Robert Hershler

The Global Decline of Nonmarine Mollusks

Abstract Invertebrate species represent more than 99% of animal diversity; however, they receive much less publicity and attract disproportionately minor research effort relative to vertebrates. Nonmarine mollusks (i.e., terrestrial and freshwater) are one of the most diverse and imperiled groups of animals, although not many people other than a few specialists who study the group seem to be aware of their plight. Nonmarine mollusks include a number of phylogenetically disparate lineages and species-rich assemblages that represent two molluscan classes, Bivalvia (clams and mussels) and Gastropoda (snails, slugs, and limpets). In this article we provide an overview of global nonmarine molluscan biodiversity and conservation status, including several case studies documenting the diversity and global decline of nonmarine mollusks. We conclude with a discussion of the roles that mollusks and malacologists should play in conservation, including research, conservation management strategies, and education and outreach.

Mitochondrial DNA sequences reveal extensive cryptic diversity within a western American springsnail

We analysed cytochrome c oxidase subunit I and NADH dehydrogenase subunit I sequence variation among 29 populations of a widely ranging southwestern springsnail (Pyrgulopsis micrococcus) and 18 regional congeners. Cladistic analyses of these sequences depict P. micrococcus as a polyphyletic composite of five well‐supported clades. Sequence divergences among these clades and subclades imply the possible occurrence of as many as seven or eight cryptic species in addition to P. micrococcus. Our finding that P. micrococcus contains multiple, genetically distinct and geographically restricted lineages suggests that diversification within this highly speciose aquatic genus has been structured in large part by the operation of terrestrial barriers to gene flow. However, these sequence data also indicate that recent dispersal among hydrographically separated areas has occurred within one of these lineages, which we attribute to passive transport on migratory waterbirds.

Phylogenetic relationships of North American nymphophiline gastropods based on mitochondrial DNA sequences

Phylogenetic relationships of 36 nymphophiline species representing 10 genera were inferred from mtCOI sequence data and compared to recent morphology‐based classifications of this group. Parsimony and maximum likelihood analyses of the molecular data set suggested monophyly of the North American nymphophilines and a sister or otherwise close relationship between this fauna and a European species assigned to the subfamily. Results also supported a previously hypothesized close relationship between the predominantly freshwater nymphophilines and the brackish‐water genus Hydrobia. Our analyses resolved a North American nymphophiline subclade composed of Floridobia, Nymphophilus, and Pyrgulopsis, and depicted the remaining North American genera (Cincinnatia, Marstonia, Notogillia, Rhapinema, Spilochlamys, Stiobia) as either a monophyletic or paraphyletic group. Two of the large North American genera (Floridobia, Marstonia) were supported as monophyletic groups while monophyly of Pyrgulopsis, a western North American group containing > 100 species, was equivocal. North American nymphophiline phylogeny implies that vicariance of eastern and western North American groups was followed by a secondary invasion of eastern coastal areas from the west. We attribute this to dispersal of salt‐tolerant progenitors along the Gulf of Mexico coast

Genetic variation in the Desert Springsnail (Tryonia porrecta): implications for reproductive mode and dispersal

Allozymes and mitochondrial cytochrome c oxidase subunit I (mtCOI) sequences were analysed to determine whether populations of the western North American gastropod Tryonia porrecta (from California, Nevada, Utah, and northwest Mexico) are strongly differentiated in accordance with traditional interpretation of regional fauna as ancient relicts inhabiting isolated fragments of late Tertiary palaeodrainages. These data were also used to assess whether this species, for which males have not been recorded, is a rare example of a molluscan parthenogen. Both data sets strongly supported monophyly of T. porrecta populations. Five of the nine sampled populations consisted of a single monoallelic allozyme genotype while the others contained two to 10 distinct genotypes. Allozymic data for genetically diverse Utah populations provided evidence of clonal and sexual reproduction. mtCOI haplotypes of T. porrecta formed two subgroups which differed by 1.99–2.60%. The common haplotype was found in seven populations with rare haplotypes observed in single populations. Based on these results and an available mtCOI molecular clock for related hydrobiid snails, T. porrecta is interpreted as a primarily parthenogenetic species that undergoes occasional sexual reproduction and has accumulated substantial diversity following its mid‐Pliocene to mid‐Pleistocene origin. Our results also suggest that the distribution of present‐day populations of these gill‐breathing snails did not result from fragmentation of an ancient, well‐integrated drainage but instead reflects overland colonization of habitats which only recently became available following desiccation of late Quaternary pluvial lakes.

The endemic gastropod fauna of Lake Titicaca: correlation between molecular evolution and hydrographic history

Lake Titicaca, situated in the Altiplano high plateau, is the only ancient lake in South America. This 2- to 3-My-old (where My is million years) water body has had a complex history that included at least five major hydrological phases during the Pleistocene. It is generally assumed that these physical events helped shape the evolutionary history of the lakes biota. Herein, we study an endemic species assemblage in Lake Titicaca, composed of members of the microgastropod genus Heleobia, to determine whether the lake has functioned as a reservoir of relic species or the site of local diversification, to evaluate congruence of the regional paleohydrology and the evolutionary history of this assemblage, and to assess whether the geographic distributions of endemic lineages are hierarchical. Our phylogenetic analyses indicate that the Titicaca/Altiplano Heleobia fauna (together with few extralimital taxa) forms a species flock. A molecular clock analysis suggests that the most recent common ancestor (MRCAs) of the Altiplano taxa evolved 0.53 (0.28–0.80) My ago and the MRCAs of the Altiplano taxa and their extralimital sister group 0.92 (0.46–1.52) My ago. The endemic species of Lake Titicaca are younger than the lake itself, implying primarily intralacustrine speciation. Moreover, the timing of evolutionary branching events and the ages of two precursors of Lake Titicaca, lakes Cabana and Ballivián, is congruent. Although Lake Titicaca appears to have been the principal site of speciation for the regional Heleobia fauna, the contemporary spatial patterns of endemism have been masked by immigration and/or emigration events of local riverine taxa, which we attribute to the unstable hydrographic history of the Altiplano. Thus, a hierarchical distribution of endemism is not evident, but instead there is a single genetic break between two regional clades. We also discuss our findings in relation to studies of other regional biota and suggest that salinity tolerance was the most likely limiting factor in the evolution of Altiplano species flocks.

Systematics of a widely distributed western North American springsnail, Pyrgulopsis micrococcus (Caenogastropoda, Hydrobiidae), with descriptions of three new congeners

Abstract We describe three new species of springsnails (genus Pyrgulopsis) from the Amargosa River basin, California and Nevada (P. licina sp. n., P. perforata sp. n., P. sanchezi sp. n.), each of which was previously considered to be part of P. micrococcus. We also restrict P. micrococcus to its type locality area (Oasis Valley) and redefine a regional congener, P. turbatrix, to include populations from the central Death Valley region and San Bernardino Mountains that had been previously identified as P. micrococcus. The five species treated herein form genetically distinct lineages that differ from each other by 4.2–12.6% for mtCOI and 5.2–13.6% for mtNDI (based on previously published and newly obtained data), and are diagnosable by shell and/or penial characters. The new molecular data presented herein confirm sympatry of P. licina and P. sanchezi in Ash Meadows (consistent with morphological evidence) and delineate an additional lineage of P. micrococcus (in the broad sense) that we do not treat taxonomically owing to the paucity of morphological material. Conservation measures are needed to ensure the long term persistence of populations of P. micrococcus and a genetically differentiated lineage of P. sanchezi which live in disturbed habitats on private lands.

Genetic and morphologic variation of the Pecos assiminea, an endangered mollusk of the Rio Grande region, United States and Mexico (Caenogastropoda: Rissooidea: Assimineidae)

Assiminea pecos is an endangered species of amphibious gastropod that occupies four widely separated portions of the Rio Grande region in the southwestern United States (Pecos River basin) and northeastern Mexico (Cuatro Cienegas basin). Our statistical and discriminant function analyses of shell variation among the disjunct populations of this species indicate that Mexican specimens differ in their morphometry from those of the United States and can be diagnosed by several characters. We also analyzed variation in the mitochondrial genome by sequencing 658 bp of mitochondrial COI from populations of A. pecos, representatives of the other three North American species of Assiminea, and several outgroups. Our results indicated substantial divergence of the Mexican population of A. pecos, which was consistently depicted as a monophyletic unit nested within or sister to the shallowly structured group comprised of American members of this species. Consistent with our findings, we describe the Mexican population as a new species, which is provisionally placed in the large, worldwide genus Assiminea pending further study of the phylogentic relationships of the North American assimineids. Our molecular data suggest that the Rio Grande region assimineids, which are among the few inland members of the otherwise estuarine subfamily Assimineinae, diverged from coastal progenitors in the late Miocene, with subsequent Pleistocene vicariance of Mexican and American species perhaps associated with development of the modern, lower course of the Rio Grande.

Taxonomic revision of the Pyrgulopsis gilae (Caenogastropoda, Hydrobiidae) species complex, with descriptions of two new species from the Gila River basin, New Mexico

Abstract We describe two new species of springsnails (genus Pyrgulopsis) for populations from the middle Fork and upper East Fork of the Gila River Basin (New Mexico) that had been previously identified as P. gilae. We also restrict P. gilae to its originally circumscribed geographic range which consists of a short reach of the East Fork Gila River and a single spring along the Gila River (below the East Fork confluence). These three species form genetically distinct lineages that differ from each other by 3.9–6.3% for mtCOI and 3.7–8.7% for mtNDI (the latter data were newly obtained for this study), and are diagnosable by shell and penial characters. Collectively the three species form a strongly supported clade that is distinguished from other congeners by the unique presence of two glandular strips on the dorsal surface of the penial filament. These findings suggest that the conservation status of P. gilae, which was recently removed from the list of candidates for listing as endangered or threatened by the United States Fish and Wildlife Service, should be revisited and that the two new species may also merit protective measures given their narrow geographic ranges.

PERMANENT GENETIC RESOURCES: Microsatellite markers for the threatened Bliss Rapids snail (Taylorconcha serpenticola) and cross-amplification in its congener, T. insperata.

We developed and tested microsatellite markers to investigate population structure of a threatened North American freshwater gastropod, Taylorconcha serpenticola. Of the 21 primer pairs that were evaluated, 11 were readily optimized and scored, providing amplification of 12 loci that were screened for 820 specimens from 29 populations. The number of alleles across 11 of these polymorphic loci ranged from three to 20 and the observed heterozygosity varied from 0.0061 to 0.7561. All loci yielded suitable amplification products in the second species of Taylorconcha (T. insperata) and three proved to be diagnostic for these congeners, demonstrating that these markers are also useful for species identification studies.

Microsatellite markers for the threatened Bliss Rapids snail (Taylorconcha serpenticola) and cross-amplification in its congener, T. inspirata

We developed and tested microsatellite markers to investigate population structure of a threatened North American freshwater gastropod, Taylorconcha serpenticola. Of the 21 primer pairs that were evaluated, 11 were readily optimized and scored, providing amplification of 12 loci that were screened for 820 specimens from 29 populations. The number of alleles across 11 of these polymorphic loci ranged from three to 20 and the observed heterozygosity varied from 0.0061 to 0.7561. All loci yielded suitable amplification products in the second species of Taylorconcha (T. insperata) and three proved to be diagnostic for these congeners, demonstrating that these markers are also useful for species identification studies.