Locally adaptive Bayesian birth-death model successfully detects slow and rapid rate shifts

Birth-death processes have given biologists a model-based framework to answer questions about changes in the birth and death rates of lineages in a phylogenetic tree. Therefore birth-death models are central to macroevolutionary as well as phylodynamic analyses. Early approaches to studying temporal variation in birth and death rates using birth-death models faced difficulties due to the restrictive choices of birth and death rate curves through time. Sufficiently flexible time-varying birth-death models are still lacking. We use a piecewise-constant birth-death model, combined with both Gaussian Markov random field (GMRF) and horseshoe Markov random field (HSMRF) prior distributions, to approximate arbitrary changes in birth rate through time. We implement these models in the widely used statistical phylogenetic software platform RevBayes, allowing us to jointly estimate birth-death process parameters, phylogeny, and nuisance parameters in a Bayesian framework. We test both GMRF-based and HSMRF-based models on a variety of simulated diversification scenarios, and then apply them to both a macroevolutionary and an epidemiological dataset. We find that both models are capable of inferring variable birth rates and correctly rejecting variable models in favor of effectively constant models. In general the HSMRF-based model has higher precision than its GMRF counterpart, with little to no loss of accuracy. Applied to a macroevolutionary dataset of the Australian gecko family Pygopodidae (where birth rates are interpretable as speciation rates), the GMRF-based model detects a slow decrease whereas the HSMRF-based model detects a rapid speciation-rate decrease in the last 12 million years. Applied to an infectious disease phylodynamic dataset of sequences from HIV subtype A in Russia and Ukraine (where birth rates are interpretable as the rate of accumulation of new infections), our models detect a strongly elevated rate of infection in the 1990s. Author summary Both the growth of groups of species and the spread of infectious diseases through populations can be modeled as birth-death processes. Birth events correspond either to speciation or infection, and death events to extinction or becoming noninfectious. The rates of birth and death may vary over time, and by examining this variation researchers can pinpoint important events in the history of life on Earth or in the course of an outbreak. Time-calibrated phylogenies track the relationships between a set of species (or infections) and the times of all speciation (or infection) events, and can thus be used to infer birth and death rates. We develop two phylogenetic birth-death models with the goal of discerning signal of rate variation from noise due to the stochastic nature of birth-death models. Using a variety of simulated datasets, we show that one of these models can accurately infer slow and rapid rate shifts without sacrificing precision. Using real data, we demonstrate that our new methodology can be used for simultaneous inference of phylogeny and rates through time

Bergmann\u27s Clines in Ectotherms: Illustrating a Life-History Perspective with Sceloporine Lizards

The generality and causes of Bergmann\u27s rule have been debated vigorously in the last few years, but Bergmann\u27s clines are rarely explained in the context of life-history theory. We used both traditional and phylogenetic comparative analyses to explore the causes of latitudinal and thermal clines in the body size of the eastern fence lizard (Sceloporus undulatus). The proximate mechanism for larger body sizes in colder environments is delayed maturation, which results in a greater fecundity but a lower survival to maturity. Life-history theory predicts that a higher survivorship of juveniles in colder environments can favor the evolution of a Bergmann\u27s cline. Consistent with this theory, lizards in colder environments survive better as juveniles and delay maturation until reaching a larger body size than that of lizards in warmer environments. We expect similar relationships among temperature, survivorship, and age/size at maturity exist in other ectotherms that exhibit Bergmann\u27s clines. However, life-history traits of S. undulatus were more strongly related to latitude than they were to temperature, indicating that both abiotic and biotic factors should be considered as causes of Bergmann\u27s clines. Nonetheless, analyses of the costs and benefits of particular body sizes in different thermal environments will enhance our understanding of geographic variation

Phylotranscriptomic insights into the diversification of endothermic Thunnus tunas

Birds, mammals, and certain fishes, including tunas, opahs and lamnid sharks, are endothermic, conserving internally generated, metabolic heat to maintain body or tissue temperatures above that of the environment. Bluefin tunas are commercially important fishes worldwide, and some populations are threatened. They are renowned for their endothermy, maintaining elevated temperatures of the oxidative locomotor muscle, viscera, brain and eyes, and occupying cold, productive high-latitude waters. Less cold-tolerant tunas, such as yellowfin tuna, by contrast, remain in warm-temperate to tropical waters year-round, reproducing more rapidly than most temperate bluefin tuna populations, providing resiliency in the face of large-scale industrial fisheries. Despite the importance of these traits to not only fisheries but also habitat utilization and responses to climate change, little is known of the genetic processes underlying the diversification of tunas. In collecting and analyzing sequence data across 29,556 genes, we found that parallel selection on standing genetic variation is associated with the evolution of endothermy in bluefin tunas. This includes two shared substitutions in genes encoding glycerol-3 phosphate dehydrogenase, an enzyme that contributes to thermogenesis in bumblebees and mammals, as well as four genes involved in the Krebs cycle, oxidative phosphorylation, β-oxidation, and superoxide removal. Using phylogenetic techniques, we further illustrate that the eight Thunnus species are genetically distinct, but found evidence of mitochondrial genome introgression across two species. Phylogeny-based metrics highlight conservation needs for some of these species

Data from: A genomic evaluation of taxonomic trends through time in coast horned lizards (genus Phrynosoma)

Determining the boundaries between species and deciding when to describe new species are challenging practices that are particularly difficult in groups with high levels of geographic variation. The coast horned lizards (Phrynosoma blainvillii, P. cerroense, and P. coronatum) have an extensive geographic distribution spanning many distinctive ecological regions ranging from northern California to the Cape Region of Baja California, Mexico, and populations differ substantially with respect to external morphology across much of this range. The number of taxa recognized in the group has been re-evaluated by herpetologists over 20 times during the last 180 years, and typically without the aid of explicit species delimitation methods, resulting in a turbulent taxonomy containing anywhere from one to seven taxa. In this study, we evaluate taxonomic trends through time by ranking 15 of these species delimitation models (SDMs) using coalescent analyses of nuclear loci and SNPs in a Bayesian model comparison framework. SDMs containing more species were generally favored by Bayesian model selection; however, several three-species models outperformed some four and five species SDMs, and the top-ranked model, which contained five species, outperformed all SDMs containing six species. Model performance peaked in the 1950s based on marginal likelihoods estimated from nuclear loci and SNPs. Not surprisingly, SDMs based on genetic data outperformed morphological taxonomies when using genetic data alone to evaluate models. The de novo estimation of population structure favors a three-population model that matches the currently recognized integrative taxonomy containing three species. We discuss why Bayesian model selection might favor models containing more species, and why recognizing more than three species might be warranted

Phenotypic evolution in high-elevation populations of western fence lizards (Sceloporus occidentalis) in the Sierra Nevada Mountains

Adaptive divergence in response to variable habitats, climates, and altitude is often accentuated along elevation gradients. We investigate phenotypic evolution in body size and coloration in the western fence lizard (Sceloporus occidentalis Baird and Girard, 1852) across elevation gradients in Yosemite National Park, California, situated in the Sierra Nevada mountains of Western North America. High-elevation populations occurring above 2100 m a.s.l. are recognized as a separate subspecies (Sceloporus occidentalis taylori Camp, 1916), with a distinctive phenotype characterized by a large body size and extensive blue ventral pigmentation. We sampled S. occidentalis from across elevation gradients in Yosemite National Park, California, and collected phenotypic data (body size and ventral coloration measurements; 410 specimens) and mitochondrial DNA sequence data (complete NADH1 gene; 969 bp, 181 specimens) to infer phylogenetic relationships, and examine the genetic and phenotypic diversity among populations. Populations of S. occidentalis in Yosemite National Park follow Bergmann's rule and exhibit larger body sizes in colder, high-elevation environments. The high-elevation subspecies S. o. taylori is not monophyletic, and the mitochondrial DNA genealogy supports a model of convergent phenotypic evolution among high-elevation populations belonging to different river drainages. The hypothesis that separate populations of S. occidentalis expanded up river drainages after the recession of glaciers is supported by population demographic analyses, and suggest that Bergmann's clines can evolve rapidly along elevation gradients. The distinctive high-elevation phenotype that is attributable to S. o. taylori has evolved independently several times, and includes adaptive phenotypic changes associated with increases in body size and ventral coloration

Phylogenetic Comparative Analysis of Life-History Variation among Populations of the Lizard Sceloporus Undulatus: An Example and Prognosis

Over the past 15 years, phylogenetic comparative methods (PCMs) have become standard in the study of life-history evolution. To date, most studies have focused on variation among species or higher taxonomic levels, generally revealing the presence of significant phylogenetic effects as well as residual variation potentially attributable to adaptive evolution

Coalescent-based species delimitation in an integrative taxonomy

The statistical rigor of species delimitation has increased dramatically over the past decade. Coalescent theory provides powerful models for population genetic inference, and is now increasingly important in phylogenetics and speciation research. By applying probabilistic models, coalescent-based species delimitation provides clear and objective testing of alternative hypotheses of evolutionary independence. As acquisition of multilocus data becomes increasingly automated, coalescent-based species delimitation will improve the discovery, resolution, consistency, and stability of the taxonomy of species. Along with other tools and data types, coalescent-based species delimitation will play an important role in an integrative taxonomy that emphasizes the identification of species limits and the processes that have promoted lineage diversification

Genetically diverse yet morphologically conserved: Hidden diversity revealed among Bornean geckos (Gekkonidae: Cyrtodactylus)

The appreciation of cryptic biological diversity, and the pace at which it is recognized, has greatly increased with the use of molecular systematic techniques. The gekkonid genus Cyrtodactylus Gray, 1827 is one example of a group that has undergone a particularly rapid increase in recognized diversity due to molecular systematic studies. Many of these new species result from recognizing closely related but diagnosable lineages into sister taxa. Our study implements a multi-faceted approach to delimit cryptic Cyrtodactylus lineages on the Southeast Asian island of Borneo using morphological, ecological, and multilocus genetic data. We use multiple species delimitation models to assess species boundaries and identify clades that warrant further investigation. Unlike most morphologically cryptic species that have recently diverged, we find evidence of cryptic lineages being polyphyletic. Using multivariate statistical analyses, we show minimal phenotypic distinction between putative cryptic species within the C. pubisulcus complex. Despite not finding morphologically diagnostic characters, we demonstrate strong evidence for the specific recognition of C. hantu sp. nov. and C. miriensis sp. nov., which are currently considered conspecific with C. pubisulcus, from Sarawak, Malaysia. Our new concept for C. pubisulcus restricts the geographic range of the species to specific regions in western Sarawak, Malaysia, thus underscoring the need to conserve the limited remaining habitats of these species, as well as the considerable undescribed diversity across Borneo.Lee Kong Chian Natural History Museum Collection Study Grant; The Society of Integrative and Comparative Biology; Museum of Comparative Zoology, Harvard University; Gerald M. Lemole Endowed Chair Fund; Government of Malaysia, Grant/Award Number: (NRGS/1087/2013(01