Taehwan Lee

Placing the Floridian marine genetic disjunction into a regional evolutionary context using the scorched mussel, Brachidontes exustus, species complex

Abstract The well‐documented Floridian Gulf/Atlantic marine genetic disjunction provides an influential example of presumed vicariant cladogenesis along a continental coastline for major elements of a diverse nearshore fauna. However, it is unclear if this disjunction represents a local anomaly for regionally distributed morphospecies, or if it is merely one of many such cryptic phylogenetic splits that underlay their assumed genetic cohesiveness. We aimed to place the previously characterized scorched mussel Gulf/Atlantic genetic disjunction into a regional phylogenetic perspective by incorporating genotypes of nominal conspecifics sampled throughout the Caribbean Basin as well as those of eastern Pacific potential geminate species. Our results show it to be one of multiple latent regional genetic disjunctions, involving five cryptic Caribbean species, that appear to be the product of a long history of regional cladogenesis. Disjunctions involving three stem lineages clearly predate formation of the Isthmus of Panama and of the Caribbean Sea, although four of the five cryptic species have within‐basin sister relationships. Surprisingly, the Atlantic clade was also found to be widespread in the southern Caribbean, and ancestral demography calculations through time for Atlantic coast‐specific genotypes are consistent with a northward range extension after the last glacial maximum. Our new data seriously undermine the hypothesis of a Floridian vicariant genesis and imply that the scorched mussel Gulf/Atlantic disjunction represents a case of geographic and temporal pseudocongruence. All five Caribbean Basin cryptic species exhibited an intriguing pattern of predominantly allopatric distribution characterized by distinct geographic areas of ecological dominance, often adjoining those of sister taxa. This pattern of distribution is consistent with allopatric speciation origins, coupled with restricted postspeciation range extensions. Several lines of indirect evidence favor the hypothesis that the predominantly allopatric distributions are maintained over evolutionary time scales, primarily by postrecruitment ecological filters rather than by oceanographic barriers to larvalmediated gene flow.

Geographic Variation in Venom Allelic Composition and Diets of the Widespread Predatory Marine Gastropod Conus ebraeus

Background Members of the predatory gastropod genus Conus use a venom comprised of a cocktail of peptide neurotoxins, termed conotoxins or conopeptides, to paralyze prey and conotoxin gene family members diversify via strong positive selection. Because Conus venoms are used primarily to subdue prey, the evolution of venoms is likely affected by predator-prey interactions. Methodology/Principal Findings To identify the selective forces that drive the differentiation of venoms within species of Conus, we examined the distribution of alleles of a polymorphic O-superfamily conotoxin locus of Conus ebraeus at Okinawa, Guam and Hawaii. Previous analyses of mitochondrial cytochrome oxidase I gene sequences suggest that populations of C. ebraeus, a worm-eating Conus, are not structured genetically in the western and central Pacific. Nonetheless, because the sample size from Guam was relatively low, we obtained additional data from this location and reexamined patterns of genetic variation at the mitochondrial gene at Okinawa, Guam and Hawaii. We also utilized a DNA-based approach to identify prey items of individuals of C. ebraeus from Guam and compared this information to published data on diets at Okinawa and Hawaii. Our results show that conotoxin allelic frequencies differ significantly among all three locations, with strongest differentiation at Hawaii. We also confirm previous inferences that C. ebraeus exhibits no genetic differentiation between Okinawa, Guam and Hawaii at the mitochondrial locus. Finally, DNA-based analyses show that eunicid polychaetes comprise the majority of the prey items of C. ebraeus at Guam; while this results compares well with observed diet of this species at Okinawa, C. ebraeus preys predominantly on nereid polychaetes at Hawaii. Conclusions/Significance These results imply that strong selection pressures affect conotoxin allelic frequencies. Based on the dietary information, the selection may derive from geographic variation in dietary specialization and local coevolutionary arms races between Conus and their prey.

Ecological Release and Venom Evolution of a Predatory Marine Snail at Easter Island

Background Ecological release is coupled with adaptive radiation and ecological diversification yet little is known about the molecular basis of phenotypic changes associated with this phenomenon. The venomous, predatory marine gastropod Conus miliaris has undergone ecological release and exhibits increased dietary breadth at Easter Island. Methodology/Principal Findings We examined the extent of genetic differentiation of two genes expressed in the venom of C. miliaris among samples from Easter Island, American Samoa and Guam. The population from Easter Island exhibits unique frequencies of alleles that encode distinct peptides at both loci. Levels of divergence at these loci exceed observed levels of divergence observed at a mitochondrial gene region at Easter Island. Conclusions/Significance Patterns of genetic variation at two genes expressed in the venom of this C. miliaris suggest that selection has operated at these genes and contributed to the divergence of venom composition at Easter Island. These results show that ecological release is associated with strong selection pressures that promote the evolution of new phenotypes.

Prehistoric inter-archipelago trading of Polynesian tree snails leaves a conservation legacy

Inter-archipelago exchange networks were an important aspect of prehistoric Polynesian societies. We report here a novel genetic characterization of a prehistoric exchange network involving an endemic Pacific island tree snail, Partula hyalina. It occurs in the Society (Tahiti only), Austral and Southern Cook Islands. Our genetic data, based on museum, captive and wild-caught samples, establish Tahiti as the source island. The source lineage is polymorphic in shell coloration and contains a second nominal species, the dark-shelled Partula clara, in addition to the white-shelled P. hyalina. Prehistoric inter-island introductions were non-random: they involved white-shelled snails only and were exclusively inter-archipelago in scope. Partulid shells were commonly used in regional Polynesian jewellery, and we propose that the white-shelled P. hyalina, originally restricted to Tahiti, had aesthetic value throughout these archipelagoes. Demand within the Society Islands could be best met by trading dead shells, but a low rate of inter-archipelago exchange may have prompted the establishment of multiple founder populations in the Australs and Southern Cooks. The alien carnivorous land snail Euglandina rosea has recently devastated populations of all 61 endemic species of Society Island partulid snails. Southern Cooks and Australs P. hyalina now represent the only unscathed wild populations remaining of this once spectacular land snail radiation.

Moorean tree snail survival revisited: a multi-island genealogical perspective.

BackgroundThe mass extirpation of the island of Mooreas endemic partulid tree snail fauna, following the deliberate introduction of the alien predator Euglandina rosea, represents one of the highest profile conservation crises of the past thirty years. All of the islands partulids were thought to be extirpated by 1987, with five species persisting in zoos, but intensive field surveys have recently detected a number of surviving wild populations. We report here a mitochondrial (mt) phylogenetic estimate of Moorean partulid wild and captive lineage survival calibrated with a reference museum collection that pre-dates the predators introduction and that also includes a parallel dataset from the neighboring island of Tahiti.ResultsAlthough severe winnowing of Mooreas mt lineage diversity has occurred, seven of eight (six Partula; two Samoana) partulid tip clades remain extant. The extinct mt clade occurred predominantly in the P. suturalis species complex and it represented a major component of Mooreas endemic partulid treespace. Extant Moorean mt clades exhibited a complex spectrum of persistence on Moorea, in captivity, and (in the form of five phylogenetically distinct sister lineages) on Tahiti. Most notably, three Partula taxa, bearing two multi-island mt lineages, have survived decades of E. rosea predation on Moorea (P. taeniata) and in the valleys of Tahiti (P. hyalina and P. clara). Their differential persistence was correlated with intrinsic attributes, such as taxonomy and mt lineages, rather than with their respective within-island distribution patterns.ConclusionConservation efforts directed toward Moorean and Tahitian partulids have typically operated within a single island frame of reference, but our discovery of robust genealogical ties among survivors on both islands implies that a multi-island perspective is required. Understanding what genetic and/or ecological factors have enabled Partula taeniata, P. hyalina and P. clara to differentially survive long-term direct exposure to the predator may provide important clues toward developing a viable long term conservation plan for Society Island partulid tree snails.

Tahitian tree snail mitochondrial clades survived recent mass extirpation.

Oceanic islands frequently support endemic faunal radiations that are highly vulnerable to introduced predators [1]. This vulnerability is epitomized by the rapid extinction in the wild of all but five of 61 described Society Islands partulid tree snails [2], following the deliberate introduction of an alien biological control agent: the carnivorous snail Euglandina rosea[3]. Tahitis tree snail populations have been almost completely extirpated and three of the islands eight endemic Partula species are officially extinct, a fourth persisting only in captivity [2]. We report a molecular phylogenetic estimate of Tahitian Partula mitochondrial lineage survival calibrated with a 1970 reference museum collection that pre-dates the predators 1974 introduction to the island [4]. Although severe winnowing of lineage diversity has occurred, none of the five primary Tahitian Partula clades present in the museum samples is extinct. Targeted conservation measures, especially of montane refuge populations, may yet preserve a representative sub-sample of Tahitis endemic tree snail genetic diversity in the wild.

6-Phosphogluconate dehydrogenase (PGD) allele phylogeny is incongruent with a recent origin of polyploidization in some North American Sphaeriidae (Mollusca, Bivalvia)

Although polyploidization is rare among bivalve mollusks, recent cytogenetic studies have revealed a remarkable degree of genome amplification (up to 13n) in the freshwater bivalve family Sphaeriidae. We generated single-copy nuclear gene trees in order to test hypotheses addressing the evolutionary origins of sphaeriid genome duplication. Polyploid North American members of three cosmopolitan sphaeriid genera (Sphaerium, Musculium, and Pisidium) were characterized for their expressed allelic repertoire of a 526 nt c-DNA fragment of 6-phosphogluconate dehydrogenase (PGD). Pronounced levels of intra-individual genetic variation were uncovered in most of the polyploid taxa and a minority of alleles showed strong evidence of recombination. Phylogenetic analyses resolved polyploid sphaeriid PGD alleles into two clades (A, B), each of which contained a subsample of intra-individual allelic diversity of the genus Sphaerium. These two clades were also recovered in Musculium, however one (B) is represented here by a single recombinant allele. With the exception of a divergent segment in one putatively recombinant allele, the expressed PGD repertoire of the three Pisidium species investigated was restricted to one of the two clades (A). Major within-clade PGD gene tree branching patterns were congruent with mitochondrial gene tree topologies for these taxa. These results are inconsistent with a pattern of recent independent attainment of a polyploid status by our Sphaerium/Musculium study taxa and indicate that they may share a common genome duplication event predating the Miocene appearance of these two genera in the fossil record.

Discovery of the Indo-Pacific oyster Hyotissa hyotis (Linnaeus, 1758) in the Florida Keys (Bivalvia : Gryphaeidae)

Recent collections from a shipwreck in ~30 m depth off the Florida Keys recovered an exceptionally large gryphaeid oyster that was identified on morphological grounds as Hyotissa hyotis (Linnaeus, 1758), a common constituent of Indian and Pacific Ocean near-shore faunas. This identification was confirmed by molecular characterisation: the Florida specimen had an almost identical large mitochondrial ribosomal subunit (16S) genotype to that obtained from a western Pacific (Guam) conspecific, differing in only two nucleotide positions that were heteroplasmic in the Guam specimen. Although this species has been variously cited to occur in the western Atlantic, careful examination of these records revealed them to be misidentifications of Hyotissa mcgintyi (Harry, 1985), originally described from south-eastern Florida. Because H. hyotis is much larger than any other regional oyster, it is unlikely to have been overlooked in earlier biotic surveys. It is therefore likely that this specimen, and another recently discovered off West Palm Beach, Florida, stem from a recent undocumented introduction to the western Atlantic.

Not completely lost: two partulid tree snail species persist on the highest peak of Raiatea, French Polynesia

The spectacular partulid tree snail fauna of the Society Islands has been almost completely extirpated in recent decades following the deliberate introduction of the alien carnivorous snail Euglandina rosea . The greatest loss has occurred on the island of Raiatea, French Polynesia, home to an estimated 34 species (including 33 single-island endemics), all of which have been deemed extirpated in the wild. However, we report here the February 2006 discovery of two surviving Raiatean partulid lineages on the upper slopes of Mount Tefatua, the highest peak on the island. They have been identified using morphological and molecular phylogenetic analyses, the latter approach employing available museum and captive reference samples. One population, at 750 m elevation, consisted of Samoana attenuata . It has a multi-island distribution within the archipelago and surviving populations persist also on Tahiti and Moorea. A second population, present just below the summit at 950 m, consisted of a previously unstudied morphospecies and it has been formally described as Partula meyeri . It is unclear if a stable altitudinal refuge from E. rosea predation exists on Mount Tefatua but the unexpected discovery of these two surviving montane populations raises the possibility of preserving some fraction of Raiateas endemic tree snail diversity in the wild.

Conservation Genetics of a Critically Endangered Limpet Genus and Rediscovery of an Extinct Species

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 20th 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.