Dramatic shifts in the gene pool of a managed population of an endangered species may be exacerbated by high genetic load

Abstract

The Devils Hole pupfish, Cyprinodon diabolis, is restricted to a small habitat in southwestern Nevada. In 1972 the species was federally listed as an endangered species. Management efforts to mitigate extinction risks have been plagued by the inability to propagate the species in aquaria-anomalous for the genus-and repeated failure of propagation attempts in large, outdoor, artificial pools designed to mimic natural conditions in Devils Hole. These difficulties indicate that the species either has niche requirements that are not adequately recreated under artificial conditions or that it harbors a relatively large genetic load of deleterious mutations that compromises propagation. We used variation at 12 microsatellite loci to evaluate the results of natural, uncontrolled hybridization involving a population of C. diabolis inhabiting an artificial pool and invaders from a nearby population of the closely related C. nevadensis. The results suggest that following invasion of the pool by three C. nevadensis individuals, the gene pool underwent a rapid shift from pure C. diabolis to one comprised mostly of C. nevadensis alleles. Alleles diagnostic for C. nevadensis increased from about 0.03 to an average of 0.76 across four diagnostic loci over the course of 8 years or less. Although we cannot exclude explanations based on adaptation to Devils Hole, genetic drift, or demographic variability, these results and various other aspects of the biology of C. diabolis are best explained by the genetic load hypothesis. The work suggest avenues for future experimental work to evaluate these possibilities directly and provide an explanation for why some previous propagation efforts designed to mitigate extinction risk have failed.

Sequencing and characterization of the complete mitochondrial genome of the endangered Devils Hole pupfish Cyprinodon diabolis (Cyprinodontiformes: Cyprinodontidae)

“…Since that time, the species experienced population bottlenecks including a low population size of 35 fish in 2013. Conservation efforts have aimed to recover C. diabolis in Devils Hole and establish additional populations in artificial refuges (Sharpe et al 1973;Baugh & Deacon 1988;Karam et al 2012), although past efforts were impeded by genetic and phenotypic changes to refuge populations (Williams 1977;Wilcox & Martin 2006;Martin et al 2012).…”

Evaluating an icon of population persistence: the Devil's Hole pupfish

“…Note that this assessment assumes that observed stochasticity in the time series is representative of population sizes from the past to the present time. As the Devil's Hole pupfish has exhibited a much smaller population size since 2004 [29,30], its likelihood of persistence into the future is at the lower end of our projections because of its current smaller population size. Furthermore, this species should not be used as a general measure of minimum viable population size or as justification for protecting vertebrate populations at sizes that are inadequate for long-term persistence [17].…”

“…This pupfish is a recognized endangered species that is protected by law, and many efforts have been made to protect the species (e.g. [24,27,29,30]). Our results, however, do suggest that assertions in the literature about the long-term persistence of the Devil's Hole pupfish (see Introduction) have been overestimated and that the persistence of C. diabolis to modern times should be viewed more modestly.…”

“…The population size recovered during the 1970s, and until recently the breeding population size (low yearly counts, pre-breeding) varied from approximately 125 to 310 individuals each year; since then, the population has varied at a smaller population size (electronic supplemental material, table S1). More recently, the population declined sharply [29,30], and intense efforts are underway to assist in population recovery.…”

“…The dataset included 12 microsatellite loci scored for 19 Devil's Hole pupfish (sampled across three time frames), 70 individuals from the Hoover Dam Refuge population of C. diabolis and 53 individuals from a population of C. n. mionectes ( [29,34]; see the electronic supplemental material, S-A). Our reference table, which consisted of 1 000 000 simulated datasets, formed the basis for parameter estimation.…”