[Show abstract][Hide abstract] ABSTRACT: Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.
[Show abstract][Hide abstract] ABSTRACT: For amphibians, non-lethal sampling methods have been developed and evaluated for only two of the three extant orders, with the limbless caecilians (Gymnophiona) thus far overlooked. Here we assess 16 different methods in five caecilian species representing five families with differing morphologies and ecologies. DNA was successfully extracted and amplified for multiple genetic markers using all tested methods in at least some cases although yields are, unsurprisingly, generally substantially lower than for DNA extractions from (lethally sampled) liver. Based on PCR performance, DNA yield and sampling considerations, buccal swabs, skin scrapes, blood pricks and dermal scalepocket biopsies performed the best.
[Show abstract][Hide abstract] ABSTRACT: Supertrees combine disparate, partially overlapping trees to generate a synthesis that provides a high level perspective that cannot be attained from the inspection of individual phylogenies. Supertrees can be seen as meta-analytical tools that can be used to make inferences based on results of previous scientific studies. Their meta-analytical application has increased in popularity since it was realised that the power of statistical tests for the study of evolutionary trends critically depends on the use of taxon-dense phylogenies. Further to that, supertrees have found applications in phylogenomics where they are used to combine gene trees and recover species phylogenies based on genome-scale data sets.
[Show abstract][Hide abstract] ABSTRACT: The hyperoliid frog Tachycnemis seychellensis, the only species of its genus, is endemic to the four largest granitic islands of the Seychelles archipelago and is reliant on freshwater bodies for reproduction. Its presence in the Seychelles is thought to be the product of a transoceanic dispersal, diverging from the genus Heterixalus, its closest living relative (currently endemic to Madagascar), between approximately 10-35Ma. A previous study documented substantial intraspecific morphological variation among island populations and also among populations within the largest island (Mahé). To assess intraspecific genetic variation and to infer the closest living relative(s) of T. seychellensis, DNA sequence data were generated for three mitochondrial and four nuclear markers. These data support a sister-group relationship between T. seychellensis and Heterixalus, with the divergence between the two occurring between approximately 11-19Ma based on cytb p-distances. Low levels of genetic variation were found among major mitochondrial haplotype clades of T. seychellensis (maximum 0.7% p-distance concatenated mtDNA), and samples from each of the islands (except La Digue) comprised multiple mitochondrial haplotype clades. Two nuclear genes (rag1 and tyr) showed no variation, and the other two (rho, pomc) lacked any notable geographic structuring, counter to patterns observed within presumably more vagile Seychelles taxa such as lizards. The low levels of genetic variation and phylogeographic structure support an interpretation that there is a single but morphologically highly variable species of Seychelles treefrog. The contrasting genetic and morphological intraspecific variation may be attributable to relatively recent admixture during low sea-level stands, ecophenotypic plasticity, local adaptation to different environmental conditions, and/or current and previously small population sizes. Low genetic diversity but substantial morphological variation is unusual within anurans.
Molecular Phylogenetics and Evolution 06/2014; 75:194-201. · 4.02 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: A new species of striped ichthyophiid caecilian, Ichthyophis multicolor sp. nov., is described on the basis of morphological and molecular data from a sample of 14 specimens from Ayeyarwady Region, Myanmar. The new species resembles superficially the Indian I. tricolor Annandale, 1909 in having both a pale lateral stripe and an adjacent dark ventrolateral stripe contrasting with a paler venter. It differs from I. tricolor in having many more annuli, and in many details of cranial osteology, and molecular data indicate that it is more closely related to other Southeast Asian Ichthyophis than to those of South Asia. The caecilian fauna of Myanmar is exceptionally poorly known but is likely to include chikilids as well as multiple species of Ichthyophis.
[Show abstract][Hide abstract] ABSTRACT: AimThe persistence and stability of habitats through time are considered predictors of high levels of biodiversity in some environments. Long-term habitat persistence and stability may explain the species-rich, endemic forest fauna and flora of the Eastern Afromontane Biodiversity Region (EABR). Using complementary phylogenetic and biogeographical approaches, we examine evolutionary patterns in EABR brevicipitid frogs. Using these data, we test whether brevicipitid history reflects patterns of long-term forest persistence and/or stability across the EABR.LocationEast Africa.MethodsA dated phylogeny for brevicipitids was constructed using two nuclear and three mitochondrial markers. Alternative diversification models were used to determine signal for constant or varying net diversification rates. Using our dated tree, we identified areas of high phylogenetic diversity (PD), and inferred ancestral areas using likelihood and Bayesian approaches.ResultsBrevicipitids have a long history, with generic diversification among extant lineages pre-dating the Oligocene (> 33 Ma). Ancestral-area reconstructions indicate the presence of brevicipitids in the EABR since the Oligocene, and support a scenario of palaeoendemics surviving in EABR refugia. Ancestral-area reconstructions indicate that the central Eastern Arc Mountains (EAM) formed the initial centre of diversification of forest brevicipitids. Measures of PD show that diversity varies across the EABR but is highest in the EAM. Constant net diversification rate in brevicipitids is a significantly better fit than alternative, rate-variable models.Main conclusionsThe degree of persistence of forest habitats appears to be a contributing factor to the varying levels of diversity across the EABR in brevicipitids (and other organisms). In contrast to the Southern Highlands and Ethiopian Bale Mountains, the EAM stands out as an area that enabled the constant accumulation of brevicipitid species over a long period of time.
Journal of Biogeography 04/2014; · 4.97 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Lake Tanganyika (LT) is a biodiversity hotspot supporting many endemic radiations that provide comparative systems in which to investigate if there are common factors leading to the build-up of its considerable diversity. Despite LT containing the highest diversity of lacustrine catfishes on Earth, the evolutionary relationships of nocturnal catfishes within the sub-family Claroteinae have not been investigated and it is unknown if its constituent genera have diversified via single or independent colonisation events. We report the first molecular phylogeny of the LT Claroteinae based on a multigene dataset (three nuclear markers, two mitochondrial totalling 4227bp), including 85 samples from LT and outside of the lake basin. These data support LT claroteine monophyly, with the exclusion of the LT endemic Chrysichthys brachynema that independently colonised the lake but has not radiated. Multiple sampling localities from LT and the use of Bayesian species delimitation methods reveal additional locally restricted diversity within the LT Claroteinae clade. Fossil calibrated molecular divergence dates suggest that diversification occurred within full lake conditions as demonstrated in other LT lineages.
Molecular Phylogenetics and Evolution 04/2014; · 4.02 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: According to current understanding, five lineages of amphibians, but no other tetrapods, are secondarily lungless and are believed to rely exclusively on cutaneous gas exchange. One explanation of the evolutionary loss of lungs interprets lunglessness as an adaptation to reduce buoyancy in fast-flowing aquatic environments, reasoning that excessive buoyancy in such an environment would cause organisms being swept away. While not uncontroversial, this hypothesis provides a plausible potential explanation of the evolution of lunglessness in four of the five lungless amphibian lineages. The exception is the most recently reported lungless lineage, the newly described Guyanan caecilian genus and species Caecilita iwokramae Wake & Donnelly, 2010, which is inconsistent with the reduced disadvantageous buoyancy hypothesis by virtue of it seemingly being terrestrial and having a terrestrial ancestry. Re-examination of the previously only known specimen of C. iwokramae and of recently collected additional material reveal that this species possesses a reasonably well-developed right lung and is a species of the pre-existing caecilian genus Microcaecilia Taylor, 1968. We therefore place Caecilita in the synonymy of Microcaecilia, and re-evaluate the plausibility of the reduced disadvantageous buoyancy hy- pothesis as a general explanation of the evolution of lunglessness.
[Show abstract][Hide abstract] ABSTRACT: The phylogenetic relationships of many taxa remain poorly known because of a lack of appropriate data and/or analyses. Despite substantial recent advances, amphibian phylogeny remains poorly resolved in many instances. The phylogenetic relationships of the Ethiopian endemic monotypic genus Ericabatrachus has been addressed thus far only with phenotypic data and remains contentious.
We obtained fresh samples of the now rare and Critically Endangered Ericabatrachus baleensis and generated DNA sequences for two mitochondrial and four nuclear genes. Analyses of these new data using de novo and constrained-tree phylogenetic reconstructions strongly support a close relationship between Ericabatrachus and Petropedetes, and allow us to reject previously proposed alternative hypotheses of a close relationship with cacosternines or Phrynobatrachus.
We discuss the implications of our results for the taxonomy, biogeography and conservation of E. baleensis, and suggest a two-tiered approach to the inclusion and analyses of new data in order to assess the phylogenetic relationships of previously unsampled taxa. Such approaches will be important in the future given the increasing availability of relevant mega-alignments and potential framework phylogenies.
[Show abstract][Hide abstract] ABSTRACT: We analyze mitochondrial genomes to reconstruct a robust phylogenetic framework for caecilian amphibians and use this to investigate life-history evolution within the group. Our study comprises 45 caecilian mitochondrial genomes (19 of them newly reported), representing all families and 27 of 32 currently recognized genera, including some for which molecular data had never been reported. Support for all relationships in the inferred phylogenetic tree is high to maximal, and topology tests reject all investigated alternatives, indicating an exceptionally robust molecular phylogenetic framework of caecilian evolution consistent with current morphology-based supraspecific classification. We used the mitogenomic phylogenetic framework to infer ancestral character states and to assess correlation among three life-history traits (free-living larvae, viviparity, specialized pre-adult or vernal teeth), each of which occurs only in some caecilian species. Our results provide evidence that an ancestor of the Seychelles caecilians abandoned direct development and re-evolved a free-living larval stage. This study yields insights into the concurrent evolution of direct development and of vernal teeth in an ancestor of Teresomata that likely gave rise to skin-feeding (maternal dermatophagy) behavior and subsequently enabled evolution of viviparity, with skin feeding possibly a homologous precursor of oviduct feeding in viviparous caecilians.
Molecular Phylogenetics and Evolution 01/2014; 73:177-189. · 4.02 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Anonymous nuclear markers were developed
for Seychelles caecilian amphibians. Using a previously
published bioinformatics pipeline (developed for Roche
454 data), 36 candidate anonymous nuclear loci (ANL) of
at least 180 bp length were identiﬁed from Illumina MiSeq
next generation sequencing data for ﬁve Seychelles species. We designed primer pairs for the 36 candidate ANL
and tested these by PCR and Sanger sequencing. Seven
ANL ampliﬁed and sequenced well for at least ﬁve of the
six nominal Seychelles caecilian species (in three genera),
and represent potentially useful markers for systematics
[Show abstract][Hide abstract] ABSTRACT: Defining homologous genes is important in many evolutionary studies but raises obvious issues. Some of these issues are conceptual, and stem from our assumptions of how a gene evolves, others are practical, and depend on the algorithmic decisions implemented in existing software. Therefore, in order to make progress in the study of homology, both ontological and epistemological questions must be considered. In particular, defining homologous genes cannot solely be addressed under the classic assumptions of strong tree-thinking, according to which genes evolve in a strictly tree-like fashion of vertical descent and divergence and the problems of homology detection are primarily methodological. Gene homology could also be considered under a different perspective where genes evolve as 'public goods', subjected to various introgressive processes. In this latter case, defining homologous genes becomes a matter of designing models suited to the actual complexity of the data and how such complexity arises, rather than trying to fit genetic data to some a priori tree-like evolutionary model, a practice that inevitably results in the loss of much information. Here we show how important aspects of the problems raised by homology detection methods can be overcome when even more fundamental roots of these problems are addressed by analysing 'public goods thinking' evolutionary processes through which genes have frequently originated. This kind of thinking acknowledges distinct types of homologs, characterised by distinct patterns, in phylogenetic and non phylogenetic unrooted or multi-rooted networks. In addition, we define "family resemblances" to include genes that are related through intermediate relatives, thereby placing notions of homology in the broader context of evolutionary relationships. We conclude by presenting some pay-offs of adopting such a pluralistic account of homology and family relationship, that expands the scope of evolutionary analyses beyond the traditional, yet relatively narrow focus allowed by a strong tree-thinking view on gene evolution.
Molecular Biology and Evolution 11/2013; · 14.31 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: A taxonomic review of the monogeneric northeast Indian caecilian family Chikilidae is presented based on 64 specimens. Chikila fulleri (Alcock, 1904), known previously only from a single specimen collected more than 100 years ago, is rediagnosed and characterised based on recent collections. We describe three additional species new to science, Chikila alcocki sp. nov., Chikila darlong sp. nov., and Chikila gaiduwani sp. nov. This species-level taxonomy is consistent with mitochondrial DNA sequence data. A key to the species of Chikila is presented.
[Show abstract][Hide abstract] ABSTRACT: We describe the distinctive but previously overlooked shape and position of the fat bodies of some scolecomorphid caecilians. Anteriorly positioned, finger-like fat bodies projecting into the coelom from narrow bases in the genital mesenteries are found in both sexes of all species of the East African caecilian genus Scolecomorphus and are unknown elsewhere. We interpret this as a visceral synapomorphy of Scolecomorphus that may be related to viviparity in this genus.
African Journal of Herpetology 06/2013; 62(1):21-27. · 1.08 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Batrachochytrium dendrobatidis (Bd) is commonly termed the 'amphibian chytrid fungus' but thus far has been documented to be a pathogen of only batrachian amphibians (anurans and caudatans). It is not proven to infect the limbless, generally poorly known, and mostly soil-dwelling caecilians (Gymnophiona). We conducted the largest qPCR survey of Bd in caecilians to date, for more than 200 field-swabbed specimens from five countries in Africa and South America, representing nearly 20 species, 12 genera, and 8 families. Positive results were recovered for 58 specimens from Tanzania and Cameroon (4 families, 6 genera, 6+ species). Quantities of Bd were not exceptionally high, with genomic equivalent (GE) values of 0.052-17.339. In addition, we report the first evidence of lethal chytridiomycosis in caecilians. Mortality in captive (wild-caught, commercial pet trade) Geotrypetes seraphini was associated with GE scores similar to those we detected for field-swabbed, wild animals.