Rescued from extinction in two buckets: genomic consequences of an extreme bottleneck in the endangered Owens pupfish

Abstract

Rapid population bottlenecks can threaten population viability by reducing genetic diversity and effective population size while increasing inbreeding. Freshwater fishes are particularly vulnerable to bottlenecks due to habitat fragmentation, water extraction, and invasive species. The Owens pupfish (Cyprinodon radiosus) is an endangered freshwater fish endemic to Owens Valley, CA that was originally thought to be extinct prior to rediscovery in 1964. In 1969, Edwin (Phil) Pister famously saved the entire species from extinction in two buckets after learning that the sole spring they inhabited was drying up. Today, six extant refuge populations ranging in size from 100 - 10,000 individuals remain, which all descend from this severe bottleneck of an estimated 400 individuals. Here, we sequenced whole genomes of 12 individuals from two populations (one extirpated, one extant) to reconstruct recent demographic history and examine the genomic consequences of this well-documented bottleneck on genetic diversity, effective population size, and inbreeding in the Owens pupfish. We estimated the timing of the bottleneck precisely to 1977-1985, closely coinciding with its documented history. Genetic diversity is low across the genome and the bottleneck caused a 17-fold contraction in effective population size over the span of 8 generations. We found low levels of inbreeding that likely predated the bottleneck. Our results suggest that Owens pupfish are threatened by reduced genetic diversity and low effective population size which may constrain adaptive potential, but that recent inbreeding is unlikely to be a serious concern due to population expansion. Our study highlights how the long-term effects of bottlenecks depend not only on severity, but also duration and the rate of population growth afterwards.