Dataset Information

Biogeography, phylogeny, and morphological evolution of central Texas cave and spring salamanders.

ABSTRACT: BACKGROUND: Subterranean faunal radiations can result in complex patterns of morphological divergence involving both convergent or parallel phenotypic evolution and cryptic species diversity. Salamanders of the genus Eurycea in central Texas provide a particularly challenging example with respect to phylogeny reconstruction, biogeography and taxonomy. These predominantly aquatic species inhabit karst limestone aquifers and spring outflows, and exhibit a wide range of morphological and genetic variation. We extensively sampled spring and cave populations of six Eurycea species within this group (eastern Blepsimolge clade), to reconstruct their phylogenetic and biogeographic history using mtDNA and examine patterns and origins of cave- and surface-associated morphological variation. RESULTS: Genetic divergence is generally low, and many populations share ancestral haplotypes and/or show evidence of introgression. This pattern likely indicates a recent radiation coupled with a complex history of intermittent connections within the aquatic karst system. Cave populations that exhibit the most extreme troglobitic morphologies show no or very low divergence from surface populations and are geographically interspersed among them, suggesting multiple instances of rapid, parallel phenotypic evolution. Morphological variation is diffuse among cave populations; this is in contrast to surface populations, which form a tight cluster in morphospace. Unexpectedly, our analyses reveal two distinct and previously unrecognized morphological groups encompassing multiple species that are not correlated with spring or cave habitat, phylogeny or geography, and may be due to developmental plasticity. CONCLUSIONS: The evolutionary history of this group of spring- and cave-dwelling salamanders reflects patterns of intermittent isolation and gene flow influenced by complex hydrogeologic dynamics that are characteristic of karst regions. Shallow genetic divergences among several species, evidence of genetic exchange, and nested relationships across morphologically disparate cave and spring forms suggests that cave invasion was recent and many troglobitic morphologies arose independently. These patterns are consistent with an adaptive-shift hypothesis of divergence, which has been proposed to explain diversification in other karst fauna. While cave and surface forms often do not appear to be genetically isolated, morphological diversity within and among populations may be maintained by developmental plasticity, selection, or a combination thereof.

SUBMITTER: Bendik NF

PROVIDER: S-EPMC3848792 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Biogeography, phylogeny, and morphological evolution of central Texas cave and spring salamanders.

Bendik Nathan F NF Meik Jesse M JM Gluesenkamp Andrew G AG Roelke Corey E CE Chippindale Paul T PT

BMC evolutionary biology 20130917

<h4>Background</h4>Subterranean faunal radiations can result in complex patterns of morphological divergence involving both convergent or parallel phenotypic evolution and cryptic species diversity. Salamanders of the genus Eurycea in central Texas provide a particularly challenging example with respect to phylogeny reconstruction, biogeography and taxonomy. These predominantly aquatic species inhabit karst limestone aquifers and spring outflows, and exhibit a wide range of morphological and gen ...[more]

PMID: 24044519

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Project description:The salamander clade Eurycea from the karst regions of central Texas provides an ideal platform for comparing divergent nervous and sensory systems since some species exhibit extreme phenotypes thought to be associated with inhabiting a subterranean environment, including highly reduced eyes, while others retain an ancestral ocular phenotype appropriate for life above ground. We describe ocular morphology, comparing three salamander species representing two phenotypes-the surface-dwelling Barton Springs salamander (E. sosorum) and San Marcos salamander (E. nana) and the obligate subterranean Texas blind salamander (E. rathbuni) - in terms of structure and size of their eyes. Eyes were examined using confocal microscopy and measurements were made using ImageJ. Statistical analysis of data was carried out using R. We also provide a developmental series and track eye development and immunolocalization of Pax6 in E. sosorum and E. rathbuni. Adult histology of the surface-dwelling San Marcos salamander (E. nana) shows similarities to E. sosorum. The eyes of adults of the epigean species E. nana and E. sosorum appear fully developed with all the histological features of a fully functional eye. In contrast, the eyes of E. rathbuni adults have fewer layers, lack lenses and other features associated with vision as has been reported previously. However, in early developmental stages eye morphology did not differ significantly between E. rathbuni and E. sosorum. Parallel development is observed between the two phenotypes in terms of morphology; however, Pax6 labeling seems to decrease in the latter stages of development in E.rathbuni. We test for immunolabeling of the visual pigment proteins opsin and rhodopsin and observe immunolocalization around photoreceptor disks in E. nana and E. sosorum, but not in the subterranean E. rathbuni. Our results from examining developing salamanders suggest a combination of underdevelopment and degeneration contribute to the reduced eyes of adult E. rathbuni.

Project description:The molecular detection of DNA fragments that are shed into the environment (eDNA) has become an increasingly applied tool used to inventory biological communities and to perform targeted species surveys. This method is particularly useful in habitats where it is difficult or not practical to visually detect or trap the target organisms. Central Texas Eurycea salamanders inhabit both surface and subterranean aquatic environments. Subterranean surveys are challenging or infeasible, and the detection of salamander eDNA in water samples is an appealing survey technique for these situations. Here, we develop and validate an eDNA assay using quantitative PCR for E. chisholmensis, E. naufragia, and E. tonkawae. These three species are federally threatened and constitute the Septentriomolge clade that occurs in the northern segment of the Edwards Aquifer. First, we validated the specificity of the assay in silico and with DNA extracted from tissue samples of both target Septentriomolge and non-target amphibians that overlap in distribution. Then, we evaluated the sensitivity of the assay in two controls, one with salamander-positive water and one at field sites known to be occupied by Septentriomolge. For the salamander-positive control, the estimated probability of eDNA occurrence (ψ) was 0.981 (SE = 0.019), and the estimated probability of detecting eDNA in a qPCR replicate (p) was 0.981 (SE = 0.011). For the field control, the estimated probability of eDNA occurring at a site (ψ) was 0.938 (95% CRI: 0.714-0.998). The estimated probability of collecting eDNA in a water sample (θ) was positively correlated with salamander relative density and ranged from 0.371 (95% CRI: 0.201-0.561) to 0.999 (95% CRI: 0.850- > 0.999) among sampled sites. Therefore, sites with low salamander density require more water samples for eDNA evaluation, and we determined that our site with the lowest estimated θ would require seven water samples for the cumulative collection probability to exceed 0.95. The estimated probability of detecting eDNA in a qPCR replicate (p) was 0.882 (95% CRI: 0.807-0.936), and our assay required two qPCR replicates for the cumulative detection probability to exceed 0.95. In complementary visual encounter surveys, the estimated probability of salamanders occurring at a known-occupied site was 0.905 (SE = 0.096), and the estimated probability of detecting salamanders in a visual encounter survey was 0.925 (SE = 0.052). We additionally discuss future research needed to refine this method and understand its limitations before practical application and incorporation into formal survey protocols for these taxa.

Project description:How species will respond to ongoing and future climate change is one of the most important questions facing biodiversity scientists today. The fossil record provides unparalleled insight into past ecological and evolutionary responses to climate change, but the resource remains virtually untapped for many organisms. We use geometric morphometrics and a 25,000 year fossil record to quantify changes in body size and mandible shape through time and across climate regimes for two bat species present in Quaternary paleontological deposits of central Texas: Myotis velifer, a bat distributed throughout the Southwestern US and Mexico that is still found in central Texas today, and Eptesicus fuscus, a bat widely distributed throughout North America that has been extirpated in central Texas. Because of ecogeographic rules like Bergmann's rule, which posits that endotherms are larger in colder environments, we hypothesized that both species were larger during cooler time intervals. Additionally, we hypothesized that both species would show variation in dental morphology across the studied sequence as a response to climate change. While we found a decrease in centroid size-a proxy for --body size-through time for both species, we could not establish a clear relationship between centroid size and temperature alone. However, we did find that specimens from drier environments were significantly larger than those from wetter ones. Furthermore, we found significant dental shape variation between environments reflecting different temperature levels for both species. Yet only M. velifer exhibited significant variation between environments of varying precipitation levels. This result was surprising because present-day populations of E. fuscus are highly variable across both temperature and precipitation gradients. We determined that the morphological change experienced by M. velifer through time, and between warmer and cooler temperatures, was associated with the coronoid process, condylar process, and the mandibular symphysis. These parts play a pivotal role in bite force, so changes in these features might relate to changes in diet. We show that long-term datasets derived from fossil material provide invaluable insight not only into the validity of ecogeographic rules, but also into the adaptive capacities of extant taxa when faced with environmental changes. Our results highlight diverging responses to a variety of climate factors that are relevant to consider in biodiversity research given ongoing global change.

Project description:BackgroundThe taxonomy and systematics of Salix subgenus Salix s.l. is difficult. The reliability and evolutionary implications of two important morphological characters (number of stamens, and morphology of bud scales) used in subgeneric classification within Salix remain untested, and a disjunct Old-New World distribution pattern of a main clade of subgenus Salix s.l., revealed by a previous study, lacks a reasonable explanation. To study these questions, we conducted phylogenetic analyses based on 4,688 bp of sequence data from four plastid (rbcL, trnD-T, matK, and atpB-rbcL) and two nuclear markers (ETS and ITS) covering all subgenera of Salix, and all sections of subgenus Salix s.l.ResultsSubgenus Salix came out as para- or polyphyletic in both nrDNA and plastid trees. The plastid phylogeny successfully resolved relationships among the major clades of Salix, but resolution within subgenus Salix s.l. remained low. Nevertheless, three monophyletic groups were identifiable in subgenus Salix s.l.: the 'main clade' of subgenus Salix s.l., with New and Old World species being reciprocally monophyletic; the section Triandroides clade; and the subgenus Pleuradenia clade. While nrDNA regions showed higher resolution within subgenus Salix s.l., they failed to resolve subgeneric relationships. Extensive, statistically significant gene-tree incongruence was detected across nrDNA-plastid as well as nrDNA ETS-ITS phylogenies, suggesting reticulate evolution or hybridization within the group. The results were supported by network analyses. Ancestral-state reconstructions indicated that multiple stamens and free bud scales represent the plesiomorphic states within Salix, and that several significant shifts in stamen number and bud scale morphology have occurred.ConclusionsSubgenus Salix s.l. is not monophyletic, and the evolutionary history of the subgenus has involved multiple reticulation events that may mainly be due to hybridization. The delimitation of subgenus Salix s.l. should be redefined by excluding section Triandrae and subgenus Pleuradenia from it. The evolutionary lability of bud-scale morphology and stamen number means that these characters are unreliable bases for classification. The disjunct Old-New World distribution of subgenus Salix s.l. appears to be linked to the profound climatic cooling during the Tertiary, which cut off gene exchange between New and Old World lineages.

Project description:BACKGROUND: Hydrocharitaceae is a fully aquatic monocot family, consists of 18 genera with approximately 120 species. The family includes both fresh and marine aquatics and exhibits great diversity in form and habit including annual and perennial life histories; submersed, partially submersed and floating leaf habits and linear to orbicular leaf shapes. The family has a cosmopolitan distribution and is well represented in the Tertiary fossil record in Europe. At present, the historical biogeography of the family is not well understood and the generic relationships remain controversial. In this study we investigated the phylogeny and biogeography of Hydrocharitaceae by integrating fossils and DNA sequences from eight genes. We also conducted ancestral state reconstruction for three morphological characters. RESULTS: Phylogenetic analyses produced a phylogeny with most branches strongly supported by bootstrap values greater than 95 and Bayesian posterior probability values of 1.0. Stratiotes is the first diverging lineage with the remaining genera in two clades, one clade consists of Lagarosiphon, Ottelia, Blyxa, Apalanthe, Elodea and Egeria; and the other consists of Hydrocharis-Limnobium, Thalassia, Enhalus, Halophila, Najas, Hydrilla, Vallisneria, Nechamandra and Maidenia. Biogeographic analyses (DIVA, Mesquite) and divergence time estimates (BEAST) resolved the most recent common ancestor of Hydrocharitaceae as being in Asia during the Late Cretaceous and Palaeocene (54.7-72.6 Ma). Dispersals (including long-distance dispersal and migrations through Tethys seaway and land bridges) probably played major roles in the intercontinental distribution of this family. Ancestral state reconstruction suggested that in Hydrocharitaceae evolution of dioecy is bidirectional, viz., from dioecy to hermaphroditism, and from hermaphroditism to dioecy, and that the aerial-submerged leaf habit and short-linear leaf shape are the ancestral states. CONCLUSIONS: Our study has shed light on the previously controversial generic phylogeny of Hydrocharitaceae. The study has resolved the historical biogeography of this family and supported dispersal as the most likely explanation for the intercontinental distribution. We have also provided valuable information for understanding the evolution of breeding system and leaf phenotype in aquatic monocots.

Dataset Information

Biogeography, phylogeny, and morphological evolution of central Texas cave and spring salamanders.

Publications

Biogeography, phylogeny, and morphological evolution of central Texas cave and spring salamanders.

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