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

Melissa R Price,Michael G Hadfield,Bi-Song Yue

doi:10.1371/journal.pone.0114377

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.

Highlights

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]
Small captive populations of species with a longlife history and low fecundity are vulnerable to synergistic interactions between demography and genetics
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]

Summary

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]. Small captive populations of species with a longlife history and low fecundity are 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]. 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]

Methods

Results

Conclusion