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

Abstract

The Devils Hole pupfish (Cyprinodon diabolis; DHP) is an icon of conservation biology. Isolated in a 50 m(2) pool (Devils Hole), DHP is one of the rarest vertebrate species known and an evolutionary anomaly, having survived in complete isolation for thousands of years. However, recent findings suggest DHP might be younger than commonly thought, potentially introduced to Devils Hole by humans in the past thousand years. As a result, the significance of DHP from an evolutionary and conservation perspective has been questioned. Here we present a high-resolution genomic analysis of DHP and two closely related species, with the goal of thoroughly examining the temporal divergence of DHP. To this end, we inferred the evolutionary history of DHP from multiple random genomic subsets and evaluated four historical scenarios using the multispecies coalescent. Our results provide substantial information regarding the evolutionary history of DHP. Genomic patterns of secondary contact present strong evidence that DHP were isolated in Devils Hole prior to 20-10 ka and the model best supported by geological history and known mutation rates predicts DHP diverged around 60 ka, approximately the same time Devils Hole opened to the surface. We make the novel prediction that DHP colonized and have survived in Devils Hole since the cavern opened, and the two events (colonization and collapse of the cavern's roof) were caused by a common geologic event. Our results emphasize the power of evolutionary theory as a predictive framework and reaffirm DHP as an important evolutionary novelty, worthy of continued conservation and exploration.

Genomic Analysis Reveals Genetic Distinctiveness of the Paiute Cutthroat Trout Oncorhynchus clarkii seleniris

“…Therefore, in this study, instead of employing the more widely used concatenation (i.e., super-matrix) methods, we used a coalescence-based method to estimate the species phylogeny from a collection of gene trees by treating each concatenated set of RAD sequences within scaffolds as independent genomic regions (Song et al 2012;Saglam et al 2016). This method not only allowed different genomic regions to have different topologies (enabling us to effectively model gene tree heterogeneity) but also resulted in a species/population tree where each branching event describes divergence between species/populations as opposed to divergence of genes or haplotypes.…”

An embryonic staging series up to hatching for Cyprinodon variegatus: An emerging fish model for developmental, evolutionary, and ecological research

“…Many species of Cyprinodon occur in desert water systems, where allopatrically distributed species isolated in different desert springs exhibit a wide range of morphological and physiological diversity (Miller, ). The genus includes species with some of the most restricted geographic distributions among vertebrates, exemplified by the Devil's Hole pupfish ( C. diabolis ), a species entirely confined to a single aquifer pool in Ash Meadows, Nevada (Martin, Crawford, Turner, & Simons, ; Sağlam et al, ). However, other species of Cyprinodon are widely distributed, such as Cyprinodon variegatus that occurs in estuaries and brackish ponds along the Atlantic coastline from Massachusetts to the Gulf of Mexico and throughout the Caribbean.…”

“…Research on Cyprinodon spans an array of disciplines including phylogenetic inferences of North American paleoenvironments (Echelle, ; Echelle et al, ) use as models to understand how organisms adapt and tolerate stressful environments (Naiman, Gerking, & Ratcliff, ; Naiman, Gerking, & Stuart, ; Plath & Strecker, ), as ecotoxicology models and biological indicators of estuarine health (Bowman, Kroll, Hemmer, Folmar, & Denslow, ; Raimondo et al, ), and as conservation models to understand the dynamics of small population size (Martin et al, ; Sağlam et al, ). Furthermore, evolutionary biologists study fishes in the genus Cyprinodon to understand the mating behavior (Kodric‐Brown, ; West & Kodric‐Brown, ), speciation and hybridization (Martin, ; Martin & Feinstein, ; McGirr & Martin, ; Richards & Martin, ; Rosenfield & Brown, ; Turner, Duvernell, Bunt, & Barton, ), and the role of developmental plasticity in morphological evolution (Lema, , , ).…”

New evidence for the recent divergence of Devil's Hole pupfish and the plausibility of elevated mutation rates in endangered taxa

“…Searching for complex histories of gene flow and introgression within endangered taxa can also highlight the need for alternative management strategies to preserve this dynamic: Are endangered species relics that must be isolated or complex interconnected communities that would not persist without periodic influxes of secondary gene flow (Martin et al., ; Wayne & Shaffer, )? Answering this question is of critical importance for proper management (e.g., Eldridge et al., ; Kennedy, Grueber, Duncan, & Jamieson, ; Martin et al., ; Robinson et al., ); however, scientists should not fall into the trap of claiming that a species' age “is vital for determining its status as a critically endangered species” (Sağlam et al., ).…”

“…Sağlam et al. (); hereafter SEA) recently estimated the age of DHP. They compared divergence times with the neighbouring Ash Meadows Amargosa pupfish population ( C. nevadensis mionectes ) and one outgroup (Owens pupfish, C. radiosus ) by placing restrictive prior distributions on divergence times corresponding to four different scenarios, which has the effect of eliminating nearly all uncertainty in their divergence time estimates.…”