Publications by authors named "Frank T Burbrink"

60 Publications

Quaternary climatic fluctuations influence the demographic history of two species of sky-island endemic amphibians in the Neotropics.

Mol Phylogenet Evol 2021 Feb 19;160:107113. Epub 2021 Feb 19.

Department of Herpetology, American Museum of Natural History, New York, NY, USA.

We evaluated the role of Quaternary climatic fluctuations on the demographic history and population structure of amphibian species endemic to the 'campo rupestre' in the Neotropics, evaluating their distributional shifts, demographic changes, and lineage formation from the end of Pleistocene to present. We chose two anurans endemic to the high-elevation 'campo rupestre' in the Espinhaço Range (ER) in northeastern and southeastern Brazil (Bokermannohyla alvarengai and Bokermannohyla oxente), as models to test the role of Quaternary climatic fluctuations over their distribution range in this region. We collected tissue samples throughout their distribution range and used statistical phylogeography to examine processes of divergence and population demography. We generated spatial-temporal reconstructions using Bayesian inference in a coalescent framework in combination with hind-cast projections of species distribution models (SDMs). We also used the results and literature information to test alternative diversification scenarios via approximate Bayesian computation (ABC). Our results show that Quaternary climatic fluctuations influenced the geographic ranges of both species showing population expansion during the last glacial maximum (LGM) and range contraction during interglacial periods, as inferred from selected ABC models and from past projections of SDMs. We recovered Pleistocene diversification for both species occuring in distinctly unique periods for each taxon. An older and range-restricted lineage was recovered in a geographically isolated geological massif, deserving conservation and further taxonomic study. The diversification and distribution of these amphibian species endemic to the Neotropical 'campo rupestre' were influenced by Quaternary climatic fluctuations. The expansion of cold adapted species restricted to higher elevations during glacial periods and their concomitant retraction during interglacial periods may have been crucial for producing patterns of species richness and endemism along elevation gradients in tropical and subtropical domains. Such processes may influence the evolution of the biota distributed in heterogeneous landscapes with varied topography.
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http://dx.doi.org/10.1016/j.ympev.2021.107113DOI Listing
February 2021

Resolving spatial complexities of hybridization in the context of the gray zone of speciation in North American ratsnakes (Pantherophis obsoletus complex).

Evolution 2021 Feb 5;75(2):260-277. Epub 2021 Jan 5.

Department of Herpetology, The American Museum of Natural History, Central Park West and 79th Street, New York, New York, 10024.

Inferring the history of divergence between species in a framework that permits the presence of gene flow has been crucial for characterizing the "gray zone" of speciation, which is the period of time where lineages have diverged but have not yet achieved strict reproductive isolation. However, estimates of both divergence times and rates of gene flow often ignore spatial information, for example when considering the location and width of hybrid zones with respect to changes in the environment between lineages. Using population genomic data from the North American ratsnake complex (Pantherophis obsoletus), we connected phylogeographic estimates of lineage structure, migration, historical demography, and timing of divergence with hybrid zone dynamics. We examined the spatial context of diversification by linking migration and timing of divergence to the location and widths of hybrid zones. Artificial neural network approaches were applied to understand how landscape features and past climate have influenced population genetic structure among these lineages. We found that rates of migration between lineages were associated with the overall width of hybrid zones. Timing of divergence was not related to migration rate or hybrid zone width across species pairs but may be related to the number of alleles weakly introgressing through hybrid zones. This research underscores how incomplete reproductive isolation can be better understood by considering differential allelic introgression and the effects of historical and contemporary landscape features on the formation of lineages as well as overall genomic estimates of migration rates through time.
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http://dx.doi.org/10.1111/evo.14141DOI Listing
February 2021

Biogeographic barriers, Pleistocene refugia, and climatic gradients in the southeastern Nearctic drive diversification in cornsnakes (Pantherophis guttatus complex).

Mol Ecol 2020 02 9;29(4):797-811. Epub 2020 Feb 9.

Department of Herpetology, The American Museum of Natural History, New York, NY, USA.

The southeastern Nearctic is a biodiversity hotspot that is also rich in cryptic species. Numerous hypotheses (e.g., vicariance, local adaptation, and Pleistocene speciation in glacial refugia) have been tested in an attempt to explain diversification and the observed pattern of extant biodiversity. However, previous phylogeographic studies have both supported and refuted these hypotheses. Therefore, while data support one or more of these diversification hypotheses, it is likely that taxa are forming within this region in species-specific ways. Here, we generate a genomic data set for the cornsnakes (Pantherophis guttatus complex), which are widespread across this region, spanning both biogeographic barriers and climatic gradients. We use phylogeographic model selection combined with hindcast ecological niche models to determine regions of habitat stability through time. This combined approach suggests that numerous drivers of population differentiation explain the current diversity of this group of snakes. The Mississippi River caused initial speciation in this species complex, with more recent divergence events linked to adaptations to ecological heterogeneity and allopatric Pleistocene refugia. Lastly, we discuss the taxonomy of this group and suggest there may be additional cryptic species in need of formal recognition.
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http://dx.doi.org/10.1111/mec.15358DOI Listing
February 2020

Interrogating Genomic-Scale Data for Squamata (Lizards, Snakes, and Amphisbaenians) Shows no Support for Key Traditional Morphological Relationships.

Syst Biol 2020 05;69(3):502-520

Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil CEP 04263-000, Brazil.

Genomics is narrowing uncertainty in the phylogenetic structure for many amniote groups. For one of the most diverse and species-rich groups, the squamate reptiles (lizards, snakes, and amphisbaenians), an inverse correlation between the number of taxa and loci sampled still persists across all publications using DNA sequence data and reaching a consensus on the relationships among them has been highly problematic. In this study, we use high-throughput sequence data from 289 samples covering 75 families of squamates to address phylogenetic affinities, estimate divergence times, and characterize residual topological uncertainty in the presence of genome-scale data. Importantly, we address genomic support for the traditional taxonomic groupings Scleroglossa and Macrostomata using novel machine-learning techniques. We interrogate genes using various metrics inherent to these loci, including parsimony-informative sites (PIS), phylogenetic informativeness, length, gaps, number of substitutions, and site concordance to understand why certain loci fail to find previously well-supported molecular clades and how they fail to support species-tree estimates. We show that both incomplete lineage sorting and poor gene-tree estimation (due to a few undesirable gene properties, such as an insufficient number of PIS), may account for most gene and species-tree discordance. We find overwhelming signal for Toxicofera, and also show that none of the loci included in this study supports Scleroglossa or Macrostomata. We comment on the origins and diversification of Squamata throughout the Mesozoic and underscore remaining uncertainties that persist in both deeper parts of the tree (e.g., relationships between Dibamia, Gekkota, and remaining squamates; among the three toxicoferan clades Iguania, Serpentes, and Anguiformes) and within specific clades (e.g., affinities among gekkotan, pleurodont iguanians, and colubroid families).
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http://dx.doi.org/10.1093/sysbio/syz062DOI Listing
May 2020

Female-biased gape and body-size dimorphism in the New World watersnakes (tribe: Thamnophiini) oppose predictions from Rensch's rule.

Ecol Evol 2019 Sep 9;9(17):9624-9633. Epub 2019 Aug 9.

Department of Herpetology The American Museum of Natural History New York NY USA.

Abstract: Sexual-size dimorphism (SSD) is ubiquitous across animals and often biased in the direction of larger females in snakes and other ectothermic organisms. To understand how SSD evolves across species, Rensch's rule predicts that in taxa where males are larger, SSD increases with body size. In contrast, where females are larger, SSD decreases with body size. While this rule holds for many taxa, it may be ambiguous for others, particularly ectothermic vertebrates. Importantly, this rule suggests that the outcomes of SSD over phylogenetic time scales depend on the direction of dimorphism predicated on the difference in reproductive efforts between males and females. Here, we examine SSD in the context of Rensch's rule in Thamnophiini, the gartersnakes and watersnakes, a prominent group that in many areas comprises the majority of the North American snake biota. Using a dated phylogeny, measurements of gape, body, and tail size, we show that these snakes do not follow Rensch's rule, but rather female-biased SSD increases with body size. We in turn find that this allometry is most pronounced with gape and is correlated with both neonate and litter size, suggesting that acquiring prey of increased size may be directly related to fecundity selection. These changes in SSD are not constrained to any particular clade; we find no evidence of phylogenetic shifts in those traits showing SSD. We suggest several ways forward to better understand the anatomical units of selection for SSD and modularity.

Open Research Badges: This article has been awarded Open Data and Open Materials Badges. All materials and data are publicly accessible via the Open Science Framework at https://doi.org/10.5061/dryad.3pn57h0.
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http://dx.doi.org/10.1002/ece3.5492DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6745821PMC
September 2019

Environmental heterogeneity and not vicariant biogeographic barriers generate community-wide population structure in desert-adapted snakes.

Mol Ecol 2019 10 11;28(20):4535-4548. Epub 2019 Aug 11.

Department of Herpetology, The American Museum of Natural History, New York, NY, USA.

Genetic structure can be influenced by local adaptation to environmental heterogeneity and biogeographic barriers, resulting in discrete population clusters. Geographic distance among populations, however, can result in continuous clines of genetic divergence that appear as structured populations. Here, we evaluate the relevant importance of these three factors over a landscape characterized by environmental heterogeneity and the presence of a hypothesized biogeographic barrier in producing population genetic structure within 13 codistributed snake species using a genomic data set. We demonstrate that geographic distance and environmental heterogeneity across western North America contribute to population genomic divergence. Surprisingly, landscape features long thought to contribute to biogeographic barriers play little role in divergence community wide. Our results suggest that isolation by environment is the most important contributor to genomic divergence. Furthermore, we show that models of population clustering that incorporate spatial information consistently outperform nonspatial models, demonstrating the importance of considering geographic distances in population clustering. We argue that environmental and geographic distances as drivers of community-wide divergence should be explored before assuming the role of biogeographic barriers.
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http://dx.doi.org/10.1111/mec.15182DOI Listing
October 2019

The Origins and Diversification of the Exceptionally Rich Gemsnakes (Colubroidea: Lamprophiidae: Pseudoxyrhophiinae) in Madagascar.

Syst Biol 2019 11;68(6):918-936

Department of Herpetology, The American Museum of Natural History, 79th Street at Central Park West, New York, NY 10024, USA.

Processes leading to spectacular diversity of both form and species on islands have been well-documented under island biogeography theory, where distance from source and island size are key factors determining immigration and extinction resistance. But far less understood are the processes governing in situ diversification on the world's mega islands, where large and isolated land masses produced morphologically distinct radiations from related taxa on continental regions. Madagascar has long been recognized as a natural laboratory due to its isolation, lack of influence from adjacent continents, and diversification of spectacular vertebrate radiations. However, only a handful of studies have examined rate shifts of in situ diversification for this island. Here, we examine rates of diversification in the Malagasy snakes of the family Pseudoxyrhophiinae (gemsnakes) to understand if rates of speciation were initially high, enhanced by diversification into distinct biomes, and associated with key dentition traits. Using a genomic sequence-capture data set for 366 samples, we determine that all previously described and newly discovered species are delimitable and therefore useful candidates for understanding diversification trajectories through time. Our analysis detected no shifts in diversification rate between clades or changes in biome or dentition type. Remarkably, we demonstrate that rates of diversification of the gemsnake radiation, which originated in Madagascar during the early Miocene, remained steady throughout the Neogene. However, we do detect a significant slowdown in diversification during the Pleistocene. We also comment on the apparent paradox where most living species originated in the Pleistocene, despite diversification rates being substantially higher during the earlier 15 myr.
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http://dx.doi.org/10.1093/sysbio/syz026DOI Listing
November 2019

Hibernation in bats (Mammalia: Chiroptera) did not evolve through positive selection of leptin.

Ecol Evol 2018 Dec 28;8(24):12576-12596. Epub 2018 Nov 28.

Division of Vertebrate Zoology, Department of Mammalogy American Museum of Natural History New York New York.

Temperature regulation is an indispensable physiological activity critical for animal survival. However, relatively little is known about the origin of thermoregulatory regimes in a phylogenetic context, or the genetic mechanisms driving the evolution of these regimes. Using bats as a study system, we examined the evolution of three thermoregulatory regimes (hibernation, daily heterothermy, and homeothermy) in relation to the evolution of leptin, a protein implicated in regulation of torpor bouts in mammals, including bats. A threshold model was used to test for a correlation between lineages with positively selected the gene encoding leptin, and the thermoregulatory regimes of those lineages. Although evidence for episodic positive selection of was found, positive selection was not correlated with lineages of heterothermic bats, a finding that contradicts results from previous studies. Evidence from our ancestral state reconstructions suggests that the most recent common ancestor of bats used daily heterothermy and that the presence of hibernation is highly unlikely at this node. Hibernation likely evolved independently at least four times in bats-once in the common ancestor of Vespertilionidae and Molossidae, once in the clade containing Rhinolophidae and Rhinopomatidae, and again independently in the lineages leading to and . Our reconstructions revealed that thermoregulatory regimes never transitioned directly from hibernation to homeothermy, or the reverse, in the evolutionary history of bats. This, in addition to recent evidence that heterothermy is best described along a continuum, suggests that thermoregulatory regimes in mammals are best represented as an ordered continuous trait (homeothermy ← → daily torpor ← → hibernation) rather than as the three discrete regimes that evolve in an unordered fashion. These results have important implications for methodological approaches in future physiological and evolutionary research.
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http://dx.doi.org/10.1002/ece3.4674DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6308895PMC
December 2018

Exploring Chihuahuan Desert diversification in the gray-banded kingsnake, Lampropeltis alterna (Serpentes: Colubridae).

Mol Phylogenet Evol 2019 02 31;131:211-218. Epub 2018 Oct 31.

Department of Herpetology, The American Museum of Natural History, Central Park West and 79(th) Street, New York, NY 10024, USA.

Within many biomes, the cause of phylogeographic structure remains unknown even across regions throughout North America, including within the biodiverse Chihuahuan Desert. For example, little is known about population structure or the timing of diversification of Chihuahuan endemics. This is due largely to the lack of population genomic studies within this region. We generated ultra-conserved element data for the gray-banded kingsnake (Lampropeltis alterna) to investigate lineage divergence and historical demography across the Chihuahuan Desert. We found three unique lineages corresponding to the Trans-Pecos and Mapimian biogeographic regions of the Chihuahuan Desert, and a distinct population in the Sierra Madre Occidental. Using several mutation rates to calibrate the timing of divergence among these lineages, we show that lineage divergence likely occurred during the Pleistocene, which indicates that careful consideration needs to be used when applying mutation rates to ultra-conserved elements. We suggest that biogeographic provinces within the Chihuahuan Desert may have served as allopatric refugia during climatic fluctuations of the Quaternary. This work serves as an important template for further testing biogeographic hypotheses within the region.
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http://dx.doi.org/10.1016/j.ympev.2018.10.031DOI Listing
February 2019

The Biogeography of Deep Time Phylogenetic Reticulation.

Syst Biol 2018 09;67(5):743-744

Department of Herpetology, The American Museum of Natural History, 79th Street at Central Park West, New York, NY 10024, USA.

Most phylogenies are typically represented as purely bifurcating. However, as genomic data have become more common in phylogenetic studies, it is not unusual to find reticulation among terminal lineages or among internal nodes (deep time reticulation; DTR). In these situations, gene flow must have happened in the same or adjacent geographic areas for these DTRs to have occurred and therefore biogeographic reconstruction should provide similar area estimates for parental nodes, provided extinction or dispersal has not eroded these patterns. We examine the phylogeny of the widely distributed New World kingsnakes (Lampropeltis), determine if DTR is present in this group, and estimate the ancestral area for reticulation. Importantly, we develop a new method that uses coalescent simulations in a machine learning framework to show conclusively that this phylogeny is best represented as reticulating at deeper time. Using joint probabilities of ancestral area reconstructions on the bifurcating parental lineages from the reticulating node, we show that this reticulation likely occurred in northwestern Mexico/southwestern US, and subsequently, led to the diversification of the Mexican kingsnakes. This region has been previously identified as an area important for understanding speciation and secondary contact with gene flow in snakes and other squamates. This research shows that phylogenetic reticulation is common, even in well-studied groups, and that the geographic scope of ancient hybridization is recoverable.
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http://dx.doi.org/10.1093/sysbio/syy019DOI Listing
September 2018

Host susceptibility to snake fungal disease is highly dispersed across phylogenetic and functional trait space.

Sci Adv 2017 12 20;3(12):e1701387. Epub 2017 Dec 20.

Department of Biology, University of Maryland, College Park, MD 20742, USA.

Emerging infectious diseases (EIDs) reduce host population sizes, cause extinction, disassemble communities, and have indirect negative effects on human well-being. Fungal EIDs have reduced population abundances in amphibians and bats across many species over large areas. The recent emergence of snake fungal disease (SFD) may have caused declines in some snake populations in the Eastern United States (EUS), which is home to a phylogenetically and ecologically diverse assembly of 98 taxa. SFD has been documented in only 23 naturally occuring species, although this is likely an underestimate of the number of susceptible taxa. Using several novel methods, including artificial neural networks, we combine phylogenetic and trait-based community estimates from all taxa in this region to show that SFD hosts are both phylogenetically and ecologically randomly dispersed. This might indicate that other species of snakes in the EUS could be currently infected or susceptible to SFD. Our models also indicate that information about key traits that enhance susceptiblity is lacking. Surveillance should consider that all snake species and habitats likely harbor this pathogen.
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http://dx.doi.org/10.1126/sciadv.1701387DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5744467PMC
December 2017

Estimating synchronous demographic changes across populations using hABC and its application for a herpetological community from northeastern Brazil.

Mol Ecol 2017 Sep 24;26(18):4756-4771. Epub 2017 Aug 24.

Department of Herpetology, American Museum of Natural History, New York, NY, USA.

Many studies propose that Quaternary climatic cycles contracted and/or expanded the ranges of species and biomes. Strong expansion-contraction dynamics of biomes presume concerted demographic changes of associated fauna. The analysis of temporal concordance of demographic changes can be used to test the influence of Quaternary climate on diversification processes. Hierarchical approximate Bayesian computation (hABC) is a powerful and flexible approach that models genetic data from multiple species, and can be used to estimate the temporal concordance of demographic processes. Using available single-locus data, we can now perform large-scale analyses, both in terms of number of species and geographic scope. Here, we first compared the power of four alternative hABC models for a collection of single-locus data. We found that the model incorporating an a priori hypothesis about the timing of simultaneous demographic change had the best performance. Second, we applied the hABC models to a data set of seven squamate and four amphibian species occurring in the Seasonally Dry Tropical Forests (Caatinga) in northeastern Brazil, which, according to paleoclimatic evidence, experienced an increase in aridity during the Pleistocene. If this increase was important for the diversification of associated xeric-adapted species, simultaneous population expansions should be evident at the community level. We found a strong signal of synchronous population expansion in the Late Pleistocene, supporting the increase of the Caatinga during this time. This expansion likely enhanced the formation of communities adapted to high aridity and seasonality and caused regional extirpation of taxa adapted to wet forest.
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http://dx.doi.org/10.1111/mec.14239DOI Listing
September 2017

Using phylogenomics to understand the link between biogeographic origins and regional diversification in ratsnakes.

Mol Phylogenet Evol 2017 06 24;111:206-218. Epub 2017 Mar 24.

Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192, United States.

Globally distributed groups may show regionally distinct rates of diversification, where speciation is elevated given timing and sources of ecological opportunity. However, for most organisms, nearly complete sampling at genomic-data scales to reduce topological error in all regions is unattainable, thus hampering conclusions related to biogeographic origins and rates of diversification. We explore processes leading to the diversity of global ratsnakes and test several important hypotheses related to areas of origin and enhanced diversification upon colonizing new continents. We estimate species trees inferred from phylogenomic scale data (304 loci) while exploring several strategies that consider topological error from each individual gene tree. With a dated species tree, we examine taxonomy and test previous hypotheses that suggest the ratsnakes originated in the Old World (OW) and dispersed to New World (NW). Furthermore, we determine if dispersal to the NW represented a source of ecological opportunity, which should show elevated rates of species diversification. We show that ratsnakes originated in the OW during the mid-Oligocene and subsequently dispersed to the NW by the mid-Miocene; diversification was also elevated in a subclade of NW taxa. Finally, the optimal biogeographic region-dependent speciation model shows that the uptick in ratsnake diversification was associated with colonization of the NW. We consider several alternative explanations that account for regionally distinct diversification rates.
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http://dx.doi.org/10.1016/j.ympev.2017.03.017DOI Listing
June 2017

Asynchronous demographic responses to Pleistocene climate change in Eastern Nearctic vertebrates.

Ecol Lett 2016 12 25;19(12):1457-1467. Epub 2016 Oct 25.

Department of Biology, The Graduate School and University Center, The City University of New York, 365 Fifth Ave., NY, 10016, USA.

Pleistocene climatic cycles altered species distributions in the Eastern Nearctic of North America, yet the degree of congruent demographic response to the Pleistocene among codistributed taxa remains unknown. We use a hierarchical approximate Bayesian computational approach to test if population sizes across lineages of snakes, lizards, turtles, mammals, birds, salamanders and frogs in this region expanded synchronously to Late Pleistocene climate changes. Expansion occurred in 75% of 74 lineages, and of these, population size trajectories across the community were partially synchronous, with coexpansion found in at least 50% of lineages in each taxonomic group. For those taxa expanding outside of these synchronous pulses, factors related to when they entered the community, ecological thresholds or biotic interactions likely condition their timing of response to Pleistocene climate change. Unified timing of population size change across communities in response to Pleistocene climate cycles is likely rare in North America.
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http://dx.doi.org/10.1111/ele.12695DOI Listing
December 2016

Complex longitudinal diversification across South China and Vietnam in Stejneger's pit viper, Viridovipera stejnegeri (Schmidt, 1925) (Reptilia: Serpentes: Viperidae).

Mol Ecol 2016 Jun 21;25(12):2920-36. Epub 2016 May 21.

Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024-5192, USA.

Viridovipera stejnegeri is one of the most common pit vipers in Asia, with a wide distribution in southern China and Vietnam. We investigated historical demography and explored how the environment and climatic factors have shaped genetic diversity and the evolutionary history of this venomous snake. A total of 171 samples from 47 localities were sequenced and analysed for two mitochondrial gene fragments and three nuclear genes. Gene trees reveal the existence of two well-supported clades (Southwest China and Southeast China) with seven distinct and strongly supported, geographically structured subclades within V. stejnegeri. Estimation of divergence time and ancestral area suggests that V. stejnegeri originated at ~6.0 Ma in the late Miocene on the Yunnan-Guizhou Plateau. The estimated date of origin and divergence of the island populations of Taiwan and Hainan closely matches the geological origin of the both islands. The mtDNA gene tree reveals the presence of west-east diversification in V. stejnegeri populations. Complex orogenesis and heterogeneous habitats, as well as climate-mediated habitat differentiation including glacial cycles, all have influenced population structure and the distribution of this taxon. The validity of V. stejnegeri chenbihuii is questionable, and this subspecies most probably represents an invalid taxon.
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http://dx.doi.org/10.1111/mec.13658DOI Listing
June 2016

Predicting community structure in snakes on Eastern Nearctic islands using ecological neutral theory and phylogenetic methods.

Proc Biol Sci 2015 Nov;282(1819)

Department of Biology, The Graduate Center, City University of New York, New York, NY 10016, USA Department of Biology, College of Staten Island, 2800 Victory Boulevard, 6S-143, Staten Island, New York, NY 10314, USA.

Predicting species presence and richness on islands is important for understanding the origins of communities and how likely it is that species will disperse and resist extinction. The equilibrium theory of island biogeography (ETIB) and, as a simple model of sampling abundances, the unified neutral theory of biodiversity (UNTB), predict that in situations where mainland to island migration is high, species-abundance relationships explain the presence of taxa on islands. Thus, more abundant mainland species should have a higher probability of occurring on adjacent islands. In contrast to UNTB, if certain groups have traits that permit them to disperse to islands better than other taxa, then phylogeny may be more predictive of which taxa will occur on islands. Taking surveys of 54 island snake communities in the Eastern Nearctic along with mainland communities that have abundance data for each species, we use phylogenetic assembly methods and UNTB estimates to predict island communities. Species richness is predicted by island area, whereas turnover from the mainland to island communities is random with respect to phylogeny. Community structure appears to be ecologically neutral and abundance on the mainland is the best predictor of presence on islands. With regard to young and proximate islands, where allopatric or cladogenetic speciation is not a factor, we find that simple neutral models following UNTB and ETIB predict the structure of island communities.
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http://dx.doi.org/10.1098/rspb.2015.1700DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4685806PMC
November 2015

Speciation with gene flow in whiptail lizards from a Neotropical xeric biome.

Mol Ecol 2015 12 25;24(23):5957-75. Epub 2015 Nov 25.

Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal, RN, 59072-970, Brazil.

Two main hypotheses have been proposed to explain the diversification of the Caatinga biota. The riverine barrier hypothesis (RBH) claims that the São Francisco River (SFR) is a major biogeographic barrier to gene flow. The Pleistocene climatic fluctuation hypothesis (PCH) states that gene flow, geographic genetic structure and demographic signatures on endemic Caatinga taxa were influenced by Quaternary climate fluctuation cycles. Herein, we analyse genetic diversity and structure, phylogeographic history, and diversification of a widespread Caatinga lizard (Cnemidophorus ocellifer) based on large geographical sampling for multiple loci to test the predictions derived from the RBH and PCH. We inferred two well-delimited lineages (Northeast and Southwest) that have diverged along the Cerrado-Caatinga border during the Mid-Late Miocene (6-14 Ma) despite the presence of gene flow. We reject both major hypotheses proposed to explain diversification in the Caatinga. Surprisingly, our results revealed a striking complex diversification pattern where the Northeast lineage originated as a founder effect from a few individuals located along the edge of the Southwest lineage that eventually expanded throughout the Caatinga. The Southwest lineage is more diverse, older and associated with the Cerrado-Caatinga boundaries. Finally, we suggest that C. ocellifer from the Caatinga is composed of two distinct species. Our data support speciation in the presence of gene flow and highlight the role of environmental gradients in the diversification process.
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http://dx.doi.org/10.1111/mec.13433DOI Listing
December 2015

Comparing species tree estimation with large anchored phylogenomic and small Sanger-sequenced molecular datasets: an empirical study on Malagasy pseudoxyrhophiine snakes.

BMC Evol Biol 2015 Oct 12;15:221. Epub 2015 Oct 12.

Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024, USA.

Background: Using molecular data generated by high throughput next generation sequencing (NGS) platforms to infer phylogeny is becoming common as costs go down and the ability to capture loci from across the genome goes up. While there is a general consensus that greater numbers of independent loci should result in more robust phylogenetic estimates, few studies have compared phylogenies resulting from smaller datasets for commonly used genetic markers with the large datasets captured using NGS. Here, we determine how a 5-locus Sanger dataset compares with a 377-locus anchored genomics dataset for understanding the evolutionary history of the pseudoxyrhophiine snake radiation centered in Madagascar. The Pseudoxyrhophiinae comprise ~86 % of Madagascar's serpent diversity, yet they are poorly known with respect to ecology, behavior, and systematics. Using the 377-locus NGS dataset and the summary statistics species-tree methods STAR and MP-EST, we estimated a well-supported species tree that provides new insights concerning intergeneric relationships for the pseudoxyrhophiines. We also compared how these and other methods performed with respect to estimating tree topology using datasets with varying numbers of loci.

Methods: Using Sanger sequencing and an anchored phylogenomics approach, we sequenced datasets comprised of 5 and 377 loci, respectively, for 23 pseudoxyrhophiine taxa. For each dataset, we estimated phylogenies using both gene-tree (concatenation) and species-tree (STAR, MP-EST) approaches. We determined the similarity of resulting tree topologies from the different datasets using Robinson-Foulds distances. In addition, we examined how subsets of these data performed compared to the complete Sanger and anchored datasets for phylogenetic accuracy using the same tree inference methodologies, as well as the program *BEAST to determine if a full coalescent model for species tree estimation could generate robust results with fewer loci compared to the summary statistics species tree approaches. We also examined the individual gene trees in comparison to the 377-locus species tree using the program MetaTree.

Results: Using the full anchored dataset under a variety of methods gave us the same, well-supported phylogeny for pseudoxyrhophiines. The African pseudoxyrhophiine Duberria is the sister taxon to the Malagasy pseudoxyrhophiines genera, providing evidence for a monophyletic radiation in Madagascar. In addition, within Madagascar, the two major clades inferred correspond largely to the aglyphous and opisthoglyphous genera, suggesting that feeding specializations associated with tooth venom delivery may have played a major role in the early diversification of this radiation. The comparison of tree topologies from the concatenated and species-tree methods using different datasets indicated the 5-locus dataset cannot beused to infer a correct phylogeny for the pseudoxyrhophiines under any method tested here and that summary statistics methods require 50 or more loci to consistently recover the species-tree inferred using the complete anchored dataset. However, as few as 15 loci may infer the correct topology when using the full coalescent species tree method *BEAST. MetaTree analyses of each gene tree from the Sanger and anchored datasets found that none of the individual gene trees matched the 377-locus species tree, and that no gene trees were identical with respect to topology.

Conclusions: Our results suggest that ≥50 loci may be necessary to confidently infer phylogenies when using summaryspecies-tree methods, but that the coalescent-based method *BEAST consistently recovers the same topology using only 15 loci. These results reinforce that datasets with small numbers of markers may result in misleading topologies, and further, that the method of inference used to generate a phylogeny also has a major influence on the number of loci necessary to infer robust species trees.
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http://dx.doi.org/10.1186/s12862-015-0503-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4603904PMC
October 2015

Independent Demographic Responses to Climate Change among Temperate and Tropical Milksnakes (Colubridae: Genus Lampropeltis).

PLoS One 2015 17;10(6):e0128543. Epub 2015 Jun 17.

Department of Biology, College of Staten Island, 2800 Victory Blvd., Staten Island, NY, 10314, United States of America; The Graduate Center, City University of New York, 365 5th Avenue, New York, NY, 10016, United States of America.

The effects of Late Quaternary climate change have been examined for many temperate New World taxa, but the impact of Pleistocene glacial cycles on Neotropical taxa is less well understood, specifically with respect to changes in population demography. Here, we examine historical demographic trends for six species of milksnake with representatives in both the temperate and tropical Americas to determine if species share responses to climate change as a taxon or by area (i.e., temperate versus tropical environments). Using a multilocus dataset, we test for the demographic signature of population expansion and decline using non-genealogical summary statistics, as well as coalescent-based methods. In addition, we determine whether range sizes are correlated with effective population sizes for milksnakes. Results indicate that there are no identifiable trends with respect to demographic response based on location, and that species responded to changing climates independently, with tropical taxa showing greater instability. There is also no correlation between range size and effective population size, with the largest population size belonging to the species with the smallest geographic distribution. Our study highlights the importance of not generalizing the demographic histories of taxa by region and further illustrates that the New World tropics may not have been a stable refuge during the Pleistocene.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0128543PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470684PMC
March 2016

Contrasting models of parity-mode evolution in squamate reptiles.

J Exp Zool B Mol Dev Evol 2015 Sep 24;324(6):467-72. Epub 2015 Feb 24.

Department of Biology, The Graduate School and University Center, The City University of New York, New York, New York.

Recent analyses using large-scale phylogenies suggest a radically different history for the evolution of live birth and egg laying in squamate reptiles (lizards and snakes) than traditionally understood. What is the ancestral condition for lizards and snakes? How frequently does live bearing evolve in egg-laying lineages? Can the eggshell ever re-evolve in live-bearing lineages? Answering these fundamental questions about the evolution of key physiological processes will require additional data from genomic, developmental, and fossil data.
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http://dx.doi.org/10.1002/jez.b.22593DOI Listing
September 2015

The phylogenetic position and taxonomic status of the Rainbow Tree Snake Gonyophis margaritatus (Peters, 1871) (Squamata: Colubridae) .

Zootaxa 2014 Nov 10;3881(6):532-48. Epub 2014 Nov 10.

Department of Biology, The College of Staten Island, The City University of New York, 2800 Victory Blvd., Staten Island, NY 10314, USA. Department of Biology, The Graduate School and University Center, The City University of New York, 365 Fifth Ave., NY, NY 10016, USA; Email: unknown.

Molecular phylogenies have provided strong evidence for clarifying the taxonomy of groups with ambiguous morphological traits, thus avoiding potentially misleading conclusions based on evolutionary convergence of these traits. For snakes, established molecular databases along with new sequences from rare species allows us to estimate phylogenies, to clarify the phylogenetic relationships and test the monophyly of most taxonomic groups. Using one mitochondrial gene and five nuclear loci, we evaluate the taxonomic status of a rare Southeast Asian serpent, the Rainbow Tree Snake Gonyophis margaritatus (Squamata: Colubridae) by inferring a molecular phylogeny of 101 snake species. Both maximum likelihood and time- calibrated Bayesian inference phylogenies demonstrate that G. margaritatus is sister to Rhadinophis prasinus, previously considered to be part of a radiation of Old World ratsnakes. This group is in turn sister to a group containing Rhadinophis frenatus and Rhynchophis boulengeri with the entire clade originating in the mid-Miocene (~16 Ma) in Southeast Asia. This group is sister to the genus Gonyosoma and together originated in the early Miocene (~20 Ma). We discuss three potential solutions towards eliminating polyphyly of the genus Rhadinophis, but recommend using the genus name Gonyosoma for all species within this clade, which currently contains all of the species within the genera Gonyosoma, Gonyophis, Rhadinophis, and Rhynchophis. 
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http://dx.doi.org/10.11646/zootaxa.3881.6.3DOI Listing
November 2014

Phylogenetic niche conservatism and the evolutionary basis of ecological speciation.

Biol Rev Camb Philos Soc 2015 Nov 26;90(4):1248-62. Epub 2014 Nov 26.

Department of Biology, The Graduate School and University Center, The City University of New York, 365 5th Avenue, New York, NY 10016, U.S.A.

Phylogenetic niche conservatism (PNC) typically refers to the tendency of closely related species to be more similar to each other in terms of niche than they are to more distant relatives. This has been implicated as a potential driving force in speciation and other species-richness patterns, such as latitudinal gradients. However, PNC has not been very well defined in most previous studies. Is it a pattern or a process? What are the underlying endogenous (e.g. genetic) and exogenous (e.g. ecological) factors that cause niches to be conserved? What degree of similarity is necessary to qualify as PNC? Is it possible for the evolutionary processes causing niches to be conserved to also result in niche divergence in different habitats? Here, we revisit these questions, codifying a theoretical and operational definition of PNC as a mechanistic evolutionary process resulting from several factors. We frame this both from a macroevolutionary and population-genetic perspective. We discuss how different axes of physical (e.g. geographic) and environmental (e.g. climatic) heterogeneity interact with the fundamental process of PNC to produce different outcomes of ecological speciation. We also review tests for PNC, and suggest ways that these could be improved or better utilized in future studies. Ultimately, PNC as a process has a well-defined mechanistic basis in organisms, and future studies investigating ecological speciation would be well served to consider this, and frame hypothesis testing in terms of the processes and expected patterns described herein. The process of PNC may lead to patterns where niches are conserved (more similar than expected), constrained (divergent within a limited subset of available niches), or divergent (less similar than expected), based on degree of phylogenetic relatedness between species.
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http://dx.doi.org/10.1111/brv.12154DOI Listing
November 2015

Effectiveness of phylogenomic data and coalescent species-tree methods for resolving difficult nodes in the phylogeny of advanced snakes (Serpentes: Caenophidia).

Mol Phylogenet Evol 2014 Dec 3;81:221-31. Epub 2014 Sep 3.

Dept. of Biology, The Graduate School and University Center, The City University of New York, 365 5th Ave., New York, NY 10016, USA; Dept. of Biology, The College of Staten Island, The City University of New York, 2800 Victory Blvd., Staten Island, NY 10314, USA. Electronic address:

Next-generation genomic sequencing promises to quickly and cheaply resolve remaining contentious nodes in the Tree of Life, and facilitates species-tree estimation while taking into account stochastic genealogical discordance among loci. Recent methods for estimating species trees bypass full likelihood-based estimates of the multi-species coalescent, and approximate the true species-tree using simpler summary metrics. These methods converge on the true species-tree with sufficient genomic sampling, even in the anomaly zone. However, no studies have yet evaluated their efficacy on a large-scale phylogenomic dataset, and compared them to previous concatenation strategies. Here, we generate such a dataset for Caenophidian snakes, a group with >2500 species that contains several rapid radiations that were poorly resolved with fewer loci. We generate sequence data for 333 single-copy nuclear loci with ∼100% coverage (∼0% missing data) for 31 major lineages. We estimate phylogenies using neighbor joining, maximum parsimony, maximum likelihood, and three summary species-tree approaches (NJst, STAR, and MP-EST). All methods yield similar resolution and support for most nodes. However, not all methods support monophyly of Caenophidia, with Acrochordidae placed as the sister taxon to Pythonidae in some analyses. Thus, phylogenomic species-tree estimation may occasionally disagree with well-supported relationships from concatenated analyses of small numbers of nuclear or mitochondrial genes, a consideration for future studies. In contrast for at least two diverse, rapid radiations (Lamprophiidae and Colubridae), phylogenomic data and species-tree inference do little to improve resolution and support. Thus, certain nodes may lack strong signal, and larger datasets and more sophisticated analyses may still fail to resolve them.
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http://dx.doi.org/10.1016/j.ympev.2014.08.023DOI Listing
December 2014

A taxonomic revision of boas (Serpentes: Boidae).

Zootaxa 2014 Aug 1;3846(2):249-60. Epub 2014 Aug 1.

Dept. of Biology, The Graduate School and University Center, The City University of New York, 365 5th Ave., New York, NY 10016. Dept. of Biology, The College of Staten Island, The City University of New York, 2800 Victory Blvd., Staten Island, NY 10314;; Email:

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http://dx.doi.org/10.11646/zootaxa.3846.2.5DOI Listing
August 2014

A hybrid phylogenetic-phylogenomic approach for species tree estimation in African Agama lizards with applications to biogeography, character evolution, and diversification.

Mol Phylogenet Evol 2014 Oct 25;79:215-30. Epub 2014 Jun 25.

Department of Biology, The College of Staten Island, The City University of New York, Staten Island, NY 10314, USA.

Africa is renowned for its biodiversity and endemicity, yet little is known about the factors shaping them across the continent. African Agama lizards (45 species) have a pan-continental distribution, making them an ideal model for investigating biogeography. Many species have evolved conspicuous sexually dimorphic traits, including extravagant breeding coloration in adult males, large adult male body sizes, and variability in social systems among colorful versus drab species. We present a comprehensive time-calibrated species tree for Agama, and their close relatives, using a hybrid phylogenetic-phylogenomic approach that combines traditional Sanger sequence data from five loci for 57 species (146 samples) with anchored phylogenomic data from 215 nuclear genes for 23 species. The Sanger data are analyzed using coalescent-based species tree inference using (*)BEAST, and the resulting posterior distribution of species trees is attenuated using the phylogenomic tree as a backbone constraint. The result is a time-calibrated species tree for Agama that includes 95% of all species, multiple samples for most species, strong support for the major clades, and strong support for most of the initial divergence events. Diversification within Agama began approximately 23 million years ago (Ma), and separate radiations in Southern, East, West, and Northern Africa have been diversifying for >10Myr. A suite of traits (morphological, coloration, and sociality) are tightly correlated and show a strong signal of high morphological disparity within clades, whereby the subsequent evolution of convergent phenotypes has accompanied diversification into new biogeographic areas.
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http://dx.doi.org/10.1016/j.ympev.2014.06.013DOI Listing
October 2014

Coalescent species delimitation in milksnakes (genus Lampropeltis) and impacts on phylogenetic comparative analyses.

Syst Biol 2014 Mar 10;63(2):231-50. Epub 2013 Dec 10.

Department of Biology, College of Staten Island, 2800 Victory Blvd., Staten Island, NY 10314, USA; The Graduate Center, City University of New York, 365 5th Avenue, NY, NY 10016, USA; Department of Biology & Burke Museum of Natural History and Culture, University of Washington, Box 351800, Seattle, WA 98195-1800, USA; Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC 20052, USA; and Department of Herpetology, American Museum of Natural History, Central Park West and 79th St., New York, NY 10024.

Both gene-tree discordance and unrecognized diversity are sources of error for accurate estimation of species trees, and can affect downstream diversification analyses by obscuring the correct number of nodes, their density, and the lengths of the branches subtending them. Although the theoretical impact of gene-tree discordance on evolutionary analyses has been examined previously, the effect of unsampled and cryptic diversity has not. Here, we examine how delimitation of previously unrecognized diversity in the milksnake (Lampropeltis triangulum) and use of a species-tree approach affects both estimation of the Lampropeltis phylogeny and comparative analyses with respect to the timing of diversification. Coalescent species delimitation indicates that L. triangulum is not monophyletic and that there are multiple species of milksnake, which increases the known species diversity in the genus Lampropeltis by 40%. Both genealogical and temporal discordance occurs between gene trees and the species tree, with evidence that mitochondrial DNA (mtDNA) introgression is a main factor. This discordance is further manifested in the preferred models of diversification, where the concatenated gene tree strongly supports an early burst of speciation during the Miocene, in contrast to species-tree estimates where diversification follows a birth-death model and speciation occurs mostly in the Pliocene and Pleistocene. This study highlights the crucial interaction among coalescent-based phylogeography and species delimitation, systematics, and species diversification analyses.
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http://dx.doi.org/10.1093/sysbio/syt099DOI Listing
March 2014

Phylogenetic estimates of speciation and extinction rates for testing ecological and evolutionary hypotheses.

Trends Ecol Evol 2013 Dec 10;28(12):729-36. Epub 2013 Oct 10.

Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC 20052, USA. Electronic address:

Phylogenies are used to estimate rates of speciation and extinction, reconstruct historical diversification scenarios, and link these to ecological and evolutionary factors, such as climate or organismal traits. Recent models can now estimate the effects of binary, multistate, continuous, and biogeographic characters on diversification rates. Others test for diversity dependence (DD) in speciation and extinction, which has become recognized as an important process in numerous clades. A third class incorporates flexible time-dependent functions, enabling reconstruction of major periods of both expanding and contracting diversity. Although there are some potential problems (particularly for estimating extinction), these methods hold promise for answering many classic questions in ecology and evolution, such as the origin of adaptive radiations, and the latitudinal gradient in species richness.
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http://dx.doi.org/10.1016/j.tree.2013.09.007DOI Listing
December 2013

Assessing species boundaries and the phylogenetic position of the rare Szechwan ratsnake, Euprepiophis perlaceus (Serpentes: Colubridae), using coalescent-based methods.

Mol Phylogenet Evol 2014 Jan 21;70:130-6. Epub 2013 Sep 21.

Department of Biology, The College of Staten Island, The City University of New York, 2800 Victory Blvd., Staten Island, NY 10314, United States; Department of Biology, The Graduate School and University Center, The City University of New York, 365 Fifth Ave., NY, NY 10016, United States. Electronic address:

Delimiting species and clarifying phylogenetic relationships are the main goals of systematics. For species with questionable taxonomic status, species delimitation approaches using multi-species coalescent models with multiple loci are recommended if morphological data are unavailable or unhelpful. Moreover, these methods will also reduce subjectivity based on genetic distance or requirement of monophyletic genetic lineages. We determine the validity and phylogenetic position of a rare and long controversial species of Chinese reptile, the Szechwan ratsnake (Euprepiophis perlaceus), using multi-locus data from multiple individuals and coalescent-based approaches. Species were first delimited using Bayesian Phylogenetics & Phylogeography (BP&P), Brownie and Bayes Factor model comparison approaches, while relationships among species were estimated using species tree inference in (*)BEAST. Results indicate that Euprepiophis perlaceus is a distinct species sister to Euprepiophis mandarinus. Despite gene tree discrepancy, the coalescent model-based approaches used here demonstrate the taxonomic validity and the phylogenetic position of Euprepiophis perlaceus. These approaches objectively test the validity of questionable species diagnoses based on morphological characters and determine their phylogenetic position.
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http://dx.doi.org/10.1016/j.ympev.2013.09.003DOI Listing
January 2014

Early origin of viviparity and multiple reversions to oviparity in squamate reptiles.

Ecol Lett 2014 Jan 19;17(1):13-21. Epub 2013 Aug 19.

Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC, 20052, USA.

Viviparity has putatively evolved 115 times in squamates (lizards and snakes), out of only ~ 140 origins in vertebrates, and is apparently related to colder climates and other factors such as body size. Viviparity apparently evolves from oviparity via egg-retention, and such taxa may thus still have the machinery to produce thick-shelled eggs. Parity mode is also associated with variable diversification rates in some groups. We reconstruct ancestral parity modes accounting for state-dependent diversification in a large-scale phylogenetic analysis, and find strong support for an early origin of viviparity at the base of Squamata, and a complex pattern of subsequent transitions. Viviparous lineages have higher rates of speciation and extinction, and greater species turnover through time. Viviparity is associated with lower environmental and body temperatures in lizards and amphisbaenians, but not female mass. These results suggest that parity mode is a labile trait that shifts frequently in response to ecological conditions.
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http://dx.doi.org/10.1111/ele.12168DOI Listing
January 2014

Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes.

Proc Natl Acad Sci U S A 2013 Jul 15;110(31):12738-43. Epub 2013 Jul 15.

Department of Ecology and Evolutionary Biology and Peabody Museum of Natural History, Yale University, New Haven, CT 06520, USA.

Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third of all living vertebrates. Despite their dominant role in aquatic ecosystems, the evolutionary history and tempo of acanthomorph diversification is poorly understood. We investigate the pattern of lineage diversification in acanthomorphs by using a well-resolved time-calibrated phylogeny inferred from a nuclear gene supermatrix that includes 520 acanthomorph species and 37 fossil age constraints. This phylogeny provides resolution for what has been classically referred to as the "bush at the top" of the teleost tree, and indicates acanthomorphs originated in the Early Cretaceous. Paleontological evidence suggests acanthomorphs exhibit a pulse of morphological diversification following the end Cretaceous mass extinction; however, the role of this event on the accumulation of living acanthomorph diversity remains unclear. Lineage diversification rates through time exhibit no shifts associated with the end Cretaceous mass extinction, but there is a global decrease in lineage diversification rates 50 Ma that occurs during a period when morphological disparity among fossil acanthomorphs increases sharply. Analysis of clade-specific shifts in diversification rates reveal that the hyperdiversity of living acanthomorphs is highlighted by several rapidly radiating lineages including tunas, gobies, blennies, snailfishes, and Afro-American cichlids. These lineages with high diversification rates are not associated with a single habitat type, such as coral reefs, indicating there is no single explanation for the success of acanthomorphs, as exceptional bouts of diversification have occurred across a wide array of marine and freshwater habitats.
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http://dx.doi.org/10.1073/pnas.1304661110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3732986PMC
July 2013