Phenotypic Integration of Sexually Selected Traits in a Songbird

Thesis (PhD) - Indiana University, Ecology and Evolutionary Biology, 2007Natural selection favors traits that fit not only the external environment, but also the internal environment of the organism. As a consequence, traits often show a pattern of correlation, or phenotypic integration. In this dissertation, I examined both the evolutionary processes and the physiological mechanisms that generate phenotypic integration. I studied a natural population of a songbird, the dark-eyed junco (Junco hyemalis), focusing on the male "mating phenotype," the suite of morphology, physiology, and behavior used to attract and compete for mates. In Chapter 1, I review literature suggesting that correlational selection, which occurs when traits interact in their effects on fitness, may have effects on the physiological mechanisms that underlie integrated suites of traits. In Chapter 2, I found that correlational sexual selection favored an association between body size and a white patch on the tail feathers ("tail white"), an ornament used both in courtship and male-male competition. I also found that body size and tail white were genetically correlated. These results suggest that correlational selection may maintain the integration of the two traits. In Chapters 3-5, I focus on the role of the steroid hormone testosterone in the mating phenotype. In Chapter 3, I measured natural variation in testosterone levels and found that more attractive males had higher androgen responsiveness. That is, males with more tail white produced more testosterone in response to an injection of GnRH, a hypothalamic hormone. This suggests that investment in mating behavior (which seems to be controlled by testosterone) may covary with attractiveness. Indeed, in Chapter 4, I found that androgen responsiveness naturally covaries with both mating and parental behavior. Males that produced more testosterone defended their territories more vigorously and fed their offspring less often. Finally, in Chapter 5, I examined how selection acts on androgen responsiveness, and found that males with very high or very low responsiveness were less likely to survive. Combined, these studies suggest that testosterone, on a physiological level, and correlational selection, on an evolutionary level, act as integrators of the male mating phenotype

Convergent Evolution of Sexual Dimorphism in Skull Shape Using Distinct Developmental Strategies

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male-specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.Organismic and Evolutionary Biolog

Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalis

Members of a gene family expressed in a single species often experience common selection pressures. Consequently, the molecular basis of complex adaptations may be expected to involve parallel evolutionary changes in multiple paralogs. Here, we use bacterial artificial chromosome library scans to investigate the evolution of the voltage-gated sodium channel (Nav) family in the garter snake Thamnophis sirtalis, a predator of highly toxic Taricha newts. Newts possess tetrodotoxin (TTX), which blocks Nav’s, arresting action potentials in nerves and muscle. Some Thamnophis populations have evolved resistance to extremely high levels of TTX. Previous work has identified amino acid sites in the skeletal muscle sodium channel Nav1.4 that confer resistance to TTX and vary across populations. We identify parallel evolution of TTX resistance in two additional Nav paralogs, Nav1.6 and 1.7, which are known to be expressed in the peripheral nervous system and should thus be exposed to ingested TTX. Each paralog contains at least one TTX-resistant substitution identical to a substitution previously identified in Nav1.4. These sites are fixed across populations, suggesting that the resistant peripheral nerves antedate resistant muscle. In contrast, three sodium channels expressed solely in the central nervous system (Nav1.1–1.3) showed no evidence of TTX resistance, consistent with protection from toxins by the blood–brain barrier. We also report the exon–intron structure of six Nav paralogs, the first such analysis for snake genes. Our results demonstrate that the molecular basis of adaptation may be both repeatable across members of a gene family and predictable based on functional considerations

Adaptive radiation along a deeply conserved genetic line of least resistance in \u3cem\u3eAnolis\u3c/em\u3e lizards

On microevolutionary timescales, adaptive evolution depends upon both natural selection and the underlying genetic architecture of traits under selection, which may constrain evolutionary outcomes. Whether such genetic constraints shape phenotypic diversity over macroevolutionary timescales is more controversial, however. One key prediction is that genetic constraints should bias the early stages of species divergence along “genetic lines of least resistance” defined by the genetic (co)variance matrix, G. This bias is expected to erode over time as species means and G matrices diverge, allowing phenotypes to evolve away from the major axis of variation. We tested for evidence of this signal in West Indian Anolis lizards, an iconic example of adaptive radiation. We found that the major axis of morphological evolution was well aligned with a major axis of genetic variance shared by all species despite separation times of 20–40 million years, suggesting that divergence occurred along a conserved genetic line of least resistance. Further, this signal persisted even as G itself evolved, apparently because the largest evolutionary changes in G were themselves aligned with the line of genetic least resistance. Our results demonstrate that the signature of genetic constraint may persist over much longer timescales than previously appreciated, even in the presence of evolving genetic architecture. This pattern may have arisen either because pervasive constraints have biased the course of adaptive evolution or because the G matrix itself has been shaped by selection to conform to the adaptive landscape

Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome

Colubridae represents the most phenotypically diverse and speciose family of snakes, yet no well-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genome structure that provide insight into the evolution of amniote genomes. Analyses of the garter snake and other squamate reptile genomes highlight shifts in repeat element abundance and expansion within snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z and W sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionary origins in a rear-fanged colubrid snake, together with new genomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes

Data from: Life histories and invasions: accelerated laying rate and incubation time in an invasive lizard, Anolis sagrei

Faster life histories are correlated with greater invasion success across taxa. However, comparisons of life-history traits across native and invasive ranges are rare, and thus it is unknown whether invasions lead directly to evolutionary shifts in life histories. Here we compare life history traits of three invasive populations of brown anoles (Anolis sagrei) to a representative native population. In a common garden, we measured a number of reproductive traits including egg-laying rate and incubation period. We hypothesized that invasive populations would exhibit faster reproduction because fast life histories are favoured both by the invasion itself and by shorter breeding seasons in the invasive range. Compared to native females, invasive females had shorter interlaying intervals and produced eggs that hatched more quickly. Invasive and native populations did not differ consistently in egg size, hatching success, or hatchling size. Our results indicate that life history traits have rapidly diverged during the brown anole invasion, potentially facilitating the successful establishment and expansion of the species range

Normalized expression data for juveniles and subadults

Normalized counts per million for transcriptome comparisons of juvenile and subadult males and female

Data from: Hormonally mediated increases in sex-biased gene expression accompany the breakdown of between-sex genetic correlations in a sexually dimorphic lizard

The evolution of sexual dimorphism is predicted to occur through reductions in between-sex genetic correlations (rmf) for shared traits, but the physiological and genetic mechanisms that facilitate these reductions remain largely speculative. Here, we use a paternal half-sibling breeding design in captive brown anole lizards (Anolis sagrei) to show that the development of sexual size dimorphism is mirrored by the ontogenetic breakdown of rmf for body size and growth rate. Using transcriptome data from the liver (which integrates growth and metabolism), we show that sex-biased gene expression also increases dramatically between ontogenetic stages bracketing this breakdown of rmf. Ontogenetic increases in sex-biased expression are particularly evident for genes involved in growth, metabolism, and cell proliferation, suggesting that they contribute to both the development of sexual dimorphism and the breakdown of rmf. Mechanistically, we show that treatment of females with testosterone stimulates the expression of male-biased genes while inhibiting the expression of female-biased genes, thereby inducing male-like phenotypes at both organismal and transcriptomic levels. Collectively, our results suggest that sex-specific modifiers such as testosterone can orchestrate sex-biased gene expression to facilitate the phenotypic development of sexual dimorphism while simultaneously reducing genetic correlations that would otherwise constrain the independent evolution of the sexes