Generalizing Bayesian phylogenetics to infer shared evolutionary events.

Many processes of biological diversification can simultaneously affect multiple evolutionary lineages. Examples include multiple members of a gene family diverging when a region of a chromosome is duplicated, multiple viral strains diverging at a "super-spreading" event, and a geological event fragmenting whole communities of species. It is difficult to test for patterns of shared divergences predicted by such processes because all phylogenetic methods assume that lineages diverge independently. We introduce a Bayesian phylogenetic approach to relax the assumption of independent, bifurcating divergences by expanding the space of topologies to include trees with shared and multifurcating divergences. This allows us to jointly infer phylogenetic relationships, divergence times, and patterns of divergences predicted by processes of diversification that affect multiple evolutionary lineages simultaneously or lead to more than two descendant lineages. Using simulations, we find that the method accurately infers shared and multifurcating divergence events when they occur and performs as well as current phylogenetic methods when divergences are independent and bifurcating. We apply our approach to genomic data from two genera of geckos from across the Philippines to test if past changes to the islands' landscape caused bursts of speciation. Unlike previous analyses restricted to only pairs of gecko populations, we find evidence for patterns of shared divergences. By generalizing the space of phylogenetic trees in a way that is independent from the likelihood model, our approach opens many avenues for future research into processes of diversification across the life sciences.

Reduced Mitochondrial Respiration in Hybrid Asexual Lizards.

AbstractThe scarcity of asexual reproduction in vertebrates alludes to an inherent cost. Several groups of asexual vertebrates exhibit lower endurance capacity (a trait predominantly sourced by mitochondrial respiration) compared with congeneric sexual species. Here we measure endurance capacity in five species of Aspidoscelis lizards and examine mitochondrial respiration between sexual and asexual species using mitochondrial respirometry. Our results show reduced endurance capacity, reduced mitochondrial respiration, and reduced phenotypic variability in asexual species compared with parental sexual species, along with a positive relationship between endurance capacity and mitochondrial respiration. Results of lower endurance capacity and lower mitochondrial respiration in asexual Aspidoscelis are consistent with hypotheses involving mitonuclear incompatibility.

Differences in Quaternary co-divergence reveals community-wide diversification in the mountains of southwest China varied among species.

The mountains of southwest China (MSWC) is a biodiversity hotspot with highly complex and unusual terrain. However, with the majority of studies focusing on the biogeographic consequences of massive mountain building, the Quaternary legacy of biodiversity for the MSWC has long been overlooked. Here, we took a statistical comparative phylogeography approach to examine factors that shaped community-wide diversification. With data from 30 vertebrate species, the results reveal spatially concordant genetic structure, and temporally clustered co-divergence events associated with river barriers during severe glacial cycles. This indicates the importance of riverine barriers in the phylogeographic history of the MSWC vertebrate community. We conclude that the repeated glacial cycles are associated with co-divergences that are themselves structured by the heterogeneity of the montane landscape of the MSWC. This orderly process of diversification has profound implications for conservation by highlighting the relative independence of different geographical areas in which some, but not all species in communities have responded similarly to climate change and calls for further comparative phylogeographic investigations to reveal the connection between biological traits and divergence pulses in this biodiversity hotspot.

A new insular species of the Cyrtodactylus intermedius (Squamata: Gekkonidae) group from Cambodia with a discussion of habitat preference and ecomorphology.

An integrative taxonomic analysis based on mitochondrial and morphological data recovered the population of Cyrtodactylus on Koh Rong Island, Preah Sihanouk Province, Cambodiaa as an endemic insular species belonging to the Cyrtodactylus intermedius group. This brings the number of species in the C. intermedius group to at least 10 and the number of species in Cambodia to at least seven. Species of this relatively small group vary widely in habitat preference, occurring in general, terrestrial, karstic, or granitic habitats. Ancestral character state mapping recovered a general habitat preference as the ancestral condition from which all others independently evolved even though this did not covary with morphology. The description of another new species of reptile from Cambodia continues to underscore the potentially significant amount of unrealized biodiversity in Indochina and Southeast Asia and the continued need for field surveys in unexplored or poorly explored areas.

A new species of Cyrtodactylus Gray (Squamata; Gekkonidae) from the Thai Highlands with a discussion on the evolution of habitat preference.

A new gekkonid lizard, Cyrtodactylus maelanoi sp. nov., from Mae Hong Son Province of the Thai Highlands is described using an integrative taxonomic analysis based on morphology, color pattern, and the mitochondrial gene NADH dehydrogenase subunit 2 (ND2) and its flanking tRNAs. Phylogenetic analyses place the new species within clade 1 of the C. sinyineensis group and as the sister species to C. inthanon with an uncorrected pairwise sequence divergence of 3.9%. Collection data gathered in the field indicate that C. maelanoi sp. nov. is a habitat generalist. Reconstruction of the ancestral habitat preference for the C. sinyineensis group by way of stochasitc character mapping (SCM) indicates that karstic environments were the ancestral condition out of which the general habitat preference of the ancestor of C. maelanoi sp. nov. and C. inthanon and that of C. amphipetreaus and C. doisuthep evolved three times independently. Additionally, SCM demonstrated that the evolution of a granitic habitat preference from a karst-adapted ancestor happened in C. aequalis. The discovery of a new upland species in the Thai Highlands brings into focus the understudied nature of the mountain systems of western Thailand and the need for their continued exploration and conservation.

Impacts of the Toba eruption and montane forest expansion on diversification in Sumatran parachuting frogs (Rhacophorus).

Catastrophic events, such as volcanic eruptions, can have profound impacts on the demographic histories of resident taxa. Due to its presumed effect on biodiversity, the Pleistocene eruption of super-volcano Toba has received abundant attention. We test the effects of the Toba eruption on the diversification, genetic diversity, and demography of three co-distributed species of parachuting frogs (Genus Rhacophorus) on Sumatra. We generate target-capture data (~950 loci and ~440,000 bp) for three species of parachuting frogs and use these data paired with previously generated double digest restriction-site associated DNA (ddRADseq) data to estimate population structure and genetic diversity, to test for population size changes using demographic modelling, and to estimate the temporal clustering of size change events using a full-likelihood Bayesian method. We find that populations around Toba exhibit reduced genetic diversity compared with southern populations, and that northern populations exhibit a shift in effective population size around the time of the eruption (~80 kya). However, we infer a stronger signal of expansion in southern populations around ~400 kya, and at least two of the northern populations may have also expanded at this time. Taken together, these findings suggest that the Toba eruption precipitated population declines in northern populations, but that the demographic history of these three species was also strongly impacted by mid-Pleistocene forest expansion during glacial periods. We propose local rather than regional effects of the Toba eruption, and emphasize the dynamic nature of diversification on the Sunda Shelf.

Insights from a general, full-likelihood Bayesian approach to inferring shared evolutionary events from genomic data: Inferring shared demographic events is challenging.

Factors that influence the distribution, abundance, and diversification of species can simultaneously affect multiple evolutionary lineages within or across communities. These include changes to the environment or inter-specific ecological interactions that cause ranges of multiple species to contract, expand, or fragment. Such processes predict temporally clustered evolutionary events across species, such as synchronous population divergences and/or changes in population size. There have been a number of methods developed to infer shared divergences or changes in population size, but not both, and the latter has been limited to approximate methods. We introduce a full-likelihood Bayesian method that uses genomic data to estimate temporal clustering of an arbitrary mix of population divergences and population-size changes across taxa. Using simulated data, we find that estimating the timing and sharing of demographic changes tends to be inaccurate and sensitive to prior assumptions, which is in contrast to accurate, precise, and robust estimates of shared divergence times. We also show that previous estimates of co-expansion among five Alaskan populations of three-spine sticklebacks (Gasterosteus aculeatus) were likely driven by prior assumptions and ignoring invariant characters. We conclude by discussing potential avenues to improve the estimation of synchronous demographic changes across populations.

Rivers of Indochina as potential drivers of lineage diversification in the spotted flying lizard (Draco maculatus) species complex.

Southeast Asia hosts a rich concentration of biodiversity within multiple biodiversity hotspots. Indochina, a region with remarkably high levels of in situ diversification, possesses five major rivers (Ayeyarwady, Chiang Mai, Mekong, Red, and Salween), several of which coincide with phylogenetic breaks of terrestrial taxa. Draco maculatus possesses a range that stretches across Indochina, which widespread geographic distribution along with potential discrete variation within subspecies alludes to the possibility of this taxon constituting multiple divergent lineages. Using sequence data from three mitochondrial (12S, 16S, and ND2) and three nuclear (BDNF, CMOS, and PNN) genes, we provide the first estimated phylogeny of this hypothesized species complex and examine its phylogeographic architecture with maximum likelihood and Bayes factor delimitation (BFD) approaches. Our results support multiple divergent lineages with phylogenetic breaks coincident with rivers, indicating that river barriers may be contributing to the elevated levels of in situ diversification of Indochina.

Two new species of Cyrtodactylus Gray, 1827 (Squamata: Gekkonidae) from a karstic archipelago in the Salween Basin of southern Myanmar (Burma).

An integrative taxonomic analysis of the 10 species of the Cyrtodactylus sinyineensis group based on squamation, color pattern, and the mitochondrial gene NADH dehydrogenase subunit 2 (ND2) and its flanking tRNA regions, recovered the newly discovered populations from Datt Kyaik and Taung Wine Hills in Kayin State as the new species Cyrtodactylus dattkyaikensis sp. nov. and C. taungwineensis sp. nov. The Maximum Likelihood and Bayesian phylogenetic estimates supported C. dattkyaikensis sp. nov. as the sister species of C. bayinnyiensis and C. taungwineensis sp. nov. as the sister species of C. sinyineensis. Each new species is differentially diagnosable from all other C. sinyineensis group species based on their morphological placement in multivariate space and several statistically significant mean differences is meristic squamation and color pattern data. The C. sinyineensis group ranges across an archipelago of karstic habitat-islands in the Salween Basin of southern Myanmar. The discovery of these new species continues to underscore the unprecedented high degree of diversity and site-specific endemism in this relatively small region and the urgent need for the conservation of its karstic terranes.

Four new Burmese species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from distantly related parapatric clades from the Shan Plateau and Salween Basin.

An integrative taxonomic analysis based on morphology, color pattern, and the mitochondrial gene ND2 recovered four new species of Hemiphyllodactylus Bleeker that are endemic to the Shan Plateau or Salween Basin in eastern Myanmar. Hemiphyllodactylus ngwelwini sp. nov. from the Shan Plateau is part of the earlier described "eastern Myanmar clade" renamed herein as the north lineage and H. kyaiktiyoensis sp. nov. and H. pinlaungensis sp. nov. of the Shan Plateau and H. zwegabinensis sp. nov. of the Salween Basin compose an entirely new Burmese clade herein referred to as the south lineage. Although the north and south lineages come within 46 km of one another on the Shan Plateau, they are not sister lineages but sequentially separated by two lineages from Yunnan, China and another from northwestern Thailand. Hemiphyllodactylus zwegabinensis sp. nov. is the first species of this genus to be recorded from the Salween Basin and is known only from a wind-blown cloud forest on the top of the insular, karstic mountain Zwegabin in Kayin State. All other Burmese species except for H. typus, are endemic to the various localities throughout the Shan Plateau. These four new species bring the total number of Hemiphyllodactylus in Myanmar to at least 10 which is certainly an extreme underestimate of the diversity of this genus given that we discover new species at every upland locality we survey.

A new potentially endangered limestone-associated Bent-toed Gecko of the Cyrtodactylus pulchellus (Squamata: Gekkonidae) complex from northern Peninsular Malaysia.

A survey of a limestone forest at Gunung Baling, Kedah, West Malaysia lead to the discovery of an undescribed species of Bent-toed Gecko from the Cyrtodactylus pulchellus complex. Cyrtodactylus evanquahi sp. nov. can be distinguished from all other species in the C. pulchellus complex by a suite of morphological and color pattern characteristics: prominent tuberculation, higher number of dark body bands, and a smaller maximum SVL. It is further differentiated from all other species as follows; no tubercles on the ventral surface of the forelimbs, gular region, or in the ventrolateral folds; 31-34 paravetebral dorsal tubercles; 18-23 longitudinal rows of tubercles; 29-33 ventral scales; 22-23 subdigital lamellae on the fourth toe; 32-36 femoroprecloacal pores; a shallow precloacal groove in males; body bands and nuchal loop edged with a thin white line bearing tubercles; no scattered white spots on the dorsum; six or seven dark body bands much thinner than interspaces; 9-11 dark caudal bands on original tail; bands on the original tail separated by immaculate white caudal bands. It is further differentiated by an uncorrected pairwise genetic divergence of 6.50-15.67% from all other congeners in the C. pulchellus complex. It is most closely related to C. pulchellus from Penang Island ∼76 km to the southwest. In addition to the new samples from Gunung Baling, we added four samples of C. bintangrendah from the new locality of Belukar Semang, Perak. The discovery of yet another new species of the C. pulchellus complex from a limestone habitat continues to underscore the high degree of endemism and the importance of these unique habitats for biodiversity, and the continued need for their conservation.

Patterns of gene evolution following duplications and speciations in vertebrates.

BACKGROUND: Eukaryotic genes typically form independent evolutionary lineages through either speciation or gene duplication events. Generally, gene copies resulting from speciation events (orthologs) are expected to maintain similarity over time with regard to sequence, structure and function. After a duplication event, however, resulting gene copies (paralogs) may experience a broader set of possible fates, including partial (subfunctionalization) or complete loss of function, as well as gain of new function (neofunctionalization). This assumption, known as the Ortholog Conjecture, is prevalent throughout molecular biology and notably plays an important role in many functional annotation methods. Unfortunately, studies that explicitly compare evolutionary processes between speciation and duplication events are rare and conflicting. METHODS: To provide an empirical assessment of ortholog/paralog evolution, we estimated ratios of nonsynonymous to synonymous substitutions (ω = dN/dS) for 251,044 lineages in 6,244 gene trees across 77 vertebrate taxa. RESULTS: Overall, we found ω to be more similar between lineages descended from speciation events (p < 0.001) than lineages descended from duplication events, providing strong support for the Ortholog Conjecture. The asymmetry in ω following duplication events appears to be largely driven by an increase along one of the paralogous lineages, while the other remains similar to the parent. This trend is commonly associated with neofunctionalization, suggesting that gene duplication is a significant mechanism for generating novel gene functions.

Comparative phylogeography of West African amphibians and reptiles.

Comparative phylogeographic studies often support shared divergence times for co-distributed species with similar life histories and habitat specializations. During the late Holocene, West Africa experienced aridification and the turnover of rain forest habitats into savannas. These fragmented rain forests harbor impressive numbers of endemic and threatened species. In this setting, populations of co-distributed rain forest species are expected to have diverged simultaneously, whereas divergence events for species adapted to savanna and forest-edge habitats should be absent or idiosyncratic. We conducted a Bayesian analysis of shared evolutionary events to test models of population divergence for 20 species of anurans (frogs) and squamates (lizards and snakes) that are distributed across the Dahomey Gap, a climate change-induced savanna barrier responsible for fragmenting previously contiguous rain forests of Ghana into two regions: the Togo-Volta Hills and the Southwestern Forests. A model of asynchronous diversification is supported for anurans and squamates, suggesting that drivers of diversification are not specifically related to ecological and life history associations with habitat types. Instead, the wide variability of genetic divergence histories exhibited by these species suggests that biodiversity in this region has been shaped by diversification events that extend beyond the Holocene. Comparisons of the genealogical divergence index, a measure of the genetic divergence between populations due to the combined effects of genetic isolation and gene flow, illustrate that these populations represent a broad sampling of the speciation continuum.

A new species of Bent-toed Gecko (Squamata, Gekkonidae, Cyrtodactylus) from the Shan Plateau in eastern Myanmar (Burma).

An integrative taxonomic analysis of the Cyrtodactylus linnwayensis group of the Shan Plateau recovered two new populations from isolated karst habitats near Pinlaung Town, Shan State as a new species, C. pinlaungensis sp. nov. Cyrtodactylus pinlaungensis sp. nov. is most closely related to a clade comprising C. linnwayensis and C. ywanganensis from the western edge of the Shan Plateau approximately 90 km to the northwest. Cyrtodactylus pinlaungensis sp. nov. can be distinguished from all members of the C. linnwayensis group by a number of statistically different morphological characters, discrete color pattern differences, and its heavy tuberculation. It also bears an uncorrected pairwise sequence divergence of 5.0-7.6% from all other species combined based on the mitochondrial gene ND2 and its flanking tRNAs. The discovery of this new species on the Shan Plateau continues to underscore the fact that this region is rapidly emerging as a herpetological diversity hot-spot for Myanmar.

Discovery of the westernmost population of the genus Ansonia Stoliczka (Anura, Bufonidae) with the description of a new species from the Shan Plateau of eastern Myanmar.

A new species of Ansonia is described from the Shan Plateau of Myanmar based on an integrative taxonomic analysis that differentiates it from all other congeners. Molecular phylogenetic analyses based on the mitochondrial genes 12S and 16S rRNA and tRNA-val recover A. kyaiktiyoensis sp. nov. as the sister species to A. inthanon from Thailand but differs from it and other congeners by at least a 5.0% sequence divergence. It is further differentiated by the following combination of morphological characters: (1) maximum SVL 24 mm in males and females; (2) first finger shorter than second; (3) absence of interorbital and tarsal ridges; (4) presence of light-coloured interscapular spot; (5) presence of yellow rictal tubercle; (6) absence of wide, light-coloured patch below eye; (7) presence of large, discrete, bright-yellow submandibular spots along the underside of lower jaw; (8) iris yellow-gold; (9) presence of markings on the snout consisting of streaks below the eye to the lip, and on the canthus rostralis to the nostril; (10) dorsum grey-brown with orange-beige spots, a dark-brown X-shaped marking on the back surrounding the interscapular spot, and dark-coloured markings on rump; (11) fore- and hind limbs with orange-beige cross-bars; and (12) venter light-gray with yellow spotting, especially near flanks and underside of hind limbs. Ansonia kyaiktiyoensis sp. nov. is the westernmost known record for the genus and the only species west of the Salween Basin. Its discovery echoes the increasing number of herpetological discoveries being made in upland regions fringing the Ayeyarwady and Salween Basins.

The Coevolution Effect as a Driver of Spillover.

Global habitat fragmentation is associated with the emergence of infectious diseases of wildlife origins in human populations. Despite this well-accepted narrative, the underlying mechanisms driving this association remain unclear. We introduce a nuanced hypothesis, the 'coevolution effect'. The central concept is that the subdivision of host populations which occurs with habitat fragmentation causes localized coevolution of hosts, obligate parasites, and pathogens which act as 'coevolutionary engines' within each fragment, accelerating pathogen diversification, and increasing pathogen diversity across the landscape. When combined with a mechanism to exit a fragment (e.g., mosquitoes), pathogen variants will spill over into human communities. Through this combined ecoevolutionary approach we may be able to understand the fine-scale mechanisms that drive disease emergence in the Anthropocene.

The comparative biogeography of Philippine geckos challenges predictions from a paradigm of climate-driven vicariant diversification across an island archipelago.

A primary goal of biogeography is to understand how large-scale environmental processes, like climate change, affect diversification. One often-invoked but seldom tested process is the "species-pump" model, in which repeated bouts of cospeciation are driven by oscillating climate-induced habitat connectivity cycles. For example, over the past three million years, the landscape of the Philippine Islands has repeatedly coalesced and fragmented due to sea-level changes associated with glacial cycles. This repeated climate-driven vicariance has been proposed as a model of speciation across evolutionary lineages codistributed throughout the islands. This model predicts speciation times that are temporally clustered around the times when interglacial rises in sea level fragmented the islands. To test this prediction, we collected comparative genomic data from 16 pairs of insular gecko populations. We analyze these data in a full-likelihood, Bayesian model-choice framework to test for shared divergence times among the pairs. Our results provide support against the species-pump model prediction in favor of an alternative interpretation, namely that each pair of gecko populations diverged independently. These results suggest the repeated bouts of climate-driven landscape fragmentation have not been an important mechanism of speciation for gekkonid lizards across the Philippine Archipelago.

Taxonomic and conservation implications of population genetic admixture, mito-nuclear discordance, and male-biased dispersal of a large endangered snake, Drymarchon couperi.

Accurate species delimitation and description are necessary to guide effective conservation of imperiled species, and this synergy is maximized when multiple data sources are used to delimit species. We illustrate this point by examining Drymarchon couperi (Eastern Indigo Snake), a large, federally-protected species in North America that was recently divided into two species based on gene sequence data from three loci and heuristic morphological assessment. Here, we re-evaluate the two-species hypothesis for D. couperi by evaluating both population genetic and gene sequence data. Our analyses of 14 microsatellite markers revealed 6-8 genetic population clusters with significant admixture, particularly across the contact zone between the two hypothesized species. Phylogenetic analyses of gene sequence data with maximum-likelihood methods suggested discordance between mitochondrial and nuclear markers and provided phylogenetic support for one species rather than two. For these reasons, we place Drymarchon kolpobasileus into synonymy with D. couperi. We suggest inconsistent patterns between mitochondrial and nuclear DNA are driven by high dispersal of males relative to females. We advocate for species delimitation exercises that evaluate admixture and gene flow in addition to phylogenetic analyses, particularly when the latter reveal monophyletic lineages. This is particularly important for taxa, such as squamates, that exhibit strong sex-biased dispersal. Problems associated with over-delimitation of species richness can become particularly acute for threatened and endangered species, because of high costs to conservation when taxonomy demands protection of more individual species than are supported by accumulating data.

Full Bayesian Comparative Phylogeography from Genomic Data.

A challenge to understanding biological diversification is accounting for community-scale processes that cause multiple, co-distributed lineages to co-speciate. Such processes predict non-independent, temporally clustered divergences across taxa. Approximate-likelihood Bayesian computation (ABC) approaches to inferring such patterns from comparative genetic data are very sensitive to prior assumptions and often biased toward estimating shared divergences. We introduce a full-likelihood Bayesian approach, ecoevolity, which takes full advantage of information in genomic data. By analytically integrating over gene trees, we are able to directly calculate the likelihood of the population history from genomic data, and efficiently sample the model-averaged posterior via Markov chain Monte Carlo algorithms. Using simulations, we find that the new method is much more accurate and precise at estimating the number and timing of divergence events across pairs of populations than existing approximate-likelihood methods. Our full Bayesian approach also requires several orders of magnitude less computational time than existing ABC approaches. We find that despite assuming unlinked characters (e.g., unlinked single-nucleotide polymorphisms), the new method performs better if this assumption is violated in order to retain the constant characters of whole linked loci. In fact, retaining constant characters allows the new method to robustly estimate the correct number of divergence events with high posterior probability in the face of character-acquisition biases, which commonly plague loci assembled from reduced-representation genomic libraries. We apply our method to genomic data from four pairs of insular populations of Gekko lizards from the Philippines that are not expected to have co-diverged. Despite all four pairs diverging very recently, our method strongly supports that they diverged independently, and these results are robust to very disparate prior assumptions.

The why, when, and how of computing in biology classrooms.

Many biologists are interested in teaching computing skills or using computing in the classroom, despite not being formally trained in these skills themselves. Thus biologists may find themselves researching how to teach these skills, and therefore many individuals are individually attempting to discover resources and methods to do so. Recent years have seen an expansion of new technologies to assist in delivering course content interactively. Educational research provides insights into how learners absorb and process information during interactive learning. In this review, we discuss the value of teaching foundational computing skills to biologists, and strategies and tools to do so. Additionally, we review the literature on teaching practices to support the development of these skills. We pay special attention to meeting the needs of diverse learners, and consider how different ways of delivering course content can be leveraged to provide a more inclusive classroom experience. Our goal is to enable biologists to teach computational skills and use computing in the classroom successfully.