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Comparative development and ocular histology between epigean and subterranean salamanders (Eurycea) from central Texas.

ABSTRACT: 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.

SUBMITTER: Tovar RU

PROVIDER: S-EPMC8325428 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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:BackgroundSubterranean 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.ResultsGenetic 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.ConclusionsThe 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.

Project description:BackgroundEurycea sosorum (Barton Springs salamander) and Eurycea nana (San Macros salamander) are listed as endangered and threatened species, respectively, by the U.S. Fish and Wildlife Service (USFWS) with habitats restricted to small regions near Austin, Texas, USA. The conservation efforts with the Eurycea salamanders at the captive breeding program in San Marcos Aquatic Resources Center (SMARC), a USFWS facility, have seen an unexpected and increased mortality rate over the past few years. The clinical signs of sick or dead salamanders included erythema, tail loss, asymmetric gills or brachial loss, rhabdomyolysis, kyphosis, and behavior changes, suggesting that an infectious disease might be the culprit. This study aimed to identify the cause of the infection, determine the taxonomic position of the pathogen, and investigate the potential reservoirs of the pathogen in the environment.ResultsHistopathological examination indicated microsporidian infection (microsporidiosis) in the sick and dead Eurycea salamanders that was later confirmed by PCR detection. We also determined the near full-length small subunit ribosomal RNA (SSU rRNA) gene from the microsporidian pathogen, which allowed us to determine its phylogenetic position, and to design primers for specific and sensitive detection of the pathogen. Phylogenetic analysis indicated that this pathogen was closely related to the insect parasites Vavraia spp. and the human opportunistic pathogen, Trachipleistophora hominis. This Vavraia-like microsporidium was present in dead salamanders at SMARC archived between 2011 and 2015 (positive rates ranging between 52.0-88.9% by PCR detection), as well as in some aquatic invertebrates at the facility (e.g. snails and small crustaceans).ConclusionsA Vavraia-like microsporidian was at least one of the major pathogens, if not solely, responsible for the sickness and mortality in the SMARC salamanders, and the pathogen had been present in the center for years. Environmental invertebrates likely served as a source and reservoir of the microsporidian pathogen. These observations provide new knowledge and a foundation for future conservation efforts for Eurycea salamanders including molecular surveys, monitoring of the pathogen, and discovery of effective treatments.

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Comparative development and ocular histology between epigean and subterranean salamanders (Eurycea) from central Texas.

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