Turtle soup, Prohibition, and the population genetic structure of Diamondback Terrapins (Malaclemys terrapin).

Diamondback terrapins (Malaclemys terrapin) were a popular food item in early twentieth century America, and were consumed in soup with sherry. Intense market demand for terrapin meat resulted in population declines, notably along the Atlantic seaboard. Efforts to supply terrapins to markets resulted in translocation events, as individuals were moved about to stock terrapin farms. However, in 1920 the market for turtle soup buckled with the enactment of the eighteenth amendment to the United States' Constitution-which initiated the prohibition of alcoholic drinks-and many terrapin fisheries dumped their stocks into local waters. We used microsatellite data to show that patterns of genetic diversity along the terrapin's coastal range are consistent with historical accounts of translocation and cultivation activities. We identified possible instances of human-mediated dispersal by estimating gene flow over historical and contemporary timescales, Bayesian model testing, and bottleneck tests. We recovered six genotypic clusters along the Gulf and Atlantic coasts with varying degrees of admixture, including increased contemporary gene flow from Texas to South Carolina, from North Carolina to Maryland, and from North Carolina to New York. In addition, Bayesian models incorporating translocation events outperformed stepping-stone models. Finally, we were unable to detect population bottlenecks, possibly due to translocation reintroducing genetic diversity into bottlenecked populations. Our data suggest that current patterns of genetic diversity in the terrapin were altered by the demand for turtle soup followed by the enactment of alcohol prohibition. In addition, our study shows that population genetic tools can elucidate metapopulation dynamics in taxa with complex genetic histories impacted by anthropogenic activities.

Multilocus Phylogeography and Species Delimitation in the Cumberland Plateau Salamander, Plethodon kentucki: Incongruence among Data Sets and Methods.

Species are a fundamental unit of biodiversity, yet can be challenging to delimit objectively. This is particularly true of species complexes characterized by high levels of population genetic structure, hybridization between genetic groups, isolation by distance, and limited phenotypic variation. Previous work on the Cumberland Plateau Salamander, Plethodon kentucki, suggested that it might constitute a species complex despite occupying a relatively small geographic range. To examine this hypothesis, we sampled 135 individuals from 43 populations, and used four mitochondrial loci and five nuclear loci (5693 base pairs) to quantify phylogeographic structure and probe for cryptic species diversity. Rates of evolution for each locus were inferred using the multidistribute package, and time calibrated gene trees and species trees were inferred using BEAST 2 and *BEAST 2, respectively. Because the parameter space relevant for species delimitation is large and complex, and all methods make simplifying assumptions that may lead them to fail, we conducted an array of analyses. Our assumption was that strongly supported species would be congruent across methods. Putative species were first delimited using a Bayesian implementation of the GMYC model (bGMYC), Geneland, and Brownie. We then validated these species using the genealogical sorting index and BPP. We found substantial phylogeographic diversity using mtDNA, including four divergent clades and an inferred common ancestor at 14.9 myr (95% HPD: 10.8-19.7 myr). By contrast, this diversity was not corroborated by nuclear sequence data, which exhibited low levels of variation and weak phylogeographic structure. Species trees estimated a far younger root than did the mtDNA data, closer to 1.0 myr old. Mutually exclusive putative species were identified by the different approaches. Possible causes of data set discordance, and the problem of species delimitation in complexes with high levels of population structure and introgressive hybridization, are discussed.

Spatiotemporal analysis of gene flow in Chesapeake Bay Diamondback Terrapins (Malaclemys terrapin).

There is widespread concern regarding the impacts of anthropogenic activities on connectivity among populations of plants and animals, and understanding how contemporary and historical processes shape metapopulation dynamics is crucial for setting appropriate conservation targets. We used genetic data to identify population clusters and quantify gene flow over historical and contemporary time frames in the Diamondback Terrapin (Malaclemys terrapin). This species has a long and complicated history with humans, including commercial overharvesting and subsequent translocation events during the early twentieth century. Today, terrapins face threats from habitat loss and mortality in fisheries bycatch. To evaluate population structure and gene flow among Diamondback Terrapin populations in the Chesapeake Bay region, we sampled 617 individuals from 15 localities and screened individuals at 12 polymorphic microsatellite loci. Our goals were to demarcate metapopulation structure, quantify genetic diversity, estimate effective population sizes, and document temporal changes in gene flow. We found that terrapins in the Chesapeake Bay region harbour high levels of genetic diversity and form four populations. Effective population sizes were variable. Among most population comparisons, estimates of historical and contemporary terrapin gene flow were generally low (m ≈ 0.01). However, we detected a substantial increase in contemporary gene flow into Chesapeake Bay from populations outside the bay, as well as between two populations within Chesapeake Bay, possibly as a consequence of translocations during the early twentieth century. Our study shows that inferences across multiple time scales are needed to evaluate population connectivity, especially as recent changes may identify threats to population persistence.

Predator-mediated natural selection on the wings of the damselfly Calopteryx splendens: differences in selection among trait types.

Traits that increase mating success in males may come at a cost, such as an increased risk of predation. However, predator-mediated selection is challenging to document in natural populations, hampering our understanding of the trade-offs between sexual selection and predation. Here we report on a study of predator-mediated natural selection on wing traits in the damselfly Calopteryx splendens, the males of which possess conspicuous wing patches. Wagtails (genus Motacilla) are important avian predators of C. splendens, capturing them in flight and removing the wings prior to consumption. Using geometric morphometric techniques, we quantified the strength and mode of selection on wing traits by comparing wings from depredated individuals with the standing variation present in the population. Our results reveal that predator-mediated selection is stronger on secondary sexual characters than on size and shape, suggesting that traits related to flight performance are closer to their adaptive peaks. This could be a consequence of the long-term evolutionary association with avian predators, whereas stronger selection on conspicuous secondary sexual traits may reflect trade-offs between sexual and natural selection. Finally, even though C. splendens possesses nearly identical fore- and hindwings, we found evidence for divergent selection between them.

Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation.

Polymorphism may play an important role in speciation because new species could originate from the distinctive morphs observed in polymorphic populations. However, much remains to be understood about the process by which morphs found new species. To detail the steps of this mode of speciation, we studied the geographic variation and evolutionary history of a throat color polymorphism that distinguishes the "rock-paper-scissors" mating strategies of the side-blotched lizard, Uta stansburiana. We found that the polymorphism is geographically widespread and has been maintained for millions of years. However, there are many populations with reduced numbers of throat color morphs. Phylogenetic reconstruction showed that the polymorphism is ancestral, but it has been independently lost eight times, often giving rise to morphologically distinct subspecies/species. Changes to the polymorphism likely involved selection because the allele for one particular male strategy, the "sneaker" morph, has been lost in all cases. Polymorphism loss was associated with accelerated evolution of male size, female size, and sexual dimorphism, which suggests that polymorphism loss can promote rapid divergence among populations and aid species formation.

Alternative mating strategies and the evolution of sexual size dimorphism in the side-blotched lizard, Uta stansburiana: a population-level comparative analysis.

Population-level comparative analyses can link microevolutionary processes within populations to macroevolutionary patterns of diversification. We used the comparative method to study the evolution of sexual size dimorphism (SSD) among populations of side-blotched lizards (Uta stansburiana). Uta stansburiana is polymorphic for different male mating and female life-history strategies in some populations, but monomorphic in others. We tested whether intrasexual selection among males, fecundity selection on females, and the presence of polymorphic strategies affected levels of SSD. We first resolved a phylogeny for 41 populations across the range of the species and documented a substantial regional structure. Our intraspecific data had significant phylogenetic signal, and correcting for phylogeny using independent contrasts had large effects on our results. Polymorphic populations had male-biased SSD and changes in male body size, levels of tail breaks, and SSD consistent with the intrasexual selection hypothesis. Monomorphic populations had changes in female size, clutch size, and SSD consistent with the fecundity selection hypothesis. Fecundity selection is a likely cause of some monomorphic populations having no SSD or female-biased SSD. Our results suggest that changes in mating strategies are associated with phenotypic diversification and multiple evolutionary forces can shape SSD.

Pronounced phylogeographic structure on a small spatial scale: geomorphological evolution and lineage history in the salamander ring species Ensatina eschscholtzii in central coastal California.

The salamander Ensatina eschscholtzii is a classic example of a ring species, and has an intricate biogeographic history. Within a part of the ring distribution, earlier work using allozymes disclosed high levels of genetic structure in central coastal California, where the subspecies oregonensis, xanthoptica, and eschscholtzii meet. We used mitochondrial cytochrome b sequences to further examine patterns of divergence in this area, including data from 155 localities (309 individuals). Our focus is on the documentation of population-level haplotype lineages. We show that oregonensis is represented by two unrelated, phenotypically similar clades, both of which possess substantial substructure of their own. The subspecies xanthoptica includes two lineages that differ in phenotype, one of which has colonized the foothills of the Sierra Nevada. The subspecies eschscholtzii occurs mainly to the south, but some populations from a northern lineage extend into the Monterey Bay region, where they approach xanthoptica geographically. In sum, populations in the central coastal California region form a distributional patchwork, including three subspecies, three clades (which differ from the three subspecies), and ten haplotype lineages. We conclude that such striking levels of phylogeographic structure reflect interspersed episodes of spatial fragmentation, in part driven by the complex geomorphological evolution of the California Coast Range system.

Why does the yellow-eyed Ensatina have yellow eyes? Batesian mimicry of Pacific newts (genus Taricha) by the salamander Ensatina eschscholtzii xanthoptica.

Color patterns commonly vary geographically within species, but it is rare that such variation corresponds with divergent antipredator strategies. The polymorphic salamander Ensatina eschscholtzii, however, may represent such a case. In this species, most subspecies are cryptically colored, whereas E. e. xanthoptica, the Yellow eyed ensatina, is hypothesized to be an aposematic mimic of highly toxic Pacific newts (genus Taricha). To test the mimicry hypothesis, we conducted feeding trials using Western Scrub-Jays, Aphelocoma californica. In every feeding trial, we found that jays, following presentation with the presumed model (T. torosa), were more hesitant to contact the presumed mimic (E. e. xanthoptica) than a control subspecies lacking the postulated aposematic colors (E. e. oregonensis). The median time to contact was 315 sec for the mimic and 52 sec for the control. These results support the mimicry hypothesis, and we suggest that E. e. xanthoptica is likely a Batesian mimic, rather a Müllerian or quasi-Batesian mimic, of Pacific newts.

Isolation by distance and post-glacial range expansion in the rough-skinned newt, Taricha granulosa.

Allozymes and mitochondrial DNA sequences were used to examine the phylogeographical history of the rough-skinned newt, Taricha granulosa, in western North America. Nineteen populations were analysed for allozyme variation at 45 loci, and 23 populations were analysed for cytochrome b sequence variation. Both data sets agree that populations in the southern part of the range are characterized by isolation by distance, whereas northern populations fit the expectations of a recent range expansion. However, the northern limit of isolation by distance (and the southern limit of range expansion) is located in Oregon State by the mtDNA data, and in Washington State by the allozyme data. Nevertheless, both data sets are consistent with the known Pleistocene history of western North America, with phylogenetically basal populations in central and northern California, and a recent range expansion in the north following the retreat of the Cordilleran ice sheet 10,000 years ago. Additionally, a population in Idaho, previously considered introduced from central California based on morphometric analyses, possesses a distinct mtDNA haplotype, suggesting it could be native. The relevance of these results for Pacific Northwest biogeography is discussed.