Pascal O. Title

BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees

Summary Understanding the dynamics of speciation, extinction and phenotypic evolution is a central challenge in evolutionary biology. Here, we present BAMMtools, an r package for the analysis and visualization of macroevolutionary dynamics on phylogenetic trees. BAMMtools is a companion package to BAMM, an open-source program for reversible-jump MCMC analyses of diversification and trait evolution. Functions in BAMMtools operate directly on output from the BAMM program. The package is oriented towards reconstructing and visualizing changes in evolutionary rates through time and across clades in a Bayesian statistical framework. BAMMtools enables users to extract credible sets of diversification shifts and to identify diversification histories with the maximum a posteriori probability. Users can compare the fit of alternative diversification models using Bayes factors and by directly comparing model posterior probabilities. By providing a robust framework for quantifying uncertainty in macroevolutionary dynamics, BAMMtools will facilitate inference on the complex mixture of processes that have shaped the distribution of species and phenotypes across the tree of life.

Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds

Thraupidae is the second largest family of birds and represents about 4% of all avian species and 12% of the Neotropical avifauna. Species in this family display a wide range of plumage colors and patterns, foraging behaviors, vocalizations, ecotypes, and habitat preferences. The lack of a complete phylogeny for tanagers has hindered the study of this evolutionary diversity. Here, we present a comprehensive, species-level phylogeny for tanagers using six molecular markers. Our analyses identified 13 major clades of tanagers that we designate as subfamilies. In addition, two species are recognized as distinct branches on the tanager tree. Our topologies disagree in many places with previous estimates of relationships within tanagers, and many long-recognized genera are not monophyletic in our analyses. Our trees identify several cases of convergent evolution in plumage ornaments and bill morphology, and two cases of social mimicry. The phylogeny produced by this study provides a robust framework for studying macroevolutionary patterns and character evolution. We use our new phylogeny to study diversification processes, and find that tanagers show a background model of exponentially declining diversification rates. Thus, the evolution of tanagers began with an initial burst of diversification followed by a rate slowdown. In addition to this background model, two later, clade-specific rate shifts are supported, one increase for Darwins finches and another increase for some species of Sporophila. The rate of diversification within these two groups is exceptional, even when compared to the overall rapid rate of diversification found within tanagers. This study provides the first robust assessment of diversification rates for the Darwins finches in the context of the larger group within which they evolved.

Rates of climatic niche evolution are correlated with species richness in a large and ecologically diverse radiation of songbirds

By employing a recently inferred phylogeny and museum occurrence records, we examine the relationship of ecological niche evolution to diversification in the largest family of songbirds, the tanagers (Thraupidae). We test whether differences in species numbers in the major clades of tanagers can be explained by differences in rate of climatic niche evolution. We develop a methodological pipeline to process and filter occurrence records. We find that, of the ecological variables examined, clade richness is higher in clades with higher climatic niche rate, and that this rate is also greater for clades that occupy a greater extent of climatic space. Additionally, we find that more speciose clades contain species with narrower niche breadths, suggesting that clades in which species are more successful at diversifying across climatic gradients have greater potential for speciation or are more buffered from the risk of extinction.

Minimal effects of latitude on present-day speciation rates in New World birds

The tropics contain far greater numbers of species than temperate regions, suggesting that rates of species formation might differ systematically between tropical and non-tropical areas. We tested this hypothesis by reconstructing the history of speciation in New World (NW) land birds using BAMM, a Bayesian framework for modelling complex evolutionary dynamics on phylogenetic trees. We estimated marginal distributions of present-day speciation rates for each of 2571 species of birds. The present-day rate of speciation varies approximately 30-fold across NW birds, but there is no difference in the rate distributions for tropical and temperate taxa. Using macroevolutionary cohort analysis, we demonstrate that clades with high tropical membership do not produce species more rapidly than temperate clades. For nearly any value of present-day speciation rate, there are far more species in the tropics than the temperate zone. Any effects of latitude on speciation rate are marginal in comparison to the dramatic variation in rates among clades.

envirem: An expanded set of bioclimatic and topographic variables increases flexibility and improves performance of ecological niche modeling

Species distribution modeling is a valuable tool with many applications across ecology and evolutionary biology. The selection of biologically meaningful environmental variables that determine relative habitat suitability is a crucial aspect of the modeling pipeline. The 19 bioclimatic variables from WorldClim are frequently employed, primarily because they are easily accessible and available globally for past, present and future climate scenarios. Yet, the availability of relatively few other comparable environmental datasets potentially limits our ability to select appropriate variables that will most successfully characterize a species’ distribution. We identified a set of 16 climatic and two topographic variables in the literature, which we call the ENVIREM dataset, many of which are likely to have direct relevance to ecological or physiological processes determining species distributions. We generated this set of variables at the same resolutions as WorldClim, for the present, mid-Holocene, and Last Glacial Maximum (LGM). For 20 North American vertebrate species, we then assessed whether including the ENVIREM variables led to improved species distribution models compared to models using only the existing WorldClim variables. We found that including the ENVIREM dataset in the pool of variables to select from led to substantial improvements in niche modeling performance in 13 out of 20 species. We also show that, when comparing models constructed with different environmental variables, differences in projected distributions were often greater in the LGM than in the present. These variables are worth consideration in species distribution modeling applications, especially as many of the variables have direct links to processes important for species ecology. We provide these variables for download at multiple resolutions and for several time periods at envirem.github.io. Furthermore, we have written the ‘envirem’ R package to facilitate the generation of these variables from other input datasets.

Tests of species‐specific models reveal the importance of drought in postglacial range shifts of a Mediterranean‐climate tree: insights from integrative distributional, demographic and coalescent modelling and ABC model selection

Past climate change has caused shifts in species distributions and undoubtedly impacted patterns of genetic variation, but the biological processes mediating responses to climate change, and their genetic signatures, are often poorly understood. We test six species‐specific biologically informed hypotheses about such processes in canyon live oak (Quercus chrysolepis) from the California Floristic Province. These hypotheses encompass the potential roles of climatic niche, niche multidimensionality, physiological trade‐offs in functional traits, and local‐scale factors (microsites and local adaptation within ecoregions) in structuring genetic variation. Specifically, we use ecological niche models (ENMs) to construct temporally dynamic landscapes where the processes invoked by each hypothesis are reflected by differences in local habitat suitabilities. These landscapes are used to simulate expected patterns of genetic variation under each model and evaluate the fit of empirical data from 13 microsatellite loci genotyped in 226 individuals from across the species range. Using approximate Bayesian computation (ABC), we obtain very strong support for two statistically indistinguishable models: a trade‐off model in which growth rate and drought tolerance drive habitat suitability and genetic structure, and a model based on the climatic niche estimated from a generic ENM, in which the variables found to make the most important contribution to the ENM have strong conceptual links to drought stress. The two most probable models for explaining the patterns of genetic variation thus share a common component, highlighting the potential importance of seasonal drought in driving historical range shifts in a temperate tree from a Mediterranean climate where summer drought is common.

Genetic variation among western populations of the Horned Lark (Eremophila alpestris) indicates recent colonization of the Channel Islands off southern California, mainland-bound dispersal, and postglacial range shifts

ABSTRACT The Channel Islands off the coast of southern California host >50 species of terrestrial vertebrates with varying degrees of phenotypic differentiation. However, most organisms that breed on the Channel Islands remain unstudied with respect to genetic differentiation from mainland populations. By comparing patterns of genetic variation between the Channel Islands and the mainland, we aimed to further our understanding of the role that the Channel Islands have played in diversification of the North American biota. We evaluated long-standing, untested hypotheses regarding colonization patterns and evolutionary relationships among western populations of the Horned Lark (Eremophila alpestris), including the endemic Channel Island subspecies E. a. insularis. We also examined how many times Horned Larks have colonized the Channel Islands, whether the species exhibits asymmetrical patterns of gene flow between mainland and island populations, and whether E. a. strigata of the Pacific Northwest is closely related to the phenotypically similar, but geographically separated, island subspecies. We found that E. a. insularis is polyphyletic, which suggests either multiple colonization events from the mainland or incomplete lineage sorting of a large ancestral population. We also inferred higher rates of migration from the Channel Islands to the mainland, with E. a. strigata being closely related to individuals from the Channel Islands and coastal southern California. Moreover, ecological niche models for E. a. strigata identified suitable abiotic conditions in southern California and the Pacific Northwest during the Last Glacial Maximum, which suggests that E. a. strigata experienced a postglacial range shift in addition to a population bottleneck. Our results provide novel insight regarding the origins of the Channel Island avifauna and the evolutionary history of the Horned Lark in the western United States. Moreover, our findings suggest that Channel Island birds may be weakly differentiated from mainland populations despite phenotypic differences between recognized subspecies.

An inverse latitudinal gradient in speciation rate for marine fishes

Far more species of organisms are found in the tropics than in temperate and polar regions, but the evolutionary and ecological causes of this pattern remain controversial1,2. Tropical marine fish communities are much more diverse than cold-water fish communities found at higher latitudes3,4, and several explanations for this latitudinal diversity gradient propose that warm reef environments serve as evolutionary ‘hotspots’ for species formation5–8. Here we test the relationship between latitude, species richness and speciation rate across marine fishes. We assembled a time-calibrated phylogeny of all ray-finned fishes (31,526 tips, of which 11,638 had genetic data) and used this framework to describe the spatial dynamics of speciation in the marine realm. We show that the fastest rates of speciation occur in species-poor regions outside the tropics, and that high-latitude fish lineages form new species at much faster rates than their tropical counterparts. High rates of speciation occur in geographical regions that are characterized by low surface temperatures and high endemism. Our results reject a broad class of mechanisms under which the tropics serve as an evolutionary cradle for marine fish diversity and raise new questions about why the coldest oceans on Earth are present-day hotspots of species formation.Contrary to previous hypotheses, high-latitude fish lineages form new species at much faster rates than their tropical counterparts especially in geographical regions that are characterized by low surface temperatures and high endemism.

Do Macrophylogenies Yield Stable Macroevolutionary Inferences? An Example from Squamate Reptiles

&NA; Advances in the generation, retrieval, and analysis of phylogenetic data have enabled researchers to create phylogenies that contain many thousands of taxa. These “macrophylogenies”—large trees that typically derive from megaphylogeny, supermatrix, or supertree approaches—provide researchers with an unprecedented ability to conduct evolutionary analyses across broad phylogenetic scales. Many studies have now used these phylogenies to explore the dynamics of speciation, extinction, and phenotypic evolution across large swaths of the tree of life. These trees are characterized by substantial phylogenetic uncertainty on multiple levels, and the stability of macroevolutionary inferences from these data sets has not been rigorously explored. As a case study, we tested whether five recently published phylogenies for squamate reptiles—each consisting of more than 4000 species—yield congruent inferences about the processes that underlie variation in species richness across replicate evolutionary radiations of Australian snakes and lizards. We find discordance across the five focal phylogenies with respect to clade age and several diversification rate metrics, and in the effects of clade age on species richness. We also find that crown clade ages reported in the literature on these Australian groups are in conflict with all of the large phylogenies examined. Macrophylogenies offer an unprecedented opportunity to address evolutionary and ecological questions at broad phylogenetic scales, but accurately representing the uncertainty that is inherent to such analyses remains a critical challenge to our field. [Australia; macroevolution; macrophylogeny; squamates; time calibration.]

Genetic diversity is largely unpredictable but scales with museum occurrences in a species-rich clade of Australian lizards

Genetic diversity is a fundamental characteristic of species and is affected by many factors, including mutation rate, population size, life history and demography. To better understand the processes that influence levels of genetic diversity across taxa, we collected genome-wide restriction-associated DNA data from more than 500 individuals spanning 76 nominal species of Australian scincid lizards in the genus Ctenotus. To avoid potential biases associated with variation in taxonomic practice across the group, we used coalescent-based species delimitation to delineate 83 species-level lineages within the genus for downstream analyses. We then used these genetic data to infer levels of within-population genetic diversity. Using a phylogenetically informed approach, we tested whether variation in genetic diversity could be explained by population size, environmental heterogeneity or historical demography. We find that the strongest predictor of genetic diversity is a novel proxy for census population size: the number of vouchered occurrences in museum databases. However, museum occurrences only explain a limited proportion of the variance in genetic diversity, suggesting that genetic diversity might be difficult to predict at shallower phylogenetic scales.