Pleistocene glaciations caused the latitudinal gradient of within-species genetic diversity.

Intraspecific genetic diversity is a key aspect of biodiversity. Quaternary climatic change and glaciation influenced intraspecific genetic diversity by promoting range shifts and population size change. However, the extent to which glaciation affected genetic diversity on a global scale is not well established. Here we quantify nucleotide diversity, a common metric of intraspecific genetic diversity, in more than 38,000 plant and animal species using georeferenced DNA sequences from millions of samples. Results demonstrate that tropical species contain significantly more intraspecific genetic diversity than nontropical species. To explore potential evolutionary processes that may have contributed to this pattern, we calculated summary statistics that measure population demographic change and detected significant correlations between these statistics and latitude. We find that nontropical species are more likely to deviate from neutral expectations, indicating that they have historically experienced dramatic fluctuations in population size likely associated with Pleistocene glacial cycles. By analyzing the most comprehensive data set to date, our results imply that Quaternary climate perturbations may be more important as a process driving the latitudinal gradient in species richness than previously appreciated.

phylogatR: Phylogeographic data aggregation and repurposing.

Patterns of genetic diversity within species contain information the history of that species, including how they have responded to historical climate change and how easily the organism is able to disperse across its habitat. More than 40,000 phylogeographic and population genetic investigations have been published to date, each collecting genetic data from hundreds of samples. Despite these millions of data points, meta-analyses are challenging because the synthesis of results across hundreds of studies, each using different methods and forms of analysis, is a daunting and time-consuming task. It is more efficient to proceed by repurposing existing data and using automated data analysis. To facilitate data repurposing, we created a database (phylogatR) that aggregates data from different sources and conducts automated multiple sequence alignments and data curation to provide users with nearly ready-to-analyse sets of data for thousands of species. Two types of scientific research will be made easier by phylogatR: large meta-analyses of thousands of species that can address classic questions in evolutionary biology and ecology, and student- or citizen- science based investigations that will introduce a broad range of people to the analysis of genetic data. phylogatR enhances the value of existing data via the creation of software and web-based tools that enable these data to be recycled and reanalysed and increase accessibility to big data for research laboratories and classroom instructors with limited computational expertise and resources.

Analysis of biodiversity data suggests that mammal species are hidden in predictable places.

SignificanceOnly an estimated 1 to 10% of Earth's species have been formally described. This discrepancy between the number of species with a formal taxonomic description and actual number of species (i.e., the Linnean shortfall) hampers research across the biological sciences. To explore whether the Linnean shortfall results from poor taxonomic practice or not enough taxonomic effort, we applied machine-learning techniques to build a predictive model to identify named species that are likely to contain hidden diversity. Results indicate that small-bodied species with large, climatically variable ranges are most likely to contain hidden species. These attributes generally match those identified in the taxonomic literature, indicating that the Linnean shortfall is caused by societal underinvestment in taxonomy rather than poor taxonomic practice.

The impact of climate change on western Plethodon salamanders' distribution.

AIM: Given that salamanders have experienced large shifts in their distributions over time, we determined how each species of Plethodon in the Pacific Northwest would respond to climate change. We incorporated several greenhouse scenarios both on a species-by-species basis, and also using phylogenetic groups, with the aim to determine the best course of action in managing land area to conserve diversity in this group. LOCATION: Pacific Northwest of the United States (northern CA, OR, WA, ID, and MT). MAJOR TAXA STUDIED: Western Plethodon salamanders. METHODS: Species distribution models were estimated using MaxEnt for the current time period and for several future climate scenarios using bioclimatic data layers. We used several methods to quantify the change in habitat suitability over time from the models. We explored aspects of the climate layers to determine whether we can expect a concerted response to climate change due to similarity in ecological niche or independent responses that could be harder to manage. RESULTS: The distribution of western Plethodon salamander species is strongly influenced by precipitation and less so by temperature. Species responses to climate change resulted in both increases and decreases in predicted suitable habitat, though most species ranges do not contract, especially when taken as a phylogenetic group. MAIN CONCLUSIONS: While some established habitats may become more or less climatically suitable, the overall distribution of species in this group is unlikely to be significantly affected. Clades of Plethodon species are unlikely to be in danger of extirpation despite the possibility that individual species may be threatened as a result of limited distributions. Grouping species into lineages with similar geographic ranges can be a viable method of determining conservation needs. More biotic and dispersal information is needed to determine the true impact that changes in climate will have on the distribution of Plethodon species.

Identifying model violations under the multispecies coalescent model using P2C2M.SNAPP.

Phylogenetic estimation under the multispecies coalescent model (MSCM) assumes all incongruence among loci is caused by incomplete lineage sorting. Therefore, applying the MSCM to datasets that contain incongruence that is caused by other processes, such as gene flow, can lead to biased phylogeny estimates. To identify possible bias when using the MSCM, we present P2C2M.SNAPP. P2C2M.SNAPP is an R package that identifies model violations using posterior predictive simulation. P2C2M.SNAPP uses the posterior distribution of species trees output by the software package SNAPP to simulate posterior predictive datasets under the MSCM, and then uses summary statistics to compare either the empirical data or the posterior distribution to the posterior predictive distribution to identify model violations. In simulation testing, P2C2M.SNAPP correctly classified up to 83% of datasets (depending on the summary statistic used) as to whether or not they violated the MSCM model. P2C2M.SNAPP represents a user-friendly way for researchers to perform posterior predictive model checks when using the popular SNAPP phylogenetic estimation program. It is freely available as an R package, along with additional program details and tutorials.

Predicting plant conservation priorities on a global scale.

The conservation status of most plant species is currently unknown, despite the fundamental role of plants in ecosystem health. To facilitate the costly process of conservation assessment, we developed a predictive protocol using a machine-learning approach to predict conservation status of over 150,000 land plant species. Our study uses open-source geographic, environmental, and morphological trait data, making this the largest assessment of conservation risk to date and the only global assessment for plants. Our results indicate that a large number of unassessed species are likely at risk and identify several geographic regions with the highest need of conservation efforts, many of which are not currently recognized as regions of global concern. By providing conservation-relevant predictions at multiple spatial and taxonomic scales, predictive frameworks such as the one developed here fill a pressing need for biodiversity science.

A pheromone by any other gene would smell as sweet.

Reproductive isolation is the result of either the inability to produce viable and fertile offspring or the avoidance of mating altogether. While these mechanisms can evolve either over time via genetic drift or natural selection, the genetic result is usually a complex set of traits that are often linked. Explaining how reproductive isolation proceeds from the initiation of divergence to the complete prevention of mating is often a difficult task, as the underlying genes for traits associated with reproductive isolation can change via molecular evolution and subsequent protein coding alterations or through alterations of gene expression regulation. In this issue of Molecular Ecology, Treer, Maex, VanBocxlaer, Proost, and Bossuyt () use transcriptomic, proteomic and phylogenetic analyses to show that species-specific sex pheromones are the result of gradual sequence divergence on the same set of proteins in two closely related newt species (Ichthyosaura alpestris and Lissotriton helveticus). This study shows that salamander pheromone systems provide an enticing opportunity to connect the evolution of reproductive isolation to the changes in genes that underlie a key phenotype.

Geographical range size and latitude predict population genetic structure in a global survey.

While genetic diversity within species is influenced by both geographical distance and environmental gradients, it is unclear what other factors are likely to promote population genetic structure. Using a machine learning framework and georeferenced DNA sequences from more than 8000 species, we demonstrate that geographical attributes of the species range, including total size, latitude and elevation, are the most important predictors of which species are likely to contain structured genetic variation. While latitude is well known as an important predictor of biodiversity, our work suggests that it also plays a key role in shaping diversity within species.

The evolution of phylogeographic data sets.

Empirical phylogeographic studies have progressively sampled greater numbers of loci over time, in part motivated by theoretical papers showing that estimates of key demographic parameters improve as the number of loci increases. Recently, next-generation sequencing has been applied to questions about organismal history, with the promise of revolutionizing the field. However, no systematic assessment of how phylogeographic data sets have changed over time with respect to overall size and information content has been performed. Here, we quantify the changing nature of these genetic data sets over the past 20 years, focusing on papers published in Molecular Ecology. We found that the number of independent loci, the total number of alleles sampled and the total number of single nucleotide polymorphisms (SNPs) per data set has improved over time, with particularly dramatic increases within the past 5 years. Interestingly, uniparentally inherited organellar markers (e.g. animal mitochondrial and plant chloroplast DNA) continue to represent an important component of phylogeographic data. Single-species studies (cf. comparative studies) that focus on vertebrates (particularly fish and to some extent, birds) represent the gold standard of phylogeographic data collection. Based on the current trajectory seen in our survey data, forecast modelling indicates that the median number of SNPs per data set for studies published by the end of the year 2016 may approach ~20,000. This survey provides baseline information for understanding the evolution of phylogeographic data sets and underscores the fact that development of analytical methods for handling very large genetic data sets will be critical for facilitating growth of the field.

Historical Species Distribution Models Predict Species Limits in Western Plethodon Salamanders.

Allopatry is commonly used to predict boundaries in species delimitation investigations under the assumption that currently allopatric distributions are indicative of reproductive isolation; however, species ranges are known to change over time. Incorporating a temporal perspective of geographic distributions should improve species delimitation; to explore this, we investigate three species of western Plethodon salamanders that have shifted their ranges since the end of the Pleistocene. We generate species distribution models (SDM) of the current range, hindcast these models onto a climatic model 21 Ka, and use three molecular approaches to delimit species in an integrated fashion. In contrast to expectations based on the current distribution, we detect no independent lineages in species with allopatric and patchy distributions (Plethodon vandykei and Plethodon larselli). The SDMs indicate that probable habitat is more expansive than their current range, especially during the last glacial maximum (LGM) (21 Ka). However, with a contiguous distribution, two independent lineages were detected in Plethodon idahoensis, possibly due to isolation in multiple glacial refugia. Results indicate that historical SDMs are a better predictor of species boundaries than current distributions, and strongly imply that researchers should incorporate SDM and hindcasting into their investigations and the development of species hypotheses.

Model choice for phylogeographic inference using a large set of models.

Model-based analyses are common in phylogeographic inference because they parameterize processes such as population division, gene flow and expansion that are of interest to biologists. Approximate Bayesian computation is a model-based approach that can be customized to any empirical system and used to calculate the relative posterior probability of several models, provided that suitable models can be identified for comparison. The question of how to identify suitable models is explored using data from Plethodon idahoensis, a salamander that inhabits the North American inland northwest temperate rainforest. First, we conduct an ABC analysis using five models suggested by previous research, calculate the relative posterior probabilities and find that a simple model of population isolation has the best fit to the data (PP=0.70). In contrast to this subjective choice of models to include in the analysis, we also specify models in a more objective manner by simulating prior distributions for 143 models that included panmixia, population isolation, change in effective population size, migration and range expansion. We then identify a smaller subset of models for comparison by generating an expectation of the highest posterior probability that a false model is likely to achieve due to chance and calculate the relative posterior probabilities of only those models that exceed this expected level. A model that parameterized divergence with population expansion and gene flow in one direction offered the best fit to the P. idahoensis data (in contrast to an isolation-only model from the first analysis). Our investigation demonstrates that the determination of which models to include in ABC model choice experiments is a vital component of model-based phylogeographic analysis.

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.

How to fail at species delimitation.

Species delimitation is the act of identifying species-level biological diversity. In recent years, the field has witnessed a dramatic increase in the number of methods available for delimiting species. However, most recent investigations only utilize a handful (i.e. 2-3) of the available methods, often for unstated reasons. Because the parameter space that is potentially relevant to species delimitation far exceeds the parameterization of any existing method, a given method necessarily makes a number of simplifying assumptions, any one of which could be violated in a particular system. We suggest that researchers should apply a wide range of species delimitation analyses to their data and place their trust in delimitations that are congruent across methods. Incongruence across the results from different methods is evidence of either a difference in the power to detect cryptic lineages across one or more of the approaches used to delimit species and could indicate that assumptions of one or more of the methods have been violated. In either case, the inferences drawn from species delimitation studies should be conservative, for in most contexts it is better to fail to delimit species than it is to falsely delimit entities that do not represent actual evolutionary lineages.