers in Physiological & Biochemical Zoology (PDF) and Functional Ecology (PDF) for more details.

Costs of reproduction

Life history theory predicts a trade-off between current and future reproductive investment due to inherent costs of reproduction, such as reduced survival and growth. While this concept is intuitively appealing, few studies have provided direct experimental evidence for costs of reproduction. In Yarrow’s spiny lizard (Sceloporus jarrovii), some females reproduce as yearlings, while others delay reproduction until their second year. The top panel shows that reproductive yearlings grow more slowly both during and after pregnancy, but this difference could simply reflect the larger initial size of reproductive females. However, when females are ovariectomized to prevent reproductive investment, the same growth differences are observed, as shown in the bottom panel. This combination of correlative and experimental approaches provides strong evidence that reproductive investment is traded off against growth in this species. Check out this article in Journal of Animal Ecology (PDF) for more details.

Unlike Sceloporus lizards, brown anoles (Anolis sagrei) have evolved reduced clutch sizes consisting of only one or occasionally two eggs, ostensibly as an adaptation to reduce the physical burden of reproduction in light of their arboreal lifestyle. However, even a single-egg clutch incurs a performance cost in this species. Ryan Calsbeek and I found that, by surgically removing oviductal eggs from reproductive females, we could increase their stamina by 10.5% and their maximal sprint speed by 12% relative to pre-treatment values! Moreover, ovariectomized females grow substantially more than reproductive controls and actually have greater survival over the course of the reproductive season! The figure on the left shows an anesthetized A. sagrei female with two eggs that were surgically removed from her oviducts -- you can easily imagine how this physical burden could reduce her speed and stamina! Next year, we're planning to combine these phenotypic manipulations with predator exclusion/introduction experiments on small islands (see below) to determine whether the survival cost of reproduction is a consequence of predation.

Evolution and maintenance of polymorphism

Many organisms are polymorphic -- they exhibit discrete phenotypic variation in some trait(s) such that individuals can be classified into alternative forms or "morphs". One of the most intriguing questions in evolutionary biology is: Why do polymorphisms persist in natural populations? Potential answers to this question invoke selective neutrality, frequency-dependent selection, temporal or spatial heterogeneity, and balance between selection and gene flow. Ryan Calsbeek has found that female brown anoles (Anolis sagrei) are polymorphic in dorsal coloration, and can be classified as "diamond" (on the left in the picture), "bar" (lower right), or intermediate "diamond-bar" (upper right) morphs. Our preliminary results show that this polymorphism is strongly heritable and that the frequencies of alternative morphs vary among different islands in the Bahamas. We are presently examining how female morphs differ in reproductive costs, behavior, survival, and other measures, as well as characterizing the developmental basis of coloration and geographic variation in morph frequency.

Experimental studies of selection in the wild

In addition to simply measuring selection in natural populations, I'm very interested in devising experiments that manipulate either the phenotypic targets of selection or the environmental factors that generate selection. Examples of the former include "phenotypic engineering" by removal and replacement of hormones important to phenotypic expression and manipulation of reproductive costs by ovariectomy or egg removal. As an example of the latter, Ryan Calsbeek devised an experiment in which we covered small islands with netting to exclude avian predators (e.g., mockingbirds, green herons). This photo shows Ryan (right) and myself setting up the pilot study. By comparing the form and intensity of selection on this island with that on control islands with open netting, we hope to determine the ecological mechanisms that underlie selection on traits such as body size, limb morphology, stamina, sprint speed, reproductive burden, and immune function.