The phylogenomic and biogeographic history of the gartersnakes, watersnakes, and allies (Natricidae: Thamnophiini).

North American Thamnophiini (gartersnakes, watersnakes, brownsnakes, and swampsnakes) are an ecologically and phenotypically diverse temperate clade of snakes representing 61 species across 10 genera. In this study, we estimate phylogenetic trees using âˆ¼3,700 ultraconserved elements (UCEs) for 76 specimens representing 75% of all Thamnophiini species. We infer phylogenies using multispecies coalescent methods and time calibrate them using the fossil record. We also conducted ancestral area estimation to identify how major biogeographic boundaries in North America affect broadscale diversification in the group. While most nodes exhibited strong statistical support, analysis of concordant data across gene trees reveals substantial heterogeneity. Ancestral area estimation demonstrated that the genus Thamnophis was the only taxon in this subfamily to cross the Western Continental Divide, even as other taxa dispersed southward toward the tropics. Additionally, levels of gene tree discordance are overall higher in transition zones between bioregions, including the Rocky Mountains. Therefore, the Western Continental Divide may be a significant transition zone structuring the diversification of Thamnophiini during the Neogene and Pleistocene. Here we show that despite high levels of discordance across gene trees, we were able to infer a highly resolved and well-supported phylogeny for Thamnophiini, which allows us to understand broadscale patterns of diversity and biogeography.

Applying stochastic and Bayesian integral projection modeling to amphibian population viability analysis.

Integral projection models (IPMs) can estimate the population dynamics of species for which both discrete life stages and continuous variables influence demographic rates. Stochastic IPMs for imperiled species, in turn, can facilitate population viability analyses (PVAs) to guide conservation decision-making. Biphasic amphibians are globally distributed, often highly imperiled, and ecologically well suited to the IPM approach. Herein, we present a stochastic size- and stage-structured IPM for a biphasic amphibian, the U.S. federally threatened California tiger salamander (CTS) (Ambystoma californiense). This Bayesian model reveals that CTS population dynamics show greatest elasticity to changes in juvenile and metamorph growth and that populations are likely to experience rapid growth at low density. We integrated this IPM with climatic drivers of CTS demography to develop a PVA and examined CTS extinction risk under the primary threats of habitat loss and climate change. The PVA indicated that long-term viability is possible with surprisingly high (20%-50%) terrestrial mortality but simultaneously identified likely minimum terrestrial buffer requirements of 600-1000 m while accounting for numerous parameter uncertainties through the Bayesian framework. These analyses underscore the value of stochastic and Bayesian IPMs for understanding both climate-dependent taxa and those with cryptic life histories (e.g., biphasic amphibians) in service of ecological discovery and biodiversity conservation. In addition to providing guidance for CTS recovery, the contributed IPM and PVA supply a framework for applying these tools to investigations of ecologically similar species.

Geography is more important than life history in the recent diversification of the tiger salamander complex.

The North American tiger salamander species complex, including its best-known species, the Mexican axolotl, has long been a source of biological fascination. The complex exhibits a wide range of variation in developmental life history strategies, including populations and individuals that undergo metamorphosis; those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis); and those that do both. The evolution of a paedomorphic life history state is thought to lead to increased population genetic differentiation and ultimately reproductive isolation and speciation, but the degree to which it has shaped population- and species-level divergence is poorly understood. Using a large multilocus dataset from hundreds of samples across North America, we identified genetic clusters across the geographic range of the tiger salamander complex. These clusters often contain a mixture of paedomorphic and metamorphic taxa, indicating that geographic isolation has played a larger role in lineage divergence than paedomorphosis in this system. This conclusion is bolstered by geography-informed analyses indicating no effect of life history strategy on population genetic differentiation and by model-based population genetic analyses demonstrating gene flow between adjacent metamorphic and paedomorphic populations. This fine-scale genetic perspective on life history variation establishes a framework for understanding how plasticity, local adaptation, and gene flow contribute to lineage divergence. Many members of the tiger salamander complex are endangered, and the Mexican axolotl is an important model system in regenerative and biomedical research. Our results chart a course for more informed use of these taxa in experimental, ecological, and conservation research.

Does breeding season variation affect evolution of a sexual signaling trait in a tropical lizard clade?

Sexually selected traits can be expected to increase in importance when the period of sexual behavior is constrained, such as in seasonally restricted breeders. Anolis lizard male dewlaps are classic examples of multifaceted signaling traits, with demonstrated intraspecific reproductive function reflected in courtship behavior. Fitch and Hillis found a correlation between dewlap size and seasonality in mainland Anolis using traditional statistical methods and suggested that seasonally restricted breeding seasons enhanced the differentiation of this signaling trait. Here, we present two tests of the Fitch-Hillis Hypothesis using new phylogenetic and morphological data sets for 44 species of Mexican Anolis. A significant relationship between dewlap size and seasonality is evident in phylogenetically uncorrected analyses but erodes once phylogeny is accounted for. This loss of strong statistical support for a relationship between a key aspect of dewlap morphology and seasonality also occurs within a species complex (A. sericeus group) that inhabits seasonal and aseasonal environments. Our results fail to support seasonality as a strong driver of evolution of Anolis dewlap size. We discuss the implications of our results and the difficulty of disentangling the strength of single mechanisms on trait evolution when multiple selection pressures are likely at play.

Phylogeography of a widespread lizard complex reflects patterns of both geographic and ecological isolation.

A primary challenge for modern phylogeography is understanding how ecology and geography, both contemporary and historical, shape the spatial distribution and evolutionary histories of species. Phylogeographic patterns are the result of many factors, including geology, climate, habitat, colonization history and lineage-specific constraints. Assessing the relative influences of these factors is difficult because few species, regions and environments are sampled in enough detail to compare competing hypotheses rigorously and because a particular phylogeographic pattern can potentially result from different evolutionary scenarios. The silky anoles (Anolis sericeus complex) of Central America and Mexico are abundant and found in all types of lowland terrestrial habitat, offering an excellent opportunity to test the relative influences of the factors affecting diversification. Here, we performed a range-wide statistical phylogeographic analysis on restriction site-associated DNA (RAD) markers from silky anoles and compared the phylogeographic patterns we recovered to historical and contemporary environmental and topographic data. We constructed niche models to compare niche overlap between sister lineages and conducted coalescent simulations to characterize how the major lineages of silky anoles have diverged. Our results revealed that the mode of divergence for major lineage diversification events was geographic isolation, resulting in ecological divergence between lineages, followed by secondary contact. Moreover, comparisons of parapatric sister lineages suggest that ecological niche divergence contributed to isolation by environment in this system, reflecting the natural history differences among populations in divergent environments.

Comparative Evolution of an Archetypal Adaptive Radiation: Innovation and Opportunity in Anolis Lizards.

Adaptive radiation is a widely recognized pattern of evolution wherein substantial phenotypic change accompanies rapid speciation. Adaptive radiation may be triggered by environmental opportunities resulting from dispersal to new areas or via the evolution of traits, called key innovations, that allow for invasion of new niches. Species sampling is a known source of bias in many comparative analyses, yet classic adaptive radiations have not been studied comparatively with comprehensively sampled phylogenies. In this study, we use unprecedented comprehensive phylogenetic sampling of Anolis lizard species to examine comparative evolution in this well-studied adaptive radiation. We compare adaptive radiation models within Anolis and in the Anolis clade and a potential sister lineage, the Corytophanidae. We find evidence for island (i.e., opportunity) effects and no evidence for trait (i.e., key innovation) effects causing accelerated body size evolution within Anolis. However, island effects are scale dependent: when Anolis and Corytophanidae are analyzed together, no island effect is evident. We find no evidence for an island effect on speciation rate and tenuous evidence for greater speciation rate due to trait effects. These results suggest the need for precision in treatments of classic adaptive radiations such as Anolis and further refinement of the concept of adaptive radiation.

A Phylogenetic, Biogeographic, and Taxonomic study of all Extant Species of Anolis (Squamata; Iguanidae).

Anolis lizards (anoles) are textbook study organisms in evolution and ecology. Although several topics in evolutionary biology have been elucidated by the study of anoles, progress in some areas has been hampered by limited phylogenetic information on this group. Here, we present a phylogenetic analysis of all 379 extant species of Anolis, with new phylogenetic data for 139 species including new DNA data for 101 species. We use the resulting estimates as a basis for defining anole clade names under the principles of phylogenetic nomenclature and to examine the biogeographic history of anoles. Our new taxonomic treatment achieves the supposed advantages of recent subdivisions of anoles that employed ranked Linnaean-based nomenclature while avoiding the pitfalls of those approaches regarding artificial constraints imposed by ranks. Our biogeographic analyses demonstrate complexity in the dispersal history of anoles, including multiple crossings of the Isthmus of Panama, two invasions of the Caribbean, single invasions to Jamaica and Cuba, and a single evolutionary dispersal from the Caribbean to the mainland that resulted in substantial anole diversity. Our comprehensive phylogenetic estimate of anoles should prove useful for rigorous testing of many comparative evolutionary hypotheses. [Anoles; biogeography; lizards; Neotropics; phylogeny; taxonomy].

Resurrection of Anolis ustus Cope, 1864 from synonymy with Anolis sericeus Hallowell, 1856 (Squamata, Dactyloidae).

In this study, based on a morphological analysis, the resurrection of the name Anolis ustus Cope 1864, is proposed for populations from the Yucatán Peninsula (Campeche, Yucatán, and Quintana Roo, Mexico, and Belize), formerly referred as Anolis sericeus Hallowell, 1856. Anolis ustus differs from Anolis sericeus by its mean snout-vent length and number of gorgetal scales in males, in tibia length and head width in females, and dorsal and ventral scales for both sexes. In addition, Anolis ustus has a small dewlap of similar size between males and females, whereas in Anolis sericeus males have a dewlap much larger than that of the females. These characteristics allow Anolis ustus to be identified within the Anolis sericeus complex. In this study, a description of the characteristics of the hemipenis is also provided, and its importance in the taxonomy of Anolis is discussed.

Delayed life history effects, multilevel selection, and evolutionary trade-offs in the California tiger salamander.

Delayed life history effects (DLHEs) occur when fitness in one life stage affects fitness in subsequent life stages. Given their biphasic life cycle, pond-breeding amphibians provide a natural system for studying DLHEs, although these effects are not restricted to species with biphasic life histories. In this study, we used multiple mark-recapture techniques enabled by a large trapping array to monitor components of fitness and resulting DLHEs in a population of the endangered California tiger salamander (Ambystoma californiense). We found that DLHEs are prominent across all life stage transitions and that there is variation in whether selection acts primarily at the individual or cohort level. We also demonstrated that there is more than an order of magnitude variation in mean cohort fitness, providing tremendous variation for DLHEs to act upon. We documented an evolutionary trade-off between mass at emergence and date of emergence, which may play a role in maintaining the variation in mass (fitness) at emergence. A literature review revealed that such high levels of intercohort variation occur in many other pond-breeding amphibians, and that appropriately documenting the magnitude of intercohort variation requires long-term studies (roughly two population turnovers). Given the profound effect that DLHEs can have on population dynamics, quantifying intercohort variation in mean fitness and the level(s) at which selection acts will be very important for developing accurate models of population dynamics. In general, when developing models of population dynamics, more attention should be paid to variation in mean fitness and not just variation in total numbers.

Cryptic seedling herbivory by nocturnal introduced generalists impacts survival, performance of native and exotic plants.

Although much of the theory on the success of invasive species has been geared at escape from specialist enemies, the impact of introduced generalist invertebrate herbivores on both native and introduced plant species has been underappreciated. The role of nocturnal invertebrate herbivores in structuring plant communities has been examined extensively in Europe, but less so in North America. Many nocturnal generalists (slugs, snails, and earwigs) have been introduced to North America, and 96% of herbivores found during a night census at our California Central Valley site were introduced generalists. We explored the role of these herbivores in the distribution, survivorship, and growth of 12 native and introduced plant species from six families. We predicted that introduced species sharing an evolutionary history with these generalists might be less vulnerable than native plant species. We quantified plant and herbivore abundances within our heterogeneous site and also established herbivore removal experiments in 160 plots spanning the gamut of microhabitats. As 18 collaborators, we checked 2000 seedling sites every day for three weeks to assess nocturnal seedling predation. Laboratory feeding trials allowed us to quantify the palatability of plant species to the two dominant nocturnal herbivores at the site (slugs and earwigs) and allowed us to account for herbivore microhabitat preferences when analyzing attack rates on seedlings. The relationship between local slug abundance and percent cover of five common plant taxa at the field site was significantly negatively associated with the mean palatability of these taxa to slugs in laboratory trials. Moreover, seedling mortality of 12 species in open-field plots was positively correlated with mean palatability of these taxa to both slugs and earwigs in laboratory trials. Counter to expectations, seedlings of native species were neither more vulnerable nor more palatable to nocturnal generalists than those of introduced species. Growth comparison of plants within and outside herbivore exclosures also revealed no differences between native and introduced plant species, despite large impacts of herbivores on growth. Cryptic nocturnal predation on seedlings was common and had large effects on plant establishment at our site. Without intensive monitoring, such predation could easily be misconstrued as poor seedling emergence.