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Population Genetics and the Effects of a Severe Bottleneck in an Ex Situ Population of Critically Endangered Hawaiian Tree Snails

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Population Genetics and the Effects of a Severe Bottleneck in an Ex Situ Population of Critically Endangered Hawaiian Tree Snails RESEARCH ARTICLE Population Genetics and the Effects of a Severe Bottleneck in an Ex Situ Population of Critically Endangered Hawaiian Tree Snails Melissa R. Price1,2*, Michael G. Hadfield1,2 1. Pacific Biosciences Research Center, University of Hawai‘i at Ma¯noa, Honolulu, Hawai‘i, United States of America, 2. Kewalo Marine Laboratories, Honolulu, Hawai‘i, United States of America *[email protected] 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 OPEN ACCESS are founded with a limited number of individuals from remnant populations. In small Citation: Price MR, Hadfield MG (2014) Population captive populations allelic richness may be lost due to genetic drift, leading to a Genetics and the Effects of a Severe Bottleneck in decline in fitness. Wild populations of the Hawaiian tree snail Achatinella lila,a an Ex Situ Population of Critically Endangered Hawaiian Tree Snails. PLoS ONE 9(12): e114377. hermaphroditic snail with a long life history, have declined precipitously due to doi:10.1371/journal.pone.0114377 introduced predators and other human impacts. A captive population initially thrived Editor: Bi-Song Yue, Sichuan University, China after its founding with seven snails, exceeding 600 captive individuals in 2009, but Received: August 18, 2014 drastically declined in the last five years. Measures of fitness were examined from Accepted: November 6, 2014 2,018 captive snails that died between 1998 and 2012, and compared with Published: December 3, 2014 genotypic data for six microsatellite loci from a subset of these deceased snails Copyright: ß 2014 Price, Hadfield. This is an (N5335), as well as live captive snails (N5198) and wild snails (N592). open-access article distributed under the terms of the Creative Commons Attribution License, which Surprisingly, the inbreeding coefficient (Fis) declined over time in the captive permits unrestricted use, distribution, and repro- population, and is now approaching values observed in the 2013 wild population, duction in any medium, provided the original author and source are credited. despite a significant decrease in allelic richness. However, adult annual survival Data Availability: The authors confirm that all data and fecundity significantly declined in the second generation. These measures of underlying the findings are fully available without fitness were positively correlated with heterozygosity. Snails with higher measures restriction. All relevant data are within the paper. of heterozygosity had more offspring, and third generation offspring with higher Funding: The work was supported by United States Fish and Wildlife Service (USFWS) Grant measures of heterozygosity were more likely to reach maturity. These results Agreement and 12200-B-G009 (F11AP00028). The funders had no role in study design, data collection highlight the importance of maintaining genetic diversity in captive populations, and analysis, decision to publish, or preparation of particularly those initiated with a small number of individuals from wild remnant the manuscript. populations. Genetic rescue may allow for an increase in genetic diversity in the Competing Interests: The authors have declared that no competing interests exist. PLOS ONE | DOI:10.1371/journal.pone.0114377 December 3, 2014 1/16 Hawaiian Tree Snail Population Genetics and Bottleneck Effects captive population, as measures of heterozygosity and rarified allelic richness were higher in wild tree snails. Introduction Many species may be rescued from extinction only by ex situ or other managed breeding programs if the threat of introduced predators and continued habitat degradation persists [1]. However, few individuals may remain with which to found a captive-breeding program, resulting in a severe bottleneck when captive populations are initiated. Our understanding of the response of invertebrates, particularly molluscs, to severe bottlenecks is limited, yet these foundational species provide essential ecosystem functions, the loss of which will likely only be appreciated when they disappear [2]. Following a severe bottleneck, small captive populations of species with a long- life history and low fecundity are particularly vulnerable to synergistic interactions between demography and genetics. Hermaphroditic molluscs with high fecundity and the ability to self-fertilize may purge deleterious alleles and recover from a severe bottleneck [5]. Conversely, low fecundity may impede recovery in long- lived, late-maturing species. Deleterious alleles are more likely to accumulate in small populations, leading to declines in measures of fitness, such as survival and fecundity [4]. These lowered birth rates lessen the chance that deleterious mutations will be purged from the population, feeding back into their fixation [3]. The genus Achatinella consists of at least 41 species of hermaphroditic tree snails with long life spans, late maturity, and single, live births [6, 7]. Populations of these snails were once dense and abundant from sea level to at least 1500 m elevation, but today only fragmented, small populations remain. Habitat loss, predation by introduced species [7], and over-harvesting by collectors [8] led to the extinction of more than 30 species of Achatinella, and resulted in the declaration of all remaining species in the genus as Endangered [9]. One species of special concern is A. lila, with less than 200 known individuals remaining over less than five percent of its historic range (Fig 1). A captive population with seven snails was established in 1997 in the captive-rearing facility at the University of Hawai‘i at Ma¯noa as a hedge against extinction [6]. Following this constricted bottleneck, the population increased substantially from 1997 to 2009, reaching over 600 individuals, but is now in a five-year decline for unknown reasons. In this study we examined correlations between heterozygosity and several fitness measures including juvenile survival, survival to sexual maturity, and fecundity, and considered trends in the inbreeding coefficient (Fis) over generations. We also compared genetic variation in wild A. lila with the captive population to provide long-term management recommendations. PLOS ONE | DOI:10.1371/journal.pone.0114377 December 3, 2014 2/16 Hawaiian Tree Snail Population Genetics and Bottleneck Effects Figure 1. Achatinella lila historical range and two sampling locations. These two locations represent the only known populations that remain for this critically endangered species. The newly built predator exclosure will support in situ conservation efforts for wild snails endemic to this area. doi:10.1371/journal.pone.0114377.g001 Materials and Methods Captive Breeding Facility and Demographic Records The captive population of A. lila was founded in 1997 at the endemic Hawaiian tree snail captive-breeding facility at the University of Hawai‘i at Ma¯noa with seven adult snails collected and housed under USFWS permit PRT-826600. Sexual maturity is indicated by a lipped shell, or thickened edge of the shell aperture, at around 15 mm shell length in this species [10]. Once the lip is fully formed, shell growth ceases. Six of the founding snails were collected from a sampling location at the southern end of the species’ range, and an additional snail came from the northern end of the range (Fig 1). The relatedness of the founders is unknown, but PLOS ONE | DOI:10.1371/journal.pone.0114377 December 3, 2014 3/16 Hawaiian Tree Snail Population Genetics and Bottleneck Effects snails from the southern location were collected over a relatively small distance (less than 10 m). Captive snails were reared in environmental chambers with controlled temperature and humidity designed to mimic wild conditions [6]. Hawaiian tree snails feed on an epiphytic fungal biofilm in the wild, so leafy branches of native plant species were placed in cages when they were cleaned biweekly, along with agar-cultured calcium-supplemented mold (Cladosporium sp.) originally isolated from a native snail-host plant [6]. At the time of cage cleaning, demographic information was collected including births, deaths, and total numbers of juveniles (shell length ,9.5 mm), subadults (9.5 mm shell length to lipped shell), and adults. Individual snails were not labeled or tracked, but at death, each snail was individually preserved in 95% ethanol in a tube labeled with the species, shell length and width, source cage, and date of preservation (within 2 weeks of death). Demographic data were collected from 2018 snails preserved between 1998 and 2013, 198 living snails in 2013, and from facility records. Using shell growth curves generated in captive A. lila [10], birth dates were estimated for both preserved and living captive snails. The number of births per year calculated using this method did not differ statistically from the number of births per year according to lab records (t520.49, P50.63). Birth dates, combined with shell length at the time of death, were used to calculate juvenile survival (snails surviving more than one year beyond their birth date) for the years 1998 through 2012. Based on published growth curves [10] and laboratory records, we added four years to the birth date to estimate the date of maturity. These data were used to estimate fecundity, or the number of offspring per adult, calculated by dividing the total number
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