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Population genetics and the effects of a severe bottleneck in an ex situ population of critically endangered Hawaiian tree snails.

ABSTRACT: As wild populations decline, ex situ propagation provides a potential bank of genetic diversity and a hedge against extinction. These programs are unlikely to succeed if captive populations do not recover from the severe bottleneck imposed when they are founded with a limited number of individuals from remnant populations. In small captive populations allelic richness may be lost due to genetic drift, leading to a decline in fitness. Wild populations of the Hawaiian tree snail Achatinella lila, a hermaphroditic snail with a long life history, have declined precipitously due to introduced predators and other human impacts. A captive population initially thrived after its founding with seven snails, exceeding 600 captive individuals in 2009, but drastically declined in the last five years. Measures of fitness were examined from 2,018 captive snails that died between 1998 and 2012, and compared with genotypic data for six microsatellite loci from a subset of these deceased snails (N?=?335), as well as live captive snails (N?=?198) and wild snails (N?=?92). Surprisingly, the inbreeding coefficient (Fis) declined over time in the captive population, and is now approaching values observed in the 2013 wild population, despite a significant decrease in allelic richness. However, adult annual survival and fecundity significantly declined in the second generation. These measures of fitness were positively correlated with heterozygosity. Snails with higher measures of heterozygosity had more offspring, and third generation offspring with higher measures of heterozygosity were more likely to reach maturity. These results highlight the importance of maintaining genetic diversity in captive populations, particularly those initiated with a small number of individuals from wild remnant populations. Genetic rescue may allow for an increase in genetic diversity in the captive population, as measures of heterozygosity and rarified allelic richness were higher in wild tree snails.

SUBMITTER: Price MR

PROVIDER: S-EPMC4255004 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Population genetics and the effects of a severe bottleneck in an ex situ population of critically endangered Hawaiian tree snails.

Price Melissa R MR Hadfield Michael G MG

PloS one 20141203 12

As wild populations decline, ex situ propagation provides a potential bank of genetic diversity and a hedge against extinction. These programs are unlikely to succeed if captive populations do not recover from the severe bottleneck imposed when they are founded with a limited number of individuals from remnant populations. In small captive populations allelic richness may be lost due to genetic drift, leading to a decline in fitness. Wild populations of the Hawaiian tree snail Achatinella lila, ...[more]

PMID: 25470182

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Project description:Wild populations of endangered Hawaiian tree snails have declined precipitously over the last century due to introduced predators and other human impacts. Life history traits, such as very low fecundity (<5 offspring per year across taxa) and maturity at approximately four years of age have made recovery difficult. Conservation efforts such as in situ predator-free enclosures may increase survival to maturity by protecting offspring from predation, but no long-term data existed prior to this study demonstrating the demographic and genetic parameters necessary to maintain populations within those enclosures. We evaluated over 20 years of evidence for the dynamics of survival and extinction in captive ex situ populations of Hawaiian tree snails established from wild-collected individuals. From 1991 to 2006, small numbers of snails (<15) from fifteen species were collected from the wild to initiate captive-reared populations as a hedge against extinction. This small number of founders resulted in a severe bottleneck in each of the captive-reared populations. We identified key demographic parameters that predicted population recovery from this bottleneck. Species with captive populations that produced between two and four offspring per adult per year and had 20-50% of those offspring survive to maturity recovered to numbers above 100 individuals, and maintained viable populations following a decline that occurred between 2009 and 2014. Those populations that had less than two offspring per adult per year and less than 20% survival to maturity did not reach 100 individuals in captivity, and many of these populations died out during the recent decline. We suggest that small reductions in fitness may contribute to extirpation in taxa with inherently low fecundity, by keeping populations below a threshold number essential to long-term recovery. Future ex situ populations should be founded with no less than 15 adults, and maintained in conditions closely approximating the temperature and humidity of source locations to optimize fitness. Permanent translocations of wild populations for conservation purposes will be more likely to succeed with greater than 100 adults, and should be limited to locations with a similar climate to source locations.

Project description:Phylogenomic studies can provide insights into speciation, adaptation, and extinction, while providing a roadmap for conservation. Hawaiian tree snails are a model system for an adaptive radiation facing an extinction crisis. In the last 5 years, nearly all populations of Hawaiian tree snails across the 30 remaining species in the subfamily Achatinellinae (Achatinellidae) have declined from hundreds or thousands in the wild down to undetectable levels. Nearly 100 species historically occurred across dramatic environmental gradients on five of the Hawaiian Islands, but habitat loss, overcollection, and predation by invasive species have decimated populations. As such, this system offers the opportunity to integrate efforts to conserve evolutionary potential into conservation planning for a rapidly declining subfamily. Here, we used genome-wide, restriction-site associated DNA sequencing (RADseq), along with mitochondrial genome reconstruction, to resolve evolutionary relationships to inform conservation efforts. Phylogenetic analysis of nearly 400k genome-wide SNPs from 59 populations and 25 species across six genera in the family Achatinellidae, was generally concordant with taxonomy, geography, and mtDNA with several notable exceptions; mtDNA was unable to resolve some deeper nodes (e.g., the monophyly of Achatinella), while SNP data did not resolve as many shallow nodes. Both phylogenetic and coalescent analysis revealed deep divergences between populations within Achatinella mustelina that were consistent with species-level differences. Given cryptic species-level divergence within populations that are geographically proximate, they are at higher risk of extirpation from invasive predators and climate change than previously assumed. This study clarifies evolutionary relationships within this model system for adaptive radiation, forming the basis for conservation strategies such as translocation, captive rearing, and hybridization trials to prevent the loss of capacity to adapt to rapidly changing environmental conditions.

Project description:The native terrestrial snail fauna of the Hawaiian Islands faces numerous threats that have led to severe range reductions, population declines, and extinction of species. With the continued declines of many wild populations, a crucial component of preserving Hawaiian terrestrial snail biodiversity is through captive rearing programs, like that implemented by the Hawai'i Department of Land and Natural Resources Snail Extinction Prevention Program. Rare and endangered tree snails in the family Achatinellidae, which feed on epiphytic microbial communities, are maintained in captivity with a diet that includes native vegetation brought in from nearby forests, as well as a cultured fungus originally isolated from native host trees. Recent mortality events in lab populations have been attributed to wild-gathered vegetation. These events have increased interest in developing a completely manufactured or cultured diet that would eliminate the need for exposure to wild-gathered plants. This study compared survival and egg production in Auriculella diaphana provided with lab-cultured fungus, and those provided with wild vegetation. We compared the number of eggs laid and number of deaths among three treatments: (1) wild collected vegetation only; (2) wild vegetation supplemented with laboratory-cultured fungus; and (3) laboratory cultured fungus only. Mortality did not significantly differ among treatments, but the number of eggs laid was significantly higher in snails provided wild vegetation and cultured fungus (F = 24.998; P < 0.001), compared with those provided with only wild vegetation (t = 1.88, P = 0.032) or only cultured fungus (t = 4.530, P = 0.004). Our results suggest: (1) the existing strain of cultured fungus alone is not sufficient to maintain captive-reared snail populations; (2) the additional energy or calcium provided by the cultured fungus appears to enhance egg reproduction in captive-reared populations; (3) the presence or absence of live vegetation influences snail behavior, including aestivation and egg laying. These results highlight the importance of ongoing research to culture additional species of fungi at a rate that could support captive-reared populations, as the diversity of fungi present in wild epiphytic microbial communities may be important for snail reproductive health.

Project description:Ex situ conservation in germplasm and living collections is a major focus of global plant conservation strategies. Prioritizing species for ex situ collection is a necessary component of this effort for which sound strategies are needed. Phylogenetic considerations can play an important role in prioritization. Collections that are more phylogenetically diverse are likely to encompass more ecological and trait variation, and thus provide stronger conservation insurance and richer resources for future restoration efforts. However, phylogenetic criteria need to be weighed against other, potentially competing objectives. We used ex situ collection and threat rank data for North American angiosperms to investigate gaps in ex situ coverage and phylogenetic diversity of collections and to develop a flexible framework for prioritizing species across multiple objectives. We found that ex situ coverage of 18,766 North American angiosperm taxa was low with respect to the most vulnerable taxa: just 43% of vulnerable to critically imperiled taxa were in ex situ collections, far short of a year-2020 goal of 75%. In addition, species held in ex situ collections were phylogenetically clustered (P < 0.001), i.e., collections comprised less phylogenetic diversity than would be expected had species been drawn at random. These patterns support incorporating phylogenetic considerations into ex situ prioritization in a manner balanced with other criteria, such as vulnerability. To meet this need, we present the 'PIECES' index (Phylogenetically Informed Ex situ Conservation of Endangered Species). PIECES integrates phylogenetic considerations into a flexible framework for prioritizing species across competing objectives using multi-criteria decision analysis. Applying PIECES to prioritizing ex situ conservation of North American angiosperms, we show strong return on investment across multiple objectives, some of which are negatively correlated with each other. A spreadsheet-based decision support tool for North American angiosperms is provided; this tool can be customized to align with different conservation objectives.

Dataset Information

Population genetics and the effects of a severe bottleneck in an ex situ population of critically endangered Hawaiian tree snails.

Publications

Population genetics and the effects of a severe bottleneck in an ex situ population of critically endangered Hawaiian tree snails.

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