Alison R. Davis Rabosky

Spatial and Temporal Drivers of Phenotypic Diversity in Polymorphic Snakes

Color polymorphism in natural populations presents an ideal opportunity to study the evolutionary drivers of phenotypic diversity. Systems with striking spatial, temporal, and qualitative variation in color can be leveraged to study the mechanisms promoting the distribution of different types of variation in nature. We used the highly polymorphic ground snake (Sonora semiannulata), a putative coral snake mimic with both cryptic and conspicuous morphs, to compare patterns of neutral genetic variation and variation over space and time in color polymorphism to investigate the mechanistic drivers of phenotypic variation across scales. We found that strong selection promotes color polymorphism across spatial and temporal scales, with morph frequencies differing markedly between juvenile and adult age classes within a single population, oscillating over time within multiple populations, and varying drastically over the landscape despite minimal population genetic structure. However, we found no evidence that conspicuousness of morphs was related to which color pattern was favored by selection or to any geographic factors, including sympatry with coral snakes. We suggest that complex patterns of phenotypic variation in polymorphic systems may be a fundamental outcome of the conspicuousness of morphs and that explicit tests of temporal and geographic variation are critical to the interpretation of conspicuousness and mimicry.

Molecular systematics of the genus Sonora (Squamata: Colubridae) in central and western Mexico

Mexico possesses high levels of endemic biodiversity, especially for squamate reptiles. However, the evolutionary relationships among many reptiles in this region are not well known. The closely related genera of Sonora Baird and Girard 1853 and Procinura Cope 1879 are coralsnake mimics found from the central and western United States to southwestern Mexico and Baja California. Although species delimitation in this group has historically relied upon colour pattern and other morphological characters, many populations of these species display colour pattern polymorphism, which may confound taxonomy. We used molecular phylogenetics to assess the evolutionary relationships and delimit species within Sonora, focusing on the phylogenetic position of Procinura and the validity of S. mutabilis and aequalis. We sequenced two mitochondrial (ND4 and cytb) and two nuclear (c-mos and RAG-1) genes for the single species of Procinura and each of the four species of Sonora. We analysed these sequences using maximum parsimony, maximum likelihood and Bayesian phylogenetic analyses on separately concatenated mitochondrial and nuclear datasets. Additionally, we used Bayesian coalescent methods to build a species tree (Bayesian species tree analysis) and delimit species boundaries (Bayesian species delimitation). All methods indicated that Procinura is deeply nested within Sonora, and most individual species are well supported. However, we found that one taxon (S. aequalis) is paraphyletic with regard to another (S. mutabilis). We recommend that the genus Procinura be synonymised with Sonora and that S. aequalis be synonymised with S. mutabilis. Additionally, the phylogenetic patterns that we document are broadly congruent with a Miocene or Pliocene divergence between S. michoacanensis and S. mutabilis along the Trans-Mexican Volcanic Belt. Finally, our data are consistent with the early evolution of coralsnake mimicry and colour pattern polymorphism within the genus Sonora.

Sequence variation in the Mc1r gene for a group of polymorphic snakes

Studying the genetic factors underlying phenotypic traits can provide insight into dynamics of selection and molecular basis of adaptation, but this goal can be difficult for non-model organisms without extensive genomic resources. However, sequencing candidate genes for the trait of interest can facilitate the study of evolutionary genetics in natural populations. We sequenced the melanocortin-1 receptor (Mc1r) to study the genetic basis of color polymorphism in a group of snake species with variable black banding, the genera Sonora, Chilomeniscus, and Chionactis. Mc1r is an important gene in the melanin synthesis pathway and is associated with ecologically important variation in color pattern in birds, mammals, and other squamate reptiles. We found that Mc1r nucleotide sequence was variable and that within our focal Sonora species, there are both fixed and heterozygous nucleotide substitutions that result in an amino acid change and selection analyses indicated that Mc1r sequence was likely under purifying selection. However, we did not detect any statistical association with the presence or absence of black bands. Our results agree with other studies that have found no role for sequence variation in Mc1r and highlight the importance of comparative data for studying the phenotypic associations of candidate genes.

Direct Fitness Correlates and Thermal Consequences of Facultative Aggregation in a Desert Lizard

Social aggregation is a common behavioral phenomenon thought to evolve through adaptive benefits to group living. Comparing fitness differences between aggregated and solitary individuals in nature – necessary to infer an evolutionary benefit to living in groups – has proven difficult because communally-living species tend to be obligately social and behaviorally complex. However, these differences and the mechanisms driving them are critical to understanding how solitary individuals transition to group living, as well as how and why nascent social systems change over time. Here we demonstrate that facultative aggregation in a reptile (the Desert Night Lizard, Xantusia vigilis) confers direct reproductive success and survival advantages and that thermal benefits of winter huddling disproportionately benefit small juveniles, which can favor delayed dispersal of offspring and the formation of kin groups. Using climate projection models, however, we estimate that future aggregation in night lizards could decline more than 50% due to warmer temperatures. Our results support the theory that transitions to group living arise from direct benefits to social individuals and offer a clear mechanism for the origin of kin groups through juvenile philopatry. The temperature dependence of aggregation in this and other taxa suggests that environmental variation may be a powerful but underappreciated force in the rapid transition between social and solitary behavior.

Predator Perspective Drives Geographic Variation in Frequency-Dependent Polymorphism

Color polymorphism in natural populations can manifest as a striking patchwork of phenotypes in space, with neighboring populations characterized by dramatic differences in morph composition. These geographic mosaics can be challenging to explain in the absence of localized selection because they are unlikely to result from simple isolation-by-distance or clinal variation in selective regimes. To identify processes that can lead to the formation of geographic mosaics, we developed a simulation-based model to explore the influence of predator perspective, selection, migration, and genetic linkage of color loci on allele frequencies in polymorphic populations over space and time. Using simulated populations inspired by the biology of Heliconius longwing butterflies, Cepaea land snails, Oophaga poison frogs, and Sonora ground snakes, we found that the relative sizes of predator and prey home ranges can produce large differences in morph composition between neighboring populations under both positive and negative frequency-dependent selection. We also demonstrated the importance of the interaction of predator perspective with the type of frequency dependence and localized directional selection across migration and selection intensities. Our results show that regional-scale predation can promote the formation of phenotypic mosaics in prey species, without the need to invoke spatial variation in selective regimes. We suggest that predator behavior can play an important and underappreciated role in the formation and maintenance of geographic mosaics in polymorphic species.

Unlinked Mendelian inheritance of red and black pigmentation in snakes: Implications for Batesian mimicry

Identifying the genetic basis of mimetic signals is critical to understanding both the origin and dynamics of mimicry over time. For species not amenable to large laboratory breeding studies, widespread color polymorphism across natural populations offers a powerful way to assess the relative likelihood of different genetic systems given observed phenotypic frequencies. We classified color phenotype for 2175 ground snakes (Sonora semiannulata) across the continental United States to analyze morph ratios and test among competing hypotheses about the genetic architecture underlying red and black coloration in coral snake mimics. We found strong support for a two‐locus model under simple Mendelian inheritance, with red and black pigmentation being controlled by separate loci. We found no evidence of either linkage disequilibrium between loci or sex linkage. In contrast to Batesian mimicry systems such as butterflies in which all color signal components are linked into a single “supergene,” our results suggest that the mimetic signal in colubrid snakes can be disrupted through simple recombination and that color evolution is likely to involve discrete gains and losses of each signal component. Both outcomes are likely to contribute to the exponential increase in rates of color evolution seen in snake mimicry systems over insect systems.

Report from the first snake genomics and integrative biology meeting.

This report summarizes the proceedings of the 1st Snake Genomics and Integrative Biology Meeting held in Vail, CO USA, 5–8 October 2011. The meeting had over twenty registered participants, and was conducted as a single session of presentations. Goals of the meeting included coordination of genomic data collection and fostering collaborative interactions among researchers using snakes as model systems.

Synopsis and taxonomic revision of three genera in the snake tribe Sonorini

ABSTRACT Delimiting species is a crucial goal of integrative biology, and yet can be misled by homoplasy and high levels of morphological variation. The snake tribe Sonorini contains three genera that have long confounded taxonomists: Chilomeniscus, Chionactis and Sonora. Dynamic colour evolution in this group, including rampant geographic variation in colour and colour polymorphism, has led to a chaotic taxonomy. We used mitochondrial and high-throughput nuclear data (ddRADseq) and complete taxonomic sampling of each genus to reconstruct phylogenetic relationships and systematically revise the genus. Our research revealed that Sonora is paraphyletic with regards to Chilomeniscus and Chionactis and that at least one species (S. semiannulata) is paraphyletic with respect to at least one other recognized species. Additionally, we found substantial undescribed genetic diversity within multiple species which is incongruent with morphological variation in coloration. Accordingly, we proposed synonymizing Chionactis and Chilomeniscus with Sonora, which has taxonomic priority over both genera. As we found genetic evidence that supported some of the historically delimited diversity within multiple taxa, we revised species-level taxonomy accordingly. This new taxonomy recognizes a revised genus of Sonora that contains 15 species of diminutive and often brightly coloured snakes that are distributed from central Mexico to north-western USA. http://www.zoobank.org/urn:lsid:zoobank.org:pub:45A553D8-6435-4E0A-84ED-DF31E2CCD872

Historical Environment Is Reflected in Modern Population Genetics and Biogeography of an Island Endemic Lizard (Xantusia riversiana reticulata)

The restricted distribution and isolation of island endemics often produces unique genetic and phenotypic diversity of conservation interest to management agencies. However, these isolated species, especially those with sensitive life history traits, are at high risk for the adverse effects of genetic drift and habitat degradation by non-native wildlife. Here, we study the population genetic diversity, structure, and stability of a classic “island giant” (Xantusia riversiana, the Island Night Lizard) on San Clemente Island, California following the removal of feral goats. Using DNA microsatellites, we found that this population is reasonably genetically robust despite historical grazing, with similar effective population sizes and genetic diversity metrics across all sampling locations irrespective of habitat type and degree of degradation. However, we also found strong site-specific patterns of genetic variation and low genetic diversity compared to mainland congeners, warranting continued special management as an island endemic. We identify both high and low elevation areas that remain valuable repositories of genetic diversity and provide a case study for other low-dispersal coastal organisms in the face of future climate change.

Disruptive selection on male reproductive polymorphism in a jumping spider, Maevia inclemens

Genetic polymorphism in males has long been considered paradoxical because sexual selection is expected to deplete additive genetic variation. Although studies have shown how divergent selection between populations can make that work, it is very rare to find disruptive selection within one population. Since intersexual selection can have a significant effect on the phenotypic morphospace of the opposite sex, we analysed the role of female preference as a disruptive selective force. In this study we evaluated how female preference acts on anatomical and sex-related behavioural traits of two male morphs in the jumping spider Maevia inclemens . We used mate choice trials to analyse how female preference for the two morphs varied. The tests indicated that females preferred opposite values of two anatomical and two behavioural traits for each male morph. This study is, to our knowledge, the first to show disruptive sexual selection in Arachnidae and significantly expands the realm of disruptive selection, by adding one more case to the very few documented instances. These processes, which act entirely within a species, are of particular interest because they could contribute to the evolution of reproductive isolation and sympatric speciation by sexual selection, a controversial topic in evolutionary biology.