Diabolical survival in Death Valley: recent pupfish colonization, gene flow and genetic assimilation in the smallest species range on earth

Abstract

One of the most endangered vertebrates, the Devils Hole pupfish Cyprinodon diabolis, survives in a nearly impossible environment: a narrow subterranean fissure in the hottest desert on earth, Death Valley. This species became a conservation icon after a landmark 1976 US Supreme Court case affirming federal groundwater rights to its unique habitat. However, one outstanding question about this species remains unresolved: how long has diabolis persisted in this hellish environment? We used next-generation sequencing of over 13 000 loci to infer the demographic history of pupfishes in Death Valley. Instead of relicts isolated 2-3 Myr ago throughout repeated flooding of the entire region by inland seas as currently believed, we present evidence for frequent gene flow among Death Valley pupfish species and divergence after the most recent flooding 13 kyr ago. We estimate that Devils Hole was colonized by pupfish between 105 and 830 years ago, followed by genetic assimilation of pelvic fin loss and recent gene flow into neighbouring spring systems. Our results provide a new perspective on an iconic endangered species using the latest population genomic methods and support an emerging consensus that timescales for speciation are overestimated in many groups of rapidly evolving species.

Phylogenetics support an ancient common origin of two scientific icons: Devils Hole and Devils Hole pupfish

“…This calibration corresponds to a mean divergence time of 400 years (100–1000 years) between the species and refers to new studies proposing recent colonization and divergence of DHP in Devil's Hole (Reed & Stockwell ; Martin et al . ).…”

“…Recent Approximate Bayesian Computation (ABC) analyses using microsatellite markers suggest a divergence time of approximately 0.2–3 ka (Reed & Stockwell ), while demographic modelling from 13 000 genomic loci indicate DHP could have diverged as recently as 0.105–0.83 ka (Martin et al . ). These studies bring up the possibility of DHP being much younger than commonly thought, perhaps established by American Indians who relocated and harvested various pupfish species (Wilke & Lawton ; Farrell ; Finger et al .…”

“…; Reed & Stockwell ) or through frequent overland dispersal and mixing of Death Valley pupfish (Martin et al . ). The uncertainty surrounding when and how DHP became isolated in Devils Hole is troubling because this information is vital for determining its status as a critically endangered species and icon of persistence.…”

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

“…The Devils Hole pupfish Cyprinodon diabolis (Wales 1930) is a small cyprinodontiform fish belonging to a clade of allopatric pupfishes that evolved in the Death Valley region of the Mojave Desert in southern Nevada, USA (Miller 1948(Miller , 1950Duvernell & Turner 1998;Echelle 2008;Martin et al 2016).…”

Endocrine and metabolic impacts of warming aquatic habitats: differential responses between recently isolated populations of a eurythermal desert pupfish

“…In this study, we examined the influences of temperature on the endocrine physiology and metabolism of Amargosa pupfish, Cyprinodon nevadensis amargosae , from the Death Valley region of California and Nevada, USA. This extreme desert region is home to a clade of three pupfish species partitioned into eight subspecies (Miller, 1948; Soltz and Naiman, 1978), which appear to have evolved within the last 5000–20 000 years (Martin et al ., 2016). Similar to most other pupfishes through the North American desert southwest, Death Valley's pupfishes occupy restricted geographical ranges and are isolated in remote groundwater-fed springs, desert streams or marshes (Soltz and Naiman, 1978).…”