Museomics and the holotype of a critically endangered cricetid rodent provide key evidence of an undescribed genus

Abstract

Historical DNA obtained from voucher specimens housed in natural history museums worldwide have allowed the study of elusive, rare or even extinct species that in many cases are solely represented by museum holdings. This has resulted in the increase of taxonomic representation of many taxa, has led to the discovery of new species, and has yielded stunning novel insights into the evolutionary history of cryptic or even undescribed species. Peromyscus mekisturus, is a critically endangered cricetid rodent endemic to Mexico and is only known from two museum specimens collected in 1898 and 1947. Intensive field work efforts to attempt to determine if viable populations still exist have failed, suggesting that this species is extinct or is nearing extinction. In addition, a recent study using mitogenomes demonstrated that P. mekisturus forms a well-supported clade outside the genus Peromyscus and hypothesized that this taxon is the sister group of the genus Reithrodontomys. Here, we used target enrichment and high-throughput sequencing of several thousand nuclear ultraconserved elements and mitogenomes to reconstruct dated phylogenies to test the previous phylogenetic hypothesis. We analyzed the holotype and the only other known specimen of P. mekisturus and museum samples from other peromyscine rodents to test the phylogenetic position of the species. Our results confirm that the only two specimens known to science of P. mekisturus belong to the same species and support the hypothesis that this species belongs to an undescribed genus of cricetid rodents that is sister to the genus Reithrodontomys. We dated the origin of P. mekisturus together with other speciation events in peromyscines during the late Pliocene – early Pleistocene and related these events with the Pleistocene climatic cycles. In light of our results, we recommend a taxonomic re-evaluation of this enigmatic species to properly recognize its taxonomic status as a new genus. We also acknowledge the relevance of generating genomic data from type specimens and highlight the need and importance of continuing to build the scientific heritage of the collections to study and better understand past, present, and future biodiversity.

An 1896 specimen helps clarify the phylogenetic placement of the Mexican endemic Hooper’s deer mouse

“…4.31 mya (95 % HPD: 3.80 to 4.70 mya). These dates coincide with previously dated phylogenies obtained from genome-wide data of peromyscines (e. g., Castañeda-Rico et al 2022). They estimated the crown of the genus Peromyscus during the Pliocene at ca.…”

“…To our knowledge, this is one of a few studies in which genome-wide data were obtained and analyzed from a specimen collected by these two naturalists (see McDonough et al 2022). Our results not only provide new evidence about the phylogenetic position of P. hooperi but also joins a short list of mammal studies within the blooming field of Museomics (see Card et al 2021 for a review) that have successfully analyzed specimens collected before 1900 within a phylogeny (e. g., Abreu-Jr et al 2020;Sacks et al 2021;Roycroft et al 2021Roycroft et al , 2022Castañeda-Rico et al 2022;McDonough et al 2022;Tavares et al 2022). Our nuclear DNA results strongly support P. hooperi as sister to a clade containing Podomys floridanus, Neotomodon alstoni, Habromys simulatus, P. mexicanus, P. megalops, P. melanophrys, P. perfulvus, P. aztecus, P. attwateri, and P. pectoralis (all Peromyscus species within the subgenus Peromyscus).…”

“…However, the current resolution of this group does not fully adhere to either of those classifications. In addition, genetic and genomic studies have demonstrated the paraphyly of Peromyscus (Bradley et al 2007;Miller and Engstrom 2008;Platt et al 2015;Sullivan et al 2017;Castañeda-Rico et al 2022). While clarifying the definition of Peromyscus is beyond the scope and objective of this manuscript, it is important to point out that whether we align to the sensu lato or sensu stricto classification of the genus, the phylogenetic placement of P. hooperi has not been well-resolved.…”

“…The calibrated Yule speciation processes model (Heled and Drummond 2012) with a randomly generated starting tree were set up as priors. We used the same three calibration points with a lognormal distribution from Castañeda-Rico et al (2022). Calibrations were based on fossil records of 1) Reithrodontomys (mean = 1.8 million years ago [mya], stdev = 1.076, offset = 1.63), as used by Steppan and Schenk (2017); 2) Onychomys (mean = 4.9, stdev = 1.169, offset = 4.753), as used by Steppan and Schenk (2017); and 3) the most recent common ancestor of P. attwateri (mean = 2.7, stdev = 0.9, offset = 2.4 [Dalquest 1962;Karow et al1996;Wright et al 2020]).…”

From historical expedition diaries to whole genome sequencing: A case study of the likely extinct Red Sea torpedo ray

“…Museum collections are the most important archives of biodiversity on Earth and are used increasingly for various studies, including identification (Wannell et al, 2020), phylogenetics (Hawkins et al, 2016; Kehlmaier et al, 2020), population genomics (Castañeda‐Rico et al, 2022; Fry et al, 2020), conservation (Feigin et al, 2017; Jensen et al, 2022), biogeography (Irestedt et al, 2006; Lynch Alfaro et al, 2012; Pedersen et al, 2016), and ecology (Muff et al, 2023; Orlando & Cooper, 2014). However, molecular analysis of old museum material remains challenging because the historical DNA (the term coined by Raxworthy and Smith (2021) and adopted throughout this study) has degraded, is fragmented, and is of low quantity (Hagelberg et al, 2015; Hawkins et al, 2022).…”