Publications by authors named "Eli Greenbaum"

39 Publications

Rivers, not refugia, drove diversification in arboreal, sub-Saharan African snakes.

Ecol Evol 2021 Jun 1;11(11):6133-6152. Epub 2021 May 1.

Department of Ecology and Evolutionary Biology University of Kansas Lawrence KS USA.

The relative roles of rivers versus refugia in shaping the high levels of species diversity in tropical rainforests have been widely debated for decades. Only recently has it become possible to take an integrative approach to test predictions derived from these hypotheses using genomic sequencing and paleo-species distribution modeling. Herein, we tested the predictions of the classic river, refuge, and river-refuge hypotheses on diversification in the arboreal sub-Saharan African snake genus . We used dated phylogeographic inferences, population clustering analyses, demographic model selection, and paleo-distribution modeling to conduct a phylogenomic and historical demographic analysis of this genus. Our results revealed significant population genetic structure within both species, corresponding geographically to river barriers and divergence times from the mid-Miocene to Pliocene. Our demographic analyses supported the interpretation that rivers are indications of strong barriers to gene flow among populations since their divergence. Additionally, we found no support for a major contraction of suitable habitat during the last glacial maximum, allowing us to reject both the refuge and river-refuge hypotheses in favor of the river-barrier hypothesis. Based on conservative interpretations of our species delimitation analyses with the Sanger and ddRAD data sets, two new cryptic species are identified from east-central Africa. This study highlights the complexity of diversification dynamics in the African tropics and the advantages of integrative approaches to studying speciation in tropical regions.
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http://dx.doi.org/10.1002/ece3.7429DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8207163PMC
June 2021

Night stalkers from above: A monograph of Toxicodryas/ tree snakes (Squamata: Colubridae) with descriptions of two new cryptic species from Central Africa.

Zootaxa 2021 Apr 27;4965(1):zootaxa.4965.1.1. Epub 2021 Apr 27.

University of Texas at El Paso, Department of Biological Sciences, 500 W. University Avenue, El Paso, Texas 79912, USA.

The genus Toxicodryas, historically included with the renowned Australasian cat-eyed snakes of the colubrid genus Boiga, currently includes two widespread species (T. blandingii and T. pulverulenta) in western, central, and eastern Africa. We leverage findings from a recent phylogenomic and historical demographic analysis of this genus (based on 2848-4471 Rad-seq loci from across the genome), with robust sampling from throughout the ranges of both species, to define two additional taxonomic units, with species boundaries corresponding to river barriers. Additional morphometric data from scores of examined museum specimens and literature records bolster the recognition of these two new cryptic species. We hypothesize that T. blandingii occurs west of the confluence of the Congo and Ubangi rivers, whereas a cryptic new species that is found east of this biogeographic barrier has significantly higher numbers of ventral scale counts in both sexes, additional significant differences in several scale counts, and lower venom toxicity. Toxicodryas pulverulenta occurs west of the Niger Delta in West Africa, whereas a cryptic new species that is found east of this biogeographic barrier has significantly higher numbers of subcaudal scale counts in both sexes. A review of published information regarding morphological variation, ecology, natural history, habitat, and venom is summarized for these four Toxicodryas species.
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http://dx.doi.org/10.11646/zootaxa.4965.1.1DOI Listing
April 2021

Developmental Systems Drift and the Drivers of Sex Chromosome Evolution.

Mol Biol Evol 2020 03;37(3):799-810

Biology Department, McMaster University, Hamilton, Canada.

Phenotypic invariance-the outcome of purifying selection-is a hallmark of biological importance. However, invariant phenotypes might be controlled by diverged genetic systems in different species. Here, we explore how an important and invariant phenotype-the development of sexually differentiated individuals-is controlled in over two dozen species in the frog family Pipidae. We uncovered evidence in different species for 1) an ancestral W chromosome that is not found in many females and is found in some males, 2) independent losses and 3) autosomal segregation of this W chromosome, 4) changes in male versus female heterogamy, and 5) substantial variation among species in recombination suppression on sex chromosomes. We further provide evidence of, and evolutionary context for, the origins of at least seven distinct systems for regulating sex determination among three closely related genera. These systems are distinct in their genomic locations, evolutionary origins, and/or male versus female heterogamy. Our findings demonstrate that the developmental control of sexual differentiation changed via loss, sidelining, and empowerment of a mechanistically influential gene, and offer insights into novel factors that impinge on the diverse evolutionary fates of sex chromosomes.
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http://dx.doi.org/10.1093/molbev/msz268DOI Listing
March 2020

Xenopus fraseri: Mr. Fraser, where did your frog come from?

PLoS One 2019 11;14(9):e0220892. Epub 2019 Sep 11.

Florida Museum of Natural History, University of Florida, Gainesville, FL, United States of America.

A comprehensive, accurate, and revisable alpha taxonomy is crucial for biodiversity studies, but is challenging when data from reference specimens are difficult to collect or observe. However, recent technological advances can overcome some of these challenges. To illustrate this, we used modern approaches to tackle a centuries-old taxonomic enigma presented by Fraser's Clawed Frog, Xenopus fraseri, including whether X. fraseri is different from other species, and if so, where it is situated geographically and phylogenetically. To facilitate these inferences, we used high-resolution techniques to examine morphological variation, and we generated and analyzed complete mitochondrial genome sequences from all Xenopus species, including >150-year-old type specimens. Our results demonstrate that X. fraseri is indeed distinct from other species, firmly place this species within a phylogenetic context, and identify its minimal geographic distribution in northern Ghana and northern Cameroon. These data also permit novel phylogenetic resolution into this intensively studied and biomedically important group. Xenopus fraseri was formerly thought to be a rainforest endemic placed alongside species in the amieti species group; in fact this species occurs in arid habitat on the borderlands of the Sahel, and is the smallest member of the muelleri species group. This study illustrates that the taxonomic enigma of Fraser's frog was a combined consequence of sparse collection records, interspecies conservation and intraspecific polymorphism in external anatomy, and type specimens with unusual morphology.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0220892PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6738922PMC
March 2020

Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians.

Syst Biol 2019 11;68(6):859-875

Forestry Research Institute of Ghana, P.O. Box 63, Fumesua, Kumasi, Ghana.

Theory predicts that sexually dimorphic traits under strong sexual selection, particularly those involved with intersexual signaling, can accelerate speciation and produce bursts of diversification. Sexual dichromatism (sexual dimorphism in color) is widely used as a proxy for sexual selection and is associated with rapid diversification in several animal groups, yet studies using phylogenetic comparative methods to explicitly test for an association between sexual dichromatism and diversification have produced conflicting results. Sexual dichromatism is rare in frogs, but it is both striking and prevalent in African reed frogs, a major component of the diverse frog radiation termed Afrobatrachia. In contrast to most other vertebrates, reed frogs display female-biased dichromatism in which females undergo color transformation, often resulting in more ornate coloration in females than in males. We produce a robust phylogeny of Afrobatrachia to investigate the evolutionary origins of sexual dichromatism in this radiation and examine whether the presence of dichromatism is associated with increased rates of net diversification. We find that sexual dichromatism evolved once within hyperoliids and was followed by numerous independent reversals to monochromatism. We detect significant diversification rate heterogeneity in Afrobatrachia and find that sexually dichromatic lineages have double the average net diversification rate of monochromatic lineages. By conducting trait simulations on our empirical phylogeny, we demonstrate that our inference of trait-dependent diversification is robust. Although sexual dichromatism in hyperoliid frogs is linked to their rapid diversification and supports macroevolutionary predictions of speciation by sexual selection, the function of dichromatism in reed frogs remains unclear. We propose that reed frogs are a compelling system for studying the roles of natural and sexual selection on the evolution of sexual dichromatism across micro- and macroevolutionary timescales.
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http://dx.doi.org/10.1093/sysbio/syz023DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6934645PMC
November 2019

Evolutionary history of burrowing asps (Lamprophiidae: Atractaspidinae) with emphasis on fang evolution and prey selection.

PLoS One 2019 17;14(4):e0214889. Epub 2019 Apr 17.

Department of Biological Sciences, University of Texas at El Paso, El Paso, Texas, United States of America.

Atractaspidines are poorly studied, fossorial snakes that are found throughout Africa and western Asia, including the Middle East. We employed concatenated gene-tree analyses and divergence dating approaches to investigate evolutionary relationships and biogeographic patterns of atractaspidines with a multi-locus data set consisting of three mitochondrial (16S, cyt b, and ND4) and two nuclear genes (c-mos and RAG1). We sampled 91 individuals from both atractaspidine genera (Atractaspis and Homoroselaps). Additionally, we used ancestral-state reconstructions to investigate fang and diet evolution within Atractaspidinae and its sister lineage (Aparallactinae). Our results indicated that current classification of atractaspidines underestimates diversity within the group. Diversification occurred predominantly between the Miocene and Pliocene. Ancestral-state reconstructions suggest that snake dentition in these taxa might be highly plastic within relatively short periods of time to facilitate adaptations to dynamic foraging and life-history strategies.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0214889PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6469773PMC
January 2020

Diversifying into the branches: Species boundaries in African green and bush snakes, Philothamnus (Serpentes: Colubridae).

Mol Phylogenet Evol 2019 01 23;130:357-365. Epub 2018 Oct 23.

South African National Biodiversity Institute, Kirstenbosch Research Centre, Private Bag X7, Claremont 7735, South Africa; Centre for Ecological Genomics and Wildlife Conservation, University of Johannesburg, Auckland Park 2000, South Africa.

The African green and bush snakes of the genus Philothamnus currently comprises 21 species and three subspecies and occurs throughout sub-Saharan Africa. The genus has been the subject of previous taxonomic revisions based on traditional morphological characters and limited genetic assessment, and may not reflect their evolutionary history. Indeed, previous findings based on phylogenetics show discordant results of interspecific relationships and question the monophyly of the genus, although taxon sampling has been limited to date. We investigated phylogenetic affinities within Philothamnus with more inclusive genetic and geographical sampling, with the aim of better understanding their evolutionary history, so that future taxonomic revision of Philothamnus can be better informed. Species relationships were examined within a phylogenetic context and sampling included 133 ingroup samples from 16 taxa. Phylogenies were constructed in Bayesian and likelihood frameworks using three mitochondrial (16S, cyt b and ND4) and two nuclear (c-mos and RAG1) markers. Competing hypotheses relating to the monophyly of the genus were tested with a Shimodaira-Hasegawa test. To examine species boundaries, Bayesian General Mixed Yule-Coalescent Model and multi-rate Poisson Tree Processes analyses were conducted. In addition, a barcoding approach was used to further clarify species-level relationships by comparing frequency distributions between intra- and interspecific sequence divergence. The genus was recovered as monophyletic; however, species-delimitation results suggest that the current taxonomy does not reflect the evolutionary history of this group. For example, Philothamnus s. semivariegatus is paraphyletic, with at least four distinct clades. Philothamnus carinatus consists of two cryptic (sister) lineages from Central and West Africa that are deeply divergent, suggesting a long history of isolation between those regions. Furthermore, the subspecies P. n. natalensis and P. n. occidentalis show strong support for species-level divergence, which reflects their morphological and ecological differences. Accordingly, we elevate P. occidentalisnov. comb. to a full species. A fully informed taxonomic revision of these taxa will require additional morphological and ecological data for corroboration, but it seems that the morphological characters (e.g. scalation, dentition) used to describe these species to date are labile within and between species. This most likely has clouded our understanding of the species boundaries within the genus. Our phylogeny and species-delimitation analyses should provide a sounder framework for taxonomy, but may also prove useful toward understanding the morphological adaptations of these species to their respective habitats.
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http://dx.doi.org/10.1016/j.ympev.2018.10.023DOI Listing
January 2019

Integration of nuclear and mitochondrial gene sequences and morphology reveals unexpected diversity in the forest cobra (Naja melanoleuca) species complex in Central and West Africa (Serpentes: Elapidae).

Zootaxa 2018 Aug 1;4455(1):68-98. Epub 2018 Aug 1.

Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor LL57 2UW, United Kingdom..

Cobras are among the most widely known venomous snakes, and yet their taxonomy remains incompletely understood, particularly in Africa. Here, we use a combination of mitochondrial and nuclear gene sequences and morphological data to diagnose species limits within the African forest cobra, Naja (Boulengerina) melanoleuca. Mitochondrial DNA sequences reveal deep divergences within this taxon. Congruent patterns of variation in mtDNA, nuclear genes and morphology support the recognition of five separate species, confirming the species status of N. subfulva and N. peroescobari, and revealing two previously unnamed West African species, which are described as new: Naja (Boulengerina) guineensis sp. nov. Broadley, Trape, Chirio, Ineich Wüster, from the Upper Guinea forest of West Africa, and Naja (Boulengerina) savannula sp. nov. Broadley, Trape, Chirio Wüster, a banded form from the savanna-forest mosaic of the Guinea and Sudanian savannas of West Africa. The discovery of cryptic diversity in this iconic group highlights our limited understanding of tropical African biodiversity, hindering our ability to conserve it effectively.
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http://dx.doi.org/10.11646/zootaxa.4455.1.3DOI Listing
August 2018

Collaborative Posters Develop Students' Ability to Communicate about Undervalued Scientific Resources to Nonscientists.

J Microbiol Biol Educ 2018 30;19(1). Epub 2018 Mar 30.

Biodiversity Collections, The University of Texas at El Paso, El Paso, TX 79968.

Scientists are increasingly called upon to communicate with the public, yet most never receive formal training in this area. Public understanding is particularly critical to maintaining support for undervalued resources such as biological collections, research data repositories, and expensive equipment. We describe activities carried out in an inquiry-driven organismal biology laboratory course designed to engage a diverse student body using biological collections. The goals of this cooperative learning experience were to increase students' ability to locate and comprehend primary research articles, and to communicate the importance of an undervalued scientific resource to nonscientists. Our results indicate that collaboratively created, research-focused informational posters are an effective tool for achieving these goals and may be applied in other disciplines or classroom settings.
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http://dx.doi.org/10.1128/jmbe.v19i1.1442DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5969409PMC
March 2018

Phylogeny and biogeography of the African burrowing snake subfamily Aparallactinae (Squamata: Lamprophiidae).

Mol Phylogenet Evol 2018 10 15;127:288-303. Epub 2018 Mar 15.

Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968, USA.

Members of the snake subfamily Aparallactinae occur in various habitats throughout sub-Saharan Africa. The monophyly of aparallactine snakes is well established, but relationships within the subfamily are poorly known. We sampled 158 individuals from six of eight aparallactine genera in sub-Saharan Africa. We employed concatenated gene-tree analyses, divergence dating approaches, and ancestral-area reconstructions to infer phylogenies and biogeographic patterns with a multi-locus data set consisting of three mitochondrial (16S, cyt b, and ND4) and two nuclear genes (c-mos and RAG1). As a result, we uncover several cryptic lineages and elevate a lineage of Polemon to full species status. Diversification occurred predominantly during the Miocene, with a few speciation events occurring subsequently in the Pliocene and Pleistocene. Biogeographic analyses suggested that the Zambezian biogeographic region, comprising grasslands and woodlands, facilitated radiations, vicariance, and dispersal for many aparallactines. Moreover, the geographic distributions of many forest species were fragmented during xeric and cooler conditions, which likely led to diversification events. Biogeographic patterns of aparallactine snakes are consistent with previous studies of other sub-Saharan herpetofauna.
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http://dx.doi.org/10.1016/j.ympev.2018.03.019DOI Listing
October 2018

Diversity and biogeography of frogs in the genus Amnirana (Anura: Ranidae) across sub-Saharan Africa.

Mol Phylogenet Evol 2018 03 12;120:274-285. Epub 2017 Dec 12.

California Academy of Sciences, San Francisco, CA 94118, USA; Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.

Frogs in the genus Amnirana (family Ranidae) are widely distributed across sub-Saharan Africa and present a model system for exploring the relationship between diversification and geography across the continent. Using multiple loci from the mitochondrial (16S) and nuclear genomes (DISP2, FICD, KIAA2013, REV3L), we generated a strongly supported species-level phylogeny that provides insights into the continental biogeography of African species of Amnirana, which form a monophyletic group within the genus. Species delimitation analyses suggest that there may be as many as seven additional species of Amnirana in Africa. The biogeographic history of Amnirana is marked by several dispersal and vicariance events, including dispersal from the Lower Guinean Forest into the Congo Basin. In addition, phylogeographic patterns within two widespread species, A. albolabris and A. galamensis, reveal undescribed cryptic diversity. Populations assigned to A. albolabris in western Africa are more closely related to A. fonensis and require recognition as a distinct species. Our analyses reveal that the Lower and Upper Guinean Forest regions served as important centers of interspecific and intraspecific diversifications for Amnirana.
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http://dx.doi.org/10.1016/j.ympev.2017.12.006DOI Listing
March 2018

Cryptic diversity in Rhampholeon boulengeri (Sauria: Chamaeleonidae), a pygmy chameleon from the Albertine Rift biodiversity hotspot.

Mol Phylogenet Evol 2018 05 2;122:125-141. Epub 2017 Dec 2.

Department of Biological Sciences, University of Texas at El Paso, El Paso, TX 79968, USA.

Several biogeographic barriers in the Central African highlands have reduced gene flow among populations of many terrestrial species in predictable ways. Yet, a comprehensive understanding of mechanisms underlying species divergence in the Afrotropics can be obscured by unrecognized levels of cryptic diversity, particularly in widespread species. We implemented a multilocus phylogeographic approach to examine diversity within the widely distributed Central African pygmy chameleon, Rhampholeon boulengeri. Gene-tree analyses coupled with a comparative coalescent-based species delimitation framework revealed R. boulengeri as a complex of at least six genetically distinct species. The spatiotemporal speciation patterns for these cryptic species conform to general biogeographic hypotheses supporting vicariance as the main factor behind patterns of divergence in the Albertine Rift, a biodiversity hotspot in Central Africa. However, we found that parapatric species and sister species inhabited adjacent habitats, but were found in largely non-overlapping elevational ranges in the Albertine Rift, suggesting that differentiation in elevation was also an important mode of divergence. The phylogeographic patterns recovered for the genus-level phylogeny provide additional evidence for speciation by isolation in forest refugia, and dating estimates indicated that the Miocene was a significant period for this diversification. Our results highlight the importance of investigating cryptic diversity in widespread species to improve understanding of diversification patterns in environmentally diverse regions such as the montane Afrotropics.
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http://dx.doi.org/10.1016/j.ympev.2017.11.015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6010225PMC
May 2018

Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands.

Mol Ecol 2017 Oct 24;26(19):5223-5244. Epub 2017 Aug 24.

Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA.

Organismal traits interact with environmental variation to mediate how species respond to shared landscapes. Thus, differences in traits related to dispersal ability or physiological tolerance may result in phylogeographic discordance among co-distributed taxa, even when they are responding to common barriers. We quantified climatic suitability and stability, and phylogeographic divergence within three reed frog species complexes across the Guineo-Congolian forests and Gulf of Guinea archipelago of Central Africa to investigate how they responded to a shared climatic and geological history. Our species-specific estimates of climatic suitability through time are consistent with temporal and spatial heterogeneity in diversification among the species complexes, indicating that differences in ecological breadth may partly explain these idiosyncratic patterns. Likewise, we demonstrated that fluctuating sea levels periodically exposed a land bridge connecting Bioko Island with the mainland Guineo-Congolian forest and that habitats across the exposed land bridge likely enabled dispersal in some species, but not in others. We did not find evidence that rivers are biogeographic barriers across any of the species complexes. Despite marked differences in the geographic extent of stable climates and temporal estimates of divergence among the species complexes, we recovered a shared pattern of intermittent climatic suitability with recent population connectivity and demographic expansion across the Congo Basin. This pattern supports the hypothesis that genetic exchange across the Congo Basin during humid periods, followed by vicariance during arid periods, has shaped regional diversity. Finally, we identified many distinct lineages among our focal taxa, some of which may reflect incipient or unrecognized species.
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http://dx.doi.org/10.1111/mec.14260DOI Listing
October 2017

The distribution of the Bururi Long-fingered Frog (Cardioglossa cyaneospila, family Arthroleptidae), a poorly known Albertine Rift endemic.

Zootaxa 2016 Sep 23;4170(2):355-364. Epub 2016 Sep 23.

Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.; Email:

The species diversity of the frog genus Cardioglossa (family Arthroleptidae) is concentrated in the Lower Guinean Forest Zone of Central Africa with most of the 19 species occurring in Cameroon and neighboring countries (Amiet 1972a,b; Blackburn 2008; Hirschfeld et al. 2015). These small leaf-litter frogs are typically found in primary or secondary forest, have shrill whistling calls, are characterized by a variety of color patterns, and lay terrestrial eggs that hatch and develop into elongate, stream-adapted tadpoles (Amiet 1972a,b, 1973; Rödel et al. 2001; Hirschfeld et al. 2012). One of the most poorly known species-the Bururi Long-fingered Frog Cardioglossa cyaneospila Laurent, 1950-is also among the most geographically peripheral to the rest of the species diversity. To date, it is known only from two locations in Burundi and four in eastern Democratic Republic of Congo, regions in which armed conflicts have long hampered scientific research. In this short contribution, we (1) document both new and long unpublished records of C. cyaneospila, associate these with known museum records, and extend its geographic range, (2) highlight fruitful areas for future field surveys based on predicting an environmental envelope for this species, and (3) summarize what little is known of its natural history.
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http://dx.doi.org/10.11646/zootaxa.4170.2.8DOI Listing
September 2016

Leapfrogging into new territory: How Mascarene ridged frogs diversified across Africa and Madagascar to maintain their ecological niche.

Mol Phylogenet Evol 2017 01 21;106:254-269. Epub 2016 Sep 21.

Trier University, Department of Biogeography, 54286 Trier, Germany. Electronic address:

The Mascarene ridged frog, Ptychadena mascareniensis, is a species complex that includes numerous lineages occurring mostly in humid savannas and open forests of mainland Africa, Madagascar, the Seychelles, and the Mascarene Islands. Sampling across this broad distribution presents an opportunity to examine the genetic differentiation within this complex and to investigate how the evolution of bioclimatic niches may have shaped current biogeographic patterns. Using model-based phylogenetic methods and molecular-clock dating, we constructed a time-calibrated molecular phylogenetic hypothesis for the group based on mitochondrial 16S rRNA and cytochrome b (cytb) genes and the nuclear RAG1 gene from 173 individuals. Haplotype networks were reconstructed and species boundaries were investigated using three species-delimitation approaches: Bayesian generalized mixed Yule-coalescent model (bGMYC), the Poisson Tree Process model (PTP) and a cluster algorithm (SpeciesIdentifier). Estimates of similarity in bioclimatic niche were calculated from species-distribution models (maxent) and multivariate statistics (Principal Component Analysis, Discriminant Function Analysis). Ancestral-area reconstructions were performed on the phylogeny using probabilistic approaches implemented in BioGeoBEARS. We detected high levels of genetic differentiation yielding ten distinct lineages or operational taxonomic units, and Central Africa was found to be a diversity hotspot for these frogs. Most speciation events took place throughout the Miocene, including "out-of-Africa" overseas dispersal events to Madagascar in the East and to São Tomé in the West. Bioclimatic niche was remarkably well conserved, with most species tolerating similar temperature and rainfall conditions common to the Central African region. The P. mascareniensis complex provides insights into how bioclimatic niche shaped the current biogeographic patterns with niche conservatism being exhibited by the Central African radiation and niche divergence shaping populations in West Africa and Madagascar. Central Africa, including the Albertine Rift region, has been an important center of diversification for this species complex.
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http://dx.doi.org/10.1016/j.ympev.2016.09.018DOI Listing
January 2017

Rescuing Perishable Neuroanatomical Information from a Threatened Biodiversity Hotspot: Remote Field Methods for Brain Tissue Preservation Validated by Cytoarchitectonic Analysis, Immunohistochemistry, and X-Ray Microcomputed Tomography.

PLoS One 2016 19;11(5):e0155824. Epub 2016 May 19.

Department of Biological Sciences, University of Texas at El Paso, El Paso, Texas, United States of America.

Biodiversity hotspots, which harbor more endemic species than elsewhere on Earth, are increasingly threatened. There is a need to accelerate collection efforts in these regions before threatened or endangered species become extinct. The diverse geographical, ecological, genetic, morphological, and behavioral data generated from the on-site collection of an individual specimen are useful for many scientific purposes. However, traditional methods for specimen preparation in the field do not permit researchers to retrieve neuroanatomical data, disregarding potentially useful data for increasing our understanding of brain diversity. These data have helped clarify brain evolution, deciphered relationships between structure and function, and revealed constraints and selective pressures that provide context about the evolution of complex behavior. Here, we report our field-testing of two commonly used laboratory-based techniques for brain preservation while on a collecting expedition in the Congo Basin and Albertine Rift, two poorly known regions associated with the Eastern Afromontane biodiversity hotspot. First, we found that transcardial perfusion fixation and long-term brain storage, conducted in remote field conditions with no access to cold storage laboratory equipment, had no observable impact on cytoarchitectural features of lizard brain tissue when compared to lizard brain tissue processed under laboratory conditions. Second, field-perfused brain tissue subjected to prolonged post-fixation remained readily compatible with subsequent immunohistochemical detection of neural antigens, with immunostaining that was comparable to that of laboratory-perfused brain tissue. Third, immersion-fixation of lizard brains, prepared under identical environmental conditions, was readily compatible with subsequent iodine-enhanced X-ray microcomputed tomography, which facilitated the non-destructive imaging of the intact brain within its skull. In summary, we have validated multiple approaches to preserving intact lizard brains in remote field conditions with limited access to supplies and a high degree of environmental exposure. This protocol should serve as a malleable framework for researchers attempting to rescue perishable and irreplaceable morphological and molecular data from regions of disappearing biodiversity. Our approach can be harnessed to extend the numbers of species being actively studied by the neuroscience community, by reducing some of the difficulty associated with acquiring brains of animal species that are not readily available in captivity.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0155824PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4873048PMC
July 2017

Molecular phylogeny of Panaspis and Afroablepharus skinks (Squamata: Scincidae) in the savannas of sub-Saharan Africa.

Mol Phylogenet Evol 2016 07 23;100:409-423. Epub 2016 Apr 23.

Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968, USA. Electronic address:

African snake-eyed skinks are relatively small lizards of the genera Panaspis and Afroablepharus. Species allocation of these genera frequently changed during the 20th century based on morphology, ecology, and biogeography. Members of these genera occur primarily in savanna habitats throughout sub-Saharan Africa and include species whose highly conserved morphology poses challenges for taxonomic studies. We sequenced two mitochondrial (16S and cyt b) and two nuclear genes (PDC and RAG1) from 76 Panaspis and Afroablepharus samples from across eastern, central, and southern Africa. Concatenated gene-tree and divergence-dating analyses were conducted to infer phylogenies and biogeographic patterns. Molecular data sets revealed several cryptic lineages, with most radiations occurring during the mid-Miocene to Pliocene. We infer that rifting processes (including the formation of the East African Rift System) and climatic oscillations contributed to the expansion and contraction of savannas, and caused cladogenesis in snake-eyed skinks. Species in Panaspis and Afroablepharus used in this study, including type species for both genera, formed a monophyletic group. As a result, the latter genus should be synonymized with the former, which has priority. Conservatively, we continue to include the West African species P. breviceps and P. togoensis within an expanded Panaspis, but note that they occur in relatively divergent clades, and their taxonomic status may change with improved taxon sampling. Divergence estimates and cryptic speciation patterns of snake-eyed skinks were consistent with previous studies of other savanna vertebrate lineages from the same areas examined in this study.
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http://dx.doi.org/10.1016/j.ympev.2016.04.026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898058PMC
July 2016

Evolutionary history of the river frog genus Amietia (Anura: Pyxicephalidae) reveals extensive diversification in Central African highlands.

Mol Phylogenet Evol 2016 06 26;99:168-181. Epub 2016 Mar 26.

Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968, USA. Electronic address:

The African river frog genus Amietia is found near rivers and other lentic water sources throughout central, eastern, and southern Africa. Because the genus includes multiple morphologically conservative species, taxonomic studies of river frogs have been relatively limited. We sampled 79 individuals of Amietia from multiple localities in and near the Albertine Rift (AR) of Burundi, Democratic Republic of the Congo, and Uganda. We utilized single-gene (16S) and concatenated (12S, 16S, cyt b and RAG1) gene-tree analyses and coalescent species-tree analyses to construct phylogenetic trees. Two divergence dating approaches were used in BEAST, including secondary calibration points with 12S, 16S, cyt b and RAG1, and a molecular clock with the 12S, 16S, and cyt b genes. All analyses recovered Amietia as monophyletic with strong support, and revealed several well-supported cryptic lineages, which is consistent with other recent phylogeography studies of AR amphibians. Dating estimates were similar, and Amietia diversification is coincident with global cooling and aridification events in the Miocene and Pliocene, respectively. Our results suggest additional taxonomic work is needed to describe multiple new species of AR Amietia, some of which have limited geographic distributions that are likely to be of conservation concern.
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http://dx.doi.org/10.1016/j.ympev.2016.03.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898062PMC
June 2016

Embryogenesis and tadpole description of Hyperolius castaneus Ahl, 1931 and H. jackie Dehling, 2012 (Anura, Hyperoliidae) from montane bog pools.

Zookeys 2015 16(546):125-52. Epub 2015 Dec 16.

Institute of Integrated Sciences, Department of Biology, University of Koblenz-Landau, Universitätsstr. 1, D-56070 Koblenz, Germany.

Tadpoles of Hyperolius castaneus and Hyperolius jackie were found in the Nyungwe National Park in Rwanda and adjacent areas. Tadpoles of both species were identified by DNA-barcoding. At the shore of a bog pool three clutches of Hyperolius castaneus of apparently different age, all laid on moss pads (Polytrichum commune, Isotachis aubertii) or grass tussocks (Andropogon shirensis) 2-5 cm above the water level, were found. One clutch of Hyperolius castaneus was infested by larval dipterid flies. The most recently laid clutch contained about 20 eggs within a broad egg-jelly envelope. The eggs were attached to single blades of a tussock and distributed over a vertical distance of 8 cm. A pair of Hyperolius castaneus found in axillary amplexus was transported in a plastic container to the lab for observation. The pair deposited a total of 57 eggs (15 eggs attached to the upper wall of the transport container, 42 eggs floated in the water). Embryogenesis of the clutch was monitored in the plastic container at 20 ± 2 °C (air temperature) and documented by photos until Gosner Stage 25. The description of the tadpole of Hyperolius castaneus is based on a Gosner Stage 29 individual from a series of 57 tadpoles (Gosner stages 25-41). The description of the tadpole of Hyperolius jackie is based on a Gosner Stage 32 individual from a series of 43 tadpoles (Gosner stages 25-41). Egg laying behavior and embryogenesis are unknown for Hyperolius jackie. The labial tooth row formula for both species is 1/3(1) with a narrow median gap of the tooth row. Variation in external morphology was observed in size and labial tooth row formula within the species. With the tadpole descriptions of Hyperolius castaneus and Hyperolius jackie, 36 tadpoles of the 135 known Hyperolius species have been described, including five of the eleven Hyperolius species known from Rwanda.
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http://dx.doi.org/10.3897/zookeys.546.6044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4714350PMC
January 2016

Assessing the Threat of Amphibian Chytrid Fungus in the Albertine Rift: Past, Present and Future.

PLoS One 2015 28;10(12):e0145841. Epub 2015 Dec 28.

Wildlife Conservation Society, Bronx, NY, United States of America.

Batrachochytrium dendrobatidis (Bd), the cause of chytridiomycosis, is a pathogenic fungus that is found worldwide and is a major contributor to amphibian declines and extinctions. We report results of a comprehensive effort to assess the distribution and threat of Bd in one of the Earth's most important biodiversity hotspots, the Albertine Rift in central Africa. In herpetological surveys conducted between 2010 and 2014, 1018 skin swabs from 17 amphibian genera in 39 sites across the Albertine Rift were tested for Bd by PCR. Overall, 19.5% of amphibians tested positive from all sites combined. Skin tissue samples from 163 amphibians were examined histologically; of these two had superficial epidermal intracorneal fungal colonization and lesions consistent with the disease chytridiomycosis. One amphibian was found dead during the surveys, and all others encountered appeared healthy. We found no evidence for Bd-induced mortality events, a finding consistent with other studies. To gain a historical perspective about Bd in the Albertine Rift, skin swabs from 232 museum-archived amphibians collected as voucher specimens from 1925-1994 were tested for Bd. Of these, one sample was positive; an Itombwe River frog (Phrynobatrachus asper) collected in 1950 in the Itombwe highlands. This finding represents the earliest record of Bd in the Democratic Republic of Congo. We modeled the distribution of Bd in the Albertine Rift using MaxEnt software, and trained our model for improved predictability. Our model predicts that Bd is currently widespread across the Albertine Rift, with moderate habitat suitability extending into the lowlands. Under climatic modeling scenarios our model predicts that optimal habitat suitability of Bd will decrease causing a major range contraction of the fungus by 2080. Our baseline data and modeling predictions are important for comparative studies, especially if significant changes in amphibian health status or climactic conditions are encountered in the future.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0145841PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4692535PMC
July 2016

Genetics, Morphology, Advertisement Calls, and Historical Records Distinguish Six New Polyploid Species of African Clawed Frog (Xenopus, Pipidae) from West and Central Africa.

PLoS One 2015 16;10(12):e0142823. Epub 2015 Dec 16.

California Academy of Sciences, San Francisco, California, United States of America.

African clawed frogs, genus Xenopus, are extraordinary among vertebrates in the diversity of their polyploid species and the high number of independent polyploidization events that occurred during their diversification. Here we update current understanding of the evolutionary history of this group and describe six new species from west and central sub-Saharan Africa, including four tetraploids and two dodecaploids. We provide information on molecular variation, morphology, karyotypes, vocalizations, and estimated geographic ranges, which support the distinctiveness of these new species. We resurrect Xenopus calcaratus from synonymy of Xenopus tropicalis and refer populations from Bioko Island and coastal Cameroon (near Mt. Cameroon) to this species. To facilitate comparisons to the new species, we also provide comments on the type specimens, morphology, and distributions of X. epitropicalis, X. tropicalis, and X. fraseri. This includes significantly restricted application of the names X. fraseri and X. epitropicalis, the first of which we argue is known definitively only from type specimens and possibly one other specimen. Inferring the evolutionary histories of these new species allows refinement of species groups within Xenopus and leads to our recognition of two subgenera (Xenopus and Silurana) and three species groups within the subgenus Xenopus (amieti, laevis, and muelleri species groups).
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0142823PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4682732PMC
June 2016

Molecular data from contemporary and historical collections reveal a complex story of cryptic diversification in the Varanus (Polydaedalus) niloticus Species Group.

Mol Phylogenet Evol 2016 Jan 22;94(Pt B):591-604. Epub 2015 Oct 22.

Department of Biological Sciences, Fordham University, 441 East Fordham Road, Bronx, NY 10458, United States. Electronic address:

Previous studies of color pattern, tongue pigmentation, and scale counts have been used to distinguish two species of semiaquatic varanids in Africa, but these findings have yet to be tested with molecular data. The Varanus (Polydaedalus) niloticus Species Group is comprised of the Nile monitor (V. niloticus) and the Ornate monitor (V. ornatus). Due to the high rate of exploitation of both species for bushmeat, the leather industry, and the pet trade, a clear understanding of the taxonomy and genetic partitioning is necessary for effective management. Here we utilize a multilocus approach, consisting of mitochondrial and nuclear markers, totaling 4251 bp, as well as microsatellite loci to assess the taxonomic validity and intraspecific evolutionary patterns within the V. niloticus Species Group. By incorporating historical specimens from museum collections as well as contemporary samples, we obtained range-wide coverage for both species across Africa. Concordant results from various approaches all suggest that V. ornatus does not represent a distinct monophyletic group. Our analyses recovered three genetic clades within V. niloticus, representing western, northern, and southern lineages. The western clade was found to diverge first, around 7.7 mya (95% HPD: 4.6-11.0 mya) and exhibits 8.4% and 8.7% uncorrected sequence divergence between the northern and southern V. niloticus clades, respectively. This geographically separate lineage corresponds to previous descriptions of Tupinambis stellatusDaudin (1802). These findings not only call for taxonomic revision of this species group, but also shed light on the biogeographic history of Africa as well as aid in the management planning of varanids and other co-distributed African species.
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http://dx.doi.org/10.1016/j.ympev.2015.10.004DOI Listing
January 2016

Pan-African phylogeography of a model organism, the African clawed frog 'Xenopus laevis'.

Mol Ecol 2015 Feb 3;24(4):909-25. Epub 2015 Feb 3.

Biology Department, McMaster University, Life Sciences Building, 1280 Main Street West, Hamilton, Ontario, Canada, L8S 4K1.

The African clawed frog Xenopus laevis has a large native distribution over much of sub-Saharan Africa and is a model organism for research, a proposed disease vector, and an invasive species. Despite its prominent role in research and abundance in nature, surprisingly little is known about the phylogeography and evolutionary history of this group. Here, we report an analysis of molecular variation of this clade based on 17 loci (one mitochondrial, 16 nuclear) in up to 159 individuals sampled throughout its native distribution. Phylogenetic relationships among mitochondrial DNA haplotypes were incongruent with those among alleles of the putatively female-specific sex-determining gene DM-W, in contrast to the expectation of strict matrilineal inheritance of both loci. Population structure and evolutionarily diverged lineages were evidenced by analyses of molecular variation in these data. These results further contextualize the chronology, and evolutionary relationships within this group, support the recognition of X. laevis sensu stricto, X. petersii, X. victorianus and herein revalidated X. poweri as separate species. We also propose that portions of the currently recognized distributions of X. laevis (north of the Congo Basin) and X. petersii (south of the Congo Basin) be reassigned to X. poweri.
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http://dx.doi.org/10.1111/mec.13076DOI Listing
February 2015

Phylogeography and species boundaries of Leptopelis (Anura: Arthroleptidae) from the Albertine Rift.

Mol Phylogenet Evol 2015 Jan 5;82 Pt A:75-86. Epub 2014 Oct 5.

Institut für Integrierte Naturwissenschaften, Abteilung Biologie, AG Zoologie, Universität Koblenz-Landau, Universitätsstraße 1, 56070 Koblenz, Germany.

The genus Leptopelis occurs in multiple habitats throughout sub-Saharan Africa, and it includes several species that have highly variable color patterns, which makes taxonomic studies challenging. In this study, we examined multiple populations of Leptopelis from the Albertine Rift (AR), a region known for its high levels of endemism and biodiversity. Currently, five species are recognized from the AR: L. anebos, L. fiziensis, L. karissimbensis, L. kivuensis, and L. mtoewaate, most of which are found in and around the Itombwe Plateau in Democratic Republic of the Congo (DRC). We sampled 90 individuals of Leptopelis from multiple localities in DRC, Uganda, Rwanda and Burundi. We employed concatenated gene-tree analyses, coalescent species-tree analyses, and divergence dating approaches to infer phylogenies and biogeographic patterns with a multi-locus data set consisting of two mitochondrial (16S and cyt b) and one nuclear gene (RAG1). All analyses revealed several cryptic lineages within the genus, suggesting that a revision of AR Leptopelis taxonomy is needed.
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http://dx.doi.org/10.1016/j.ympev.2014.09.024DOI Listing
January 2015

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

Phylogeography of the reed frog Hyperolius castaneus (Anura: Hyperoliidae) from the Albertine Rift of Central Africa: implications for taxonomy, biogeography and conservation.

Zootaxa 2013 Nov 1;3731:473-94. Epub 2013 Nov 1.

Affiliation: unknown; Email: unknown.

We examine the systematics of multiple populations of the Albertine Rift endemic amphibian Hyperolius castaneus, which currently incorporates four subspecies. Standard morphometric data were analyzed with principal components analyses and analyses of covariance. Phylogenetic analyses of two mitochondrial (16S, cyt b) and one nuclear (RAG1) genes were analyzed from 41 samples representing three subspecies. Results indicated some significant morphometric differences between the nominate subspecies H. c. castaneus and the Itombwe Plateau subspecies H. c. constellatus, and phylogenetic analyses of molecular data recovered these taxa as reciprocally monophyletic groups. We recognize these two allopatric populations as recently diverged, but distinct species, H. castaneus and H. constellatus. The subspecies H. c. submarginatus from the Kabobo Plateau is transferred to the synonymy of H. constellatus, but the status of the unsampled subspecies H. c. rhodogaster, described from mid-elevations of the western Itombwe Plateau, remains problematic. The phylogeographic pattern of our study resembles some, but not all, Albertine Rift vertebrates that have been examined with molecular data. Hyperolius constellatus is restricted to the Itombwe and Kabobo plateaus, which are of special conservation concern because of high levels of amphibian diversity and endemism, and multiple threats from deforestation, mining activities and road construction.
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http://dx.doi.org/10.11646/zootaxa.3731.4.3DOI Listing
November 2013

Molecular phylogeny of microhylid frogs (Anura: Microhylidae) with emphasis on relationships among New World genera.

BMC Evol Biol 2012 Dec 10;12:241. Epub 2012 Dec 10.

Department of Biology, University of Richmond, Richmond, VA 23173, USA.

Background: Over the last ten years we have seen great efforts focused on revising amphibian systematics. Phylogenetic reconstructions derived from DNA sequence data have played a central role in these revisionary studies but have typically under-sampled the diverse frog family Microhylidae. Here, we present a detailed phylogenetic study focused on expanding previous hypotheses of relationships within this cosmopolitan family. Specifically, we placed an emphasis on assessing relationships among New World genera and those taxa with uncertain phylogenetic affinities (i.e., incertae sedis).

Results: One mitochondrial and three nuclear genes (about 2.8 kb) were sequenced to assess phylogenetic relationships. We utilized an unprecedented sampling of 200 microhylid taxa representing 91% of currently recognized subfamilies and 95% of New World genera. Our analyses do not fully resolve relationships among subfamilies supporting previous studies that have suggested a rapid early diversification of this clade. We observed a close relationship between Synapturanus and Otophryne of the subfamily Otophryninae. Within the subfamily Gastrophryninae relationships between genera were well resolved.

Conclusion: Otophryninae is distantly related to all other New World microhylids that were recovered as a monophyletic group, Gastrophryninae. Within Gastrophryninae, five genera were recovered as non-monophyletic; we propose taxonomic re-arrangements to render all genera monophyletic. This hypothesis of relationships and updated classification for New World microhylids may serve as a guide to better understand the evolutionary history of this group that is apparently subject to convergent morphological evolution and chromosome reduction. Based on a divergence analysis calibrated with hypotheses from previous studies and fossil data, it appears that microhylid genera inhabiting the New World originated during a period of gradual cooling from the late Oligocene to mid Miocene.
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http://dx.doi.org/10.1186/1471-2148-12-241DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3561245PMC
December 2012

Evolution of gliding in Southeast Asian geckos and other vertebrates is temporally congruent with dipterocarp forest development.

Biol Lett 2012 Dec 12;8(6):994-7. Epub 2012 Sep 12.

Department of Biology, Villanova University, Mendel Hall, 800 Lancaster Avenue, Villanova, PA 19085, USA.

Gliding morphologies occur in diverse vertebrate lineages in Southeast Asian rainforests, including three gecko genera, plus frogs, snakes, agamid lizards and squirrels. It has been hypothesized that repeated evolution of gliding is related to the dominance of Asian rainforest tree floras by dipterocarps. For dipterocarps to have influenced the evolution of gliding in Southeast Asian vertebrates, gliding lineages must have Eocene or later origins. However, divergence times are not known for most lineages. To investigate the temporal pattern of Asian gliding vertebrate evolution, we performed phylogenetic and molecular clock analyses. New sequence data for geckos incorporate exemplars of each gliding genus (Cosymbotus, Luperosaurus and Ptychozoon), whereas analyses of other vertebrate lineages use existing sequence data. Stem ages of most gliding vertebrates, including all geckos, cluster in the time period when dipterocarps came to dominate Asian tropical forests. These results demonstrate that a gliding/dipterocarp correlation is temporally viable, and caution against the assumption of early origins for apomorphic taxa.
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http://dx.doi.org/10.1098/rsbl.2012.0648DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3497132PMC
December 2012

Repeated origin and loss of adhesive toepads in geckos.

PLoS One 2012 27;7(6):e39429. Epub 2012 Jun 27.

Department of Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, Minnesota, United States of America.

Geckos are well known for their extraordinary clinging abilities and many species easily scale vertical or even inverted surfaces. This ability is enabled by a complex digital adhesive mechanism (adhesive toepads) that employs van der Waals based adhesion, augmented by frictional forces. Numerous morphological traits and behaviors have evolved to facilitate deployment of the adhesive mechanism, maximize adhesive force and enable release from the substrate. The complex digital morphologies that result allow geckos to interact with their environment in a novel fashion quite differently from most other lizards. Details of toepad morphology suggest multiple gains and losses of the adhesive mechanism, but lack of a comprehensive phylogeny has hindered efforts to determine how frequently adhesive toepads have been gained and lost. Here we present a multigene phylogeny of geckos, including 107 of 118 recognized genera, and determine that adhesive toepads have been gained and lost multiple times, and remarkably, with approximately equal frequency. The most likely hypothesis suggests that adhesive toepads evolved 11 times and were lost nine times. The overall external morphology of the toepad is strikingly similar in many lineages in which it is independently derived, but lineage-specific differences are evident, particularly regarding internal anatomy, with unique morphological patterns defining each independent derivation.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0039429PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3384654PMC
March 2013