Inferring Species Trees from Gene Trees in a Radiation of California Trapdoor Spiders (Araneae, Antrodiaetidae, Aliatypus)

The California Floristic Province is a biodiversity hotspot, reflecting a complex geologic history, strong selective gradients, and a heterogeneous landscape. These factors have led to high endemic diversity across many lifeforms within this region, including the richest diversity of mygalomorph spiders (tarantulas, trapdoor spiders, and kin) in North America. The trapdoor spider genus Aliatypus encompasses twelve described species, eleven of which are endemic to California. Several Aliatypus species show disjunct distributional patterns in California (some are found on both sides of the vast Central Valley), and the genus as a whole occupies an impressive variety of habitats.We collected specimens from 89 populations representing all described species. DNA sequence data were collected from seven gene regions, including two newly developed for spider systematics. Bayesian inference (in individual gene tree and species tree approaches) recovered a general "3 clade" structure for the genus (A. gulosus, californicus group, erebus group), with three other phylogenetically isolated species differing slightly in position across different phylogenetic analyses. Because of extremely high intraspecific divergences in mitochondrial COI sequences, the relatively slowly evolving 28S rRNA gene was found to be more useful than mitochondrial data for identification of morphologically indistinguishable immatures. For multiple species spanning the Central Valley, explicit hypothesis testing suggests a lack of monophyly for regional populations (e.g., western Coast Range populations). Phylogenetic evidence clearly shows that syntopy is restricted to distant phylogenetic relatives, consistent with ecological niche conservatism.This study provides fundamental insight into a radiation of trapdoor spiders found in the biodiversity hotspot of California. Species relationships are clarified and undescribed lineages are discovered, with more geographic sampling likely to lead to additional species diversity. These dispersal-limited taxa provide novel insight into the biogeography and Earth history processes of California

Poor fit to the multispecies coalescent is widely detectable in empirical data

Model checking is a critical part of Bayesian data analysis, yet it remains largely unused in systematic studies. Phylogeny estimation has recently moved into an era of increasingly complex models that simultaneously account for multiple evolutionary processes, the statistical fit of these models to the data has rarely been tested. Here we develop a posterior predictive simulation-based model check for a commonly used multispecies coalescent model, implemented in *BEAST, and apply it to 25 published data sets. We show that poor model fit is detectable in the majority of data sets; that this poor fit can mislead phylogenetic estimation; and that in some cases it stems from processes of inherent interest to systematists. We suggest that as systematists scale up to phylogenomic data sets, which will be subject to a heterogeneous array of evolutionary processes, critically evaluating the fit of models to data is an analytical step that can no longer be ignored. [Gene duplication and extinction; gene tree; hybridization; model fit; multispecies coalescent; next-generation sequencing; posterior predictive simulation; species delimitation; species tree.] © The Author(s) 2013

Inferring Processes of Coevolutionary Diversification in a Community of Panamanian Strangler Figs and Associated Pollinating Wasps

The fig and pollinator wasp obligate mutualism is diverse (~750 described species), ecologically important, and ancient (~80-90 Ma), providing model systems for generating and testing many questions in evolution and ecology. Once thought to be a prime example of strict one-to-one cospeciation, current thinking suggests that genera of pollinator wasps coevolve with corresponding subsections of figs, but the degree to which cospeciation or other processes contributes to the association at finer scales is unclear. Here we use genome-wide sequence data from a community of Panamanian strangler figs (Ficus subgenus Urostigma, section Americana) and associated fig wasp pollinators (Pegoscapus spp.) to infer the process of coevolutionary diversification in this obligate mutualism. Using a model-based approach adapted from the study of gene family evolution, our results indicate pervasive and ongoing host switching of pollinator wasps at this fine phylogenetic and regional scale. Although the model estimates a modest amount of cospeciation, simulations reveal this signal to be consistent with levels of co-association expected under a model of free host switching. Our findings provide an outline for testing how ecological and evolutionary processes can be modeled to evaluate the history of association of interacting lineages in a phylogenetic framework

Data from: Phylogeographic concordance factors quantify phylogeographic congruence among co-distributed species in the Sarracenia alata pitcher plant system

Comparative phylogeographic investigations have identified congruent phylogeographic breaks in co-distributed species in nearly every region of the world. The qualitative assessments of phylogeographic patterns traditionally used to identify such breaks, however, are limited because they rely on identifying monophyletic groups across species and do not account for coalescent stochasticity. Only long-standing phylogeographic breaks are likely to be obvious; many species could have had a concerted response to more recent landscape events, yet possess subtle signs of phylogeographic congruence because ancestral polymorphism has not completely sorted. Here we introduce Phylogeographic Concordance Factors (PCFs), a novel method for quantifying phylogeographic congruence across species. We apply this method to the Sarracenia alata pitcher plant system, a carnivorous plant with a diverse array of commensal organisms. We explore whether a group of ecologically associated arthropods have co-diversified with the host pitcher plant, and identify if there is a positive correlation between ecological interaction and PCFs. Results demonstrate that multiple arthropods share congruent phylogeographic breaks with S. alata, and provide evidence that the level of ecological association can be used to predict the degree of similarity in the phylogeographic pattern. This study outlines an approach for quantifying phylogeographic congruence, a central concept in biogeographic research

Data from: The carnivorous plant described as Sarracenia alata contains two cryptic species

Modern methods for species delimitation provide biologists with the power to detect cryptic diversity in nearly any system. To illustrate the application of such methods, we collected data (21 sequence loci) from a carnivorous plant in southeastern North America and applied several recently developed methods (Gaussian clustering, Structurama, BPP, spedeSTEM). The pale pitcher plant Sarracenia alata inhabits the southeastern USA along the northern coast of the Gulf of Mexico. Sarracenia alata populations are separated by the Mississippi River and Atchafalaya Basin, a known biogeographical barrier in this region, but the cohesiveness of S. alata as currently classified has not been tested rigorously. Multiple analytical approaches (including allelic clustering and species trees methods) suggest that S. alata comprises two cryptic lineages that correspond to the eastern and western portions of the plant's distribution. That such clear genetic evidence for cryptic diversity exists within S. alata and is in conflict with other sources of data (e.g. morphology, environmental differentiation) illustrates a conundrum faced by those who investigate species boundaries: genetic data are often the first type of data to accumulate evidence of differentiation, but most existing taxonomic treatments are based on nongenetic data. Our results suggest that S. alata as currently described contains two cryptic species, and we recommend the elevation of the western populations to species status

Data from: Do ecological communities disperse across biogeographic barriers as a unit?

Biogeographic barriers have long been implicated as drivers of biological diversification, but how these barriers influence co-occurring taxa can vary depending on factors intrinsic to the organism and in their relationships with other species. Due to the interdependence among taxa, ecological communities present a compelling opportunity to explore how interactions among species may lead to a shared response to historical events. Here we collect single nucleotide polymorphism (SNP) data from five commensal arthropods associated with the Sarracenia alata carnivorous pitcher plant, and test for co-diversification across the Mississippi River, a major biogeographic barrier in the southeastern United States. Population genetic structure in three of the ecologically dependent arthropods mirrors that of the host pitcher plant, with divergence time estimates suggesting two of the species (the pitcher plant moth Exyra semicrocea and a flesh fly Sarcophaga sarraceniae) dispersed synchronously across this barrier along with the pitcher plant. Patterns in population size and genetic diversity suggest the plant and ecologically dependent arthropods dispersed from east to west across the Mississippi River. In contrast, species less dependent on the plant ecologically show discordant phylogeographic patterns. This study demonstrates that ecological relationships may be an important predictor of co-diversification, and supports recent suggestions that organismal trait data should be prominently featured in comparative phylogeographic investigations

Data from: The Sarracenia alata pitcher plant system and obligate arthropod inquilines should be considered an evolutionary community

Aim: The Sarracenia alata pitcher plant and inquiline species comprise an ecological community. These inquilines span the continuum in their ecological association with the host pitcher plant, from species that contain little-to-no interaction with the plant to species that are completely dependent on the plant for their entire life cycle. We are interested in testing if degree of ecological dependence is positively correlated with a shared evolutionary history, and in identifying members of this community that display concordant phylogeographic structure. Location: Southeastern United States Methods: We collected genome-wide sequence data from a set of arthropods that are ecologically-associated with the plant to estimate comparative phylogeographic patterns among the species. We estimated species tree distributions from biallelic unlinked SNP data and used phylogeographic concordance factors (PCFs) to test degree of phylogeographic concordance among community members. In addition, we calculated AMOVAs and FST values to identify population genetic structure across the landscape, and compared these traditional values to the tree-based approach. Results: Obligate members of the pitcher plant community display concordant phylogeographic patterns, suggesting their ecological dependence has manifested itself into a shared evolutionary history. In contrast, two spider species do not contain significant population genetic structure or similar phylogeographic histories, highlighting their loose association with the host pitcher plant. Main conclusion: The Sarracenia alata pitcher plant system should be considered an evolutionary community, where multiple members sharing strong ecological interactions also display concordant phylogeographic structure. This work demonstrates that PCFs provide an important quantitative measure into assessing community structure and illustrate how simulations can be used to assess significance of shared patterns of phylogeographic structure across the landscape

Nexus files for all six loci

DNA sequences for individuals used in all multilocus analyses

Supplemental Material

Supplemental material file