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Conservation genetics of a critically endangered limpet genus and rediscovery of an extinct species.

Ó Foighil D, Li J, Lee T, Johnson P, Evans R, Burch JB - PLoS ONE (2011)

Bottom Line: It persists in a Coosa River tributary and morphometric and phylogenetic analyses confirm its taxonomic validity.All three surviving populations of the genus Rhodacmea merit specific status.We recommend the establishment of a proactive targeted conservation program that may include their captive propagation and reintroduction.

View Article: PubMed Central - PubMed

Affiliation: Museum of Zoology and Department of Ecology and Evolutionary Biology, The University of Michigan, Ann Arbor, Michigan, United States of America. diarmaid@umich.edu

ABSTRACT

Background: A third of all known freshwater mollusk extinctions worldwide have occurred within a single medium-sized American drainage. The Mobile River Basin (MRB) of Alabama, a global hotspot of temperate freshwater biodiversity, was intensively industrialized during the 20(th) century, driving 47 of its 139 endemic mollusk species to extinction. These include the ancylinid limpet Rhodacmea filosa, currently classified as extinct (IUCN Red List), a member of a critically endangered southeastern North American genus reduced to a single known extant population (of R. elatior) in the MRB.

Methodology/principal findings: We document here the tripling of known extant populations of this North American limpet genus with the rediscovery of enduring Rhodacmea filosa in a MRB tributary and of R. elatior in its type locality: the Green River, Kentucky, an Ohio River Basin (ORB) tributary. Rhodacmea species are diagnosed using untested conchological traits and we reassessed their systematic and conservation status across both basins using morphometric and genetic characters. Our data corroborated the taxonomic validity of Rhodacmea filosa and we inferred a within-MRB cladogenic origin from a common ancestor bearing the R. elatior shell phenotype. The geographically-isolated MRB and ORB R. elatior populations formed a cryptic species complex: although overlapping morphometrically, they exhibited a pronounced phylogenetic disjunction that greatly exceeded that of within-MRB R. elatior and R. filosa sister species.

Conclusions/significance: Rhodacmea filosa, the type species of the genus, is not extinct. It persists in a Coosa River tributary and morphometric and phylogenetic analyses confirm its taxonomic validity. All three surviving populations of the genus Rhodacmea merit specific status. They collectively contain all known survivors of a phylogenetically highly distinctive North American endemic genus and therefore represent a concentrated fraction of continental freshwater gastropod biodiversity. We recommend the establishment of a proactive targeted conservation program that may include their captive propagation and reintroduction.

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Molecular phylogenetic analyses of Rhodacmea populations.Results for two genetic markers are shown: a bayesian consensus phylogram derived from the mitochondrial cytochrome oxidase I (mt COI) dataset and the single most parsimonious tree found for the nuclear second internal transcribed ribosomal spacer (ITS-2) dataset. For the former, available New World Laevapecini haplotypes were employed as outgroups [24]. For the latter, the Old World Ancylus fluviatilis was the outgroup [24]. Nodal support levels >50 are shown above the respective branches: MP bootstrap/ML bootstrap/Bayesian posterior probabilities for COI tree and MP bootstrap for ITS-2 tree. GenBank accession numbers are given for non-novel genotypes.
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pone-0020496-g004: Molecular phylogenetic analyses of Rhodacmea populations.Results for two genetic markers are shown: a bayesian consensus phylogram derived from the mitochondrial cytochrome oxidase I (mt COI) dataset and the single most parsimonious tree found for the nuclear second internal transcribed ribosomal spacer (ITS-2) dataset. For the former, available New World Laevapecini haplotypes were employed as outgroups [24]. For the latter, the Old World Ancylus fluviatilis was the outgroup [24]. Nodal support levels >50 are shown above the respective branches: MP bootstrap/ML bootstrap/Bayesian posterior probabilities for COI tree and MP bootstrap for ITS-2 tree. GenBank accession numbers are given for non-novel genotypes.

Mentions: Limpets from all three study populations were genotyped for three gene fragments. One of these, a relatively conserved large nuclear ribosomal (28S rDNA) gene, was monomorphic across all three populations. They exhibited the same 28S genotype published previously for Cahaba R. elatior [24] that placed sister to the European ancylid Ancylus fluviatilis in global ancylinid 28S gene trees [24], [34]. The other two gene fragments exhibited population-level genetic differences and the results of their phylogenetic analyses are presented in Fig. 4. For the mitochondrial marker (COI), the availability of an extensive ancylinid GenBank database allowed us to place the Rhodacmea lineages within the Holartic Ancylinae, using the New World Laevapecini as outgroups [24]. Our mt COI topologies corrorborated the phylogenetic distinctiveness of the genus Rhodacmea within North America [24], [34], showing it to be sister to the western Palaeartic genus Ancylus, rather than to the other North American ancylinid genera (Ferrissia, Laevapex and Hebetancylus).


Conservation genetics of a critically endangered limpet genus and rediscovery of an extinct species.

Ó Foighil D, Li J, Lee T, Johnson P, Evans R, Burch JB - PLoS ONE (2011)

Molecular phylogenetic analyses of Rhodacmea populations.Results for two genetic markers are shown: a bayesian consensus phylogram derived from the mitochondrial cytochrome oxidase I (mt COI) dataset and the single most parsimonious tree found for the nuclear second internal transcribed ribosomal spacer (ITS-2) dataset. For the former, available New World Laevapecini haplotypes were employed as outgroups [24]. For the latter, the Old World Ancylus fluviatilis was the outgroup [24]. Nodal support levels >50 are shown above the respective branches: MP bootstrap/ML bootstrap/Bayesian posterior probabilities for COI tree and MP bootstrap for ITS-2 tree. GenBank accession numbers are given for non-novel genotypes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105076&req=5

pone-0020496-g004: Molecular phylogenetic analyses of Rhodacmea populations.Results for two genetic markers are shown: a bayesian consensus phylogram derived from the mitochondrial cytochrome oxidase I (mt COI) dataset and the single most parsimonious tree found for the nuclear second internal transcribed ribosomal spacer (ITS-2) dataset. For the former, available New World Laevapecini haplotypes were employed as outgroups [24]. For the latter, the Old World Ancylus fluviatilis was the outgroup [24]. Nodal support levels >50 are shown above the respective branches: MP bootstrap/ML bootstrap/Bayesian posterior probabilities for COI tree and MP bootstrap for ITS-2 tree. GenBank accession numbers are given for non-novel genotypes.
Mentions: Limpets from all three study populations were genotyped for three gene fragments. One of these, a relatively conserved large nuclear ribosomal (28S rDNA) gene, was monomorphic across all three populations. They exhibited the same 28S genotype published previously for Cahaba R. elatior [24] that placed sister to the European ancylid Ancylus fluviatilis in global ancylinid 28S gene trees [24], [34]. The other two gene fragments exhibited population-level genetic differences and the results of their phylogenetic analyses are presented in Fig. 4. For the mitochondrial marker (COI), the availability of an extensive ancylinid GenBank database allowed us to place the Rhodacmea lineages within the Holartic Ancylinae, using the New World Laevapecini as outgroups [24]. Our mt COI topologies corrorborated the phylogenetic distinctiveness of the genus Rhodacmea within North America [24], [34], showing it to be sister to the western Palaeartic genus Ancylus, rather than to the other North American ancylinid genera (Ferrissia, Laevapex and Hebetancylus).

Bottom Line: It persists in a Coosa River tributary and morphometric and phylogenetic analyses confirm its taxonomic validity.All three surviving populations of the genus Rhodacmea merit specific status.We recommend the establishment of a proactive targeted conservation program that may include their captive propagation and reintroduction.

View Article: PubMed Central - PubMed

Affiliation: Museum of Zoology and Department of Ecology and Evolutionary Biology, The University of Michigan, Ann Arbor, Michigan, United States of America. diarmaid@umich.edu

ABSTRACT

Background: A third of all known freshwater mollusk extinctions worldwide have occurred within a single medium-sized American drainage. The Mobile River Basin (MRB) of Alabama, a global hotspot of temperate freshwater biodiversity, was intensively industrialized during the 20(th) century, driving 47 of its 139 endemic mollusk species to extinction. These include the ancylinid limpet Rhodacmea filosa, currently classified as extinct (IUCN Red List), a member of a critically endangered southeastern North American genus reduced to a single known extant population (of R. elatior) in the MRB.

Methodology/principal findings: We document here the tripling of known extant populations of this North American limpet genus with the rediscovery of enduring Rhodacmea filosa in a MRB tributary and of R. elatior in its type locality: the Green River, Kentucky, an Ohio River Basin (ORB) tributary. Rhodacmea species are diagnosed using untested conchological traits and we reassessed their systematic and conservation status across both basins using morphometric and genetic characters. Our data corroborated the taxonomic validity of Rhodacmea filosa and we inferred a within-MRB cladogenic origin from a common ancestor bearing the R. elatior shell phenotype. The geographically-isolated MRB and ORB R. elatior populations formed a cryptic species complex: although overlapping morphometrically, they exhibited a pronounced phylogenetic disjunction that greatly exceeded that of within-MRB R. elatior and R. filosa sister species.

Conclusions/significance: Rhodacmea filosa, the type species of the genus, is not extinct. It persists in a Coosa River tributary and morphometric and phylogenetic analyses confirm its taxonomic validity. All three surviving populations of the genus Rhodacmea merit specific status. They collectively contain all known survivors of a phylogenetically highly distinctive North American endemic genus and therefore represent a concentrated fraction of continental freshwater gastropod biodiversity. We recommend the establishment of a proactive targeted conservation program that may include their captive propagation and reintroduction.

Show MeSH
Related in: MedlinePlus