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.

Demographic and genetic factors in the recovery or demise ofex situpopulations following a severe bottleneck in fifteen species of Hawaiian tree snails

“…However, the ability to self-fertilize may be linked with high inbreeding coefficients and decreased heterozygosity, similar to other hermaphroditic species of snails (reviewed in Jordaens, Dillen & Backeljau, 2007 ). High inbreeding coefficients were observed in all generations of A. fuscobasis , A. lila , and P. variabilis ( Sischo et al, in press ; Price & Hadfield, 2014 ; this study), which were all very successful in captivity. One explanation for these high inbreeding coefficients may be that these species have a high occurrence of self-fertilization, even when mates for outcrossing are available.…”

“…For four of six species examined in this and previous studies, heterozygosity correlated with demographic measures. Positive correlations between heterozygosity and survival to maturity were observed for A. fulgens , A. sowerbyana, P. variabilis and A. lila (this study; Price & Hadfield, 2014 ), highlighting the importance of maintaining genetic diversity and avoiding breeding among close relatives in endangered populations, particularly those raised ex situ ( Theodorou & Couvet, 2015 ). Individuals of A. lila with higher heterozygosity were also more fecund ( Price & Hadfield, 2014 ), suggesting fecundity might be improved by increasing genetic diversity within populations.…”

“…Genetic samples were obtained from four species, A. apexfulva, A. fulgens, A. sowerbyana , and P. variabilis ( Table 4 ), for comparison with published results from sister species A. fuscobasis ( Sischo et al, in press ) and A. lila ( Price & Hadfield, 2014 ). Some correlations between heterozygosity and survival were observed within species ( Fig.…”

“…Genotypic data were collected from four achatinelline snail species ( Achatinella apexfulva, A. fulgens, A. sowerbyana, Partulina variabilis ) for comparison with two species assessed in two other studies ( A. lila , Price & Hadfield, 2014 ; A. fuscobasis , Sischo et al, in press ) to identify trends across species. Null-allele frequencies were assessed using the software Genepop ( Rousset, 2008 ).…”

“…Next, fitness measures were compared among three groups ( Table 1 ): (1) species that exceeded 100 individuals in captivity; (2) species that did not exceed 100 individuals in captivity; and (3) species that have since died out. Additionally, genetic influences on survival and population persistence were evaluated for four species, and compared with results from previous studies of two of the most successfully-reared tree snail species in the same lab ( Price & Hadfield, 2014 ; Sischo et al, in press ) to potentially identify trends across species.…”