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

Abstract

Sa glam et al. recently argued that the Devil's Hole pupfish (Cyprinodon diabolis), a conservation icon with the smallest known species range, was isolated 60 kya based on a new genomic data set. If true, this would be a radically long timescale for any species to persist at population sizes <500 individuals, in contrast to conservation genetics theory. However, here we argue that their analyses and interpretation are inappropriate. They placed highly restrictive prior distributions on divergence times, which do not appropriately model the large uncertainty and result in removing nearly all uncertainty from their analyses, and chose among models by assuming that pupfishes exhibit human mutation rates. We reanalysed their data with their same methods, only using an informative prior for the plausible range of mutation rates observed across vertebrates, including an estimate of the genomewide mutation rate from a pedigree analysis of cichlid fishes. In fact, Saglam et al.'s phylogenetic data support much younger median divergence times for C. diabolis, ranging from 6.2 to 19.9 kya, overlapping with our previous phylogenetic divergence time estimates of 2.5-6.5 kya. There are many reasons to suspect an even younger age and higher mutation rate in C. diabolis, as we previously estimated, due to their high metabolism, small adult size, small population size and severe environmental stressors. In conclusion, our results highlight the need for measuring mutation rate in this fascinating species and suggest that the ages of endangered taxa present in small, isolated populations may frequently be overestimated.

Speciation in sympatry with ongoing secondary gene flow and a potential olfactory trigger in a radiation of Cameroon cichlids

“…It should be noted that this estimate in turn relies on an estimate of the mutation rate. We here use an estimate from stickleback (Guo et al., ), following previous studies on cichlids (Kautt, Machado‐Schiaffino, Meyer et al., ; Kautt, Machado‐Schiaffino, Torres‐Dowdall et al., ), but it cannot be excluded that our focal species may have substantially different spontaneous mutation rates (Martin & Höhna, ; Martin et al., ; Recknagel, Elmer, & Meyer, ).…”

“…It should be noted that this estimate in turn relies on an estimate of the mutation rate. We here use an estimate from stickleback (Guo et al, 2013), following previous studies on cichlids Kautt, Machado-Schiaffino, Torres-Dowdall et al, 2016), but it cannot be excluded that our focal species may have substantially different spontaneous mutation rates (Martin & Höhna, 2018;Martin et al, 2017;Recknagel, Elmer, & Meyer, 2013). Martin, Cutler et al (2015) argued that the Cameroon lakes containing cichlid radiations may not be as isolated as has previously been suggested, based on the inference of secondary gene flow into all four radiations and the fact that each lake has been colonized by several different fish lineages (five in the case of Lake Ejagham).…”

Best available science still supports an ancient common origin of Devils Hole and Devils Hole pupfish

“…Recently, two different publications (Martin, Crawford, Turner, & Simons, & Sağlam et al., ) tackled this issue using genomic data sets and demographic models but came to widely different conclusions. In their comment, Martin and Höhne () argue that our results (Sağlam et al., ) were misleading because we used inappropriate calibration information and biased a priori assumptions. They then re‐analysed our data using a “biologically informed” mutation rate prior and concluded that our data support a much younger age of DHP (12.6 kya) as opposed to 60 kya reported in our study.…”

Editorial 2019

“…One Comment and its Reply debated whether high levels of observed hybridization and recombination challenges the "predominant clonal evolution" model of Trypanosoma congolense , which is the major pathogen responsible for nagana (sleeping sickness), a disease of cattle and other animals in Africa transmitted by the tsetse fly (Van den Broeck, Tavernier, Vermeiren, Dujardin, & Abbeele, ; Tibayrenc & Ayala, ). Other News and Views discussions included whether a very recent origin, assuming an unusually high mutation rate (Martin & Höhna, ) or an ancient origin, along with a more typical mutation rate (Saglam et al, ), is more likely for the endangered Devil's Hole pupfish.…”

“…Opinion papers discussed the best practices for effective SNP filtering for use in population genetic analyses (O'Leary, Puritz, Willis, Hollenbeck, & Portnoy, 2018) and argued for more consistent use of COI as the community DNA metabarcode for metazoans (Andujar, Arribas, Yu, Vogler, & Emerson, 2018). One Comment and its Reply debated whether high levels of observed hybridization and recombination challenges the "predominant clonal evolution" model of Other News and Views discussions included whether a very recent origin, assuming an unusually high mutation rate (Martin & Höhna, 2018) or an ancient origin, along with a more typical mutation rate (Saglam et al, 2018), is more likely for the endangered Devil's Hole pupfish.…”