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      Patterns of Cave Biodiversity and Endemism in the Appalachians and Interior Plateau of Tennessee, USA

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          Abstract

          Using species distribution data, we developed a georeferenced database of troglobionts (cave-obligate species) in Tennessee to examine spatial patterns of species richness and endemism, including >2000 records for 200 described species. Forty aquatic troglobionts (stygobionts) and 160 terrestrial troglobionts are known from caves in Tennessee, the latter having the greatest diversity of any state in the United States. Endemism was high, with 25% of terrestrial troglobionts (40 species) and 20% of stygobionts (eight species) known from just a single cave and nearly two-thirds of all troglobionts (130 species) known from five or fewer caves. Species richness and endemism were greatest in the Interior Plateau (IP) and Southwestern Appalachians (SWA) ecoregions, which were twice as diverse as the Ridge and Valley (RV). Troglobiont species assemblages were most similar between the IP and SWA, which shared 59 species, whereas the RV cave fauna was largely distinct. We identified a hotspot of cave biodiversity with a center along the escarpment of the Cumberland Plateau in south-central Tennessee defined by both species richness and endemism that is contiguous with a previously defined hotspot in northeastern Alabama. Nearly half (91 species) of Tennessee’s troglobiont diversity occurs in this region where several cave systems contain ten or more troglobionts, including one with 23 species. In addition, we identified distinct troglobiont communities across the state. These communities corresponded to hydrological boundaries and likely reflect past or current connectivity between subterranean habitats within and barriers between hydrological basins. Although diverse, Tennessee’s subterranean fauna remains poorly studied and many additional species await discovery and description. We identified several undersampled regions and outlined conservation and management priorities to improve our knowledge and aid in protection of the subterranean biodiversity in Tennessee.

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          Most cited references6

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          Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies.

          Cave organisms occupy a special place in evolutionary biology because convergent morphologies of many species demonstrate repeatability in evolution even as they obscure phylogenetic relationships. The origin of specialized cave-dwelling species also raises the issue of the relative importance of isolation vs. natural selection in speciation. Two alternative hypotheses describe the origin of subterranean species. The 'climate-relict' model proposes allopatric speciation after populations of cold-adapted species become stranded in caves due to climate change. The 'adaptive-shift' model proposes parapatric speciation driven by divergent selection between subterranean and surface habitats. Our study of the Tennessee cave salamander complex shows that the three nominal forms (Gyrinophilus palleucus palleucus, G. p. necturoides, and G. gulolineatus) arose recently and are genealogically nested within the epigean (surface-dwelling) species, G. porphyriticus. Short branch lengths and discordant gene trees were consistent with a complex history involving gene flow between diverging forms. Results of coalescent-based analysis of the distribution of haplotypes among groups reject the allopatric speciation model and support continuous or recurrent genetic exchange during divergence. These results strongly favour the hypothesis that Tennessee cave salamanders originated from spring salamanders via divergence with gene flow.
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            Delimiting species using multilocus data: diagnosing cryptic diversity in the southern cavefish, Typhlichthys subterraneus (Teleostei: Amblyopsidae).

            A major challenge facing biodiversity conservation and management is that a significant portion of species diversity remains undiscovered or undescribed. This is particularly evident in subterranean animals in which species delimitation based on morphology is difficult because differentiation is often obscured by phenotypic convergence. Multilocus genetic data constitute a valuable source of information for species delimitation in such organisms, but until recently, few methods were available to objectively test species delimitation hypotheses using genetic data. Here, we use recently developed methods for discovering and testing species boundaries and relationships using a multilocus dataset in a widely distributed subterranean teleost fish, Typhlichthys subterraneus, endemic to Eastern North America. We provide evidence that species diversity in T. subterraneus is currently underestimated and that the picture of a single, widely distributed species is not supported. Rather, several morphologically cryptic lineages comprise the diversity in this clade, including support for the recognition of T. eigenmanni. The high number of cryptic species in Typhlichthys highlights the utility of multilocus genetic data in delimiting species, particularly in lineages that exhibit slight morphological disparity, such as subterranean organisms. However, results depend on sampling of individuals and loci; this issue needs further study. © 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.
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              Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape.

              The landscape of the Pilbara region of Western Australia has been relatively unchanged for 100 million years. The ancient river systems of this region might be expected to be sources of isolation and divergence for aquatic species. Hence, the occurrence of widespread groundwater taxa in this landscape offers the opportunity to examine associations between genetic diversity and drainage patterns. Pilbarus and Chydaekata are two widespread genera of subterranean amphipods endemic to the Pilbara, each occupying multiple tributaries. We used molecular data to examine the roles of drainage patterns in structuring genetic diversity. Gene flow within a tributary may be facilitated by the occasional occurrence of these amphipods in springs, which results in their downstream dispersal during episodic flooding. However, tributary boundaries may form hydrological barriers to gene flow, resulting in localised isolation of populations and divergence. Samples of both genera, collected throughout three river basins, were examined for sequence divergence in the cytochrome c oxidase I mitochondrial gene. There was no evidence of contemporary gene flow among populations of either genus, and each tributary contained highly divergent lineages, which were not associated with similar morphological differentiation. This suggests cryptic speciation has occurred, and similar phylogenetic signals in both taxa imply similar evolutionary histories. Surface populations may have been driven into subterranean refugia by the cessation of flow in the rivers, associated with Tertiary climate change, while morphological evolution may have been constrained by stabilising selection. The lack of congruence between molecular diversity and morphology raises important practical issues for conservation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                22 May 2013
                : 8
                : 5
                : e64177
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United States of America
                [2 ]Department of Biology, University of the South, Sewanee, Tennessee, United States of America
                Ecole Normale Supérieure de Lyon, France
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MLN KSZ. Performed the experiments: MLN KSZ. Analyzed the data: MLN KSZ. Contributed reagents/materials/analysis tools: MLN KSZ. Wrote the paper: MLZ KSZ.

                Article
                PONE-D-12-38765
                10.1371/journal.pone.0064177
                3661478
                23717562
                da5cfa8a-0a4e-49d7-a447-e981852cd8f4
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 December 2012
                : 13 April 2013
                Page count
                Pages: 17
                Funding
                This work was supported by the Tennessee Wildlife Resources Agency (contract nos. ED-06-02149-99 and ED-08-023417-00 to MLN), American Museum of Natural History (MLN), Cave Research Foundation (MLN), National Speleological Society (MLN), the Yale Institute for Biospheric Studies (MLN), and the University of the South (KSZ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Community Assembly
                Community Structure
                Biogeography
                Conservation Science
                Freshwater Ecology
                Spatial and Landscape Ecology
                Zoology
                Entomology
                Helminthology
                Herpetology
                Ichthyology
                Malacology

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                Uncategorized

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