Phylogeographic analysis delimits three evolutionary significant units of least chipmunks in North America and identifies unique genetic diversity within the imperiled Peñasco population

Abstract

Although least chipmunks (Neotamias minimus) are a widely distributed North American species of least concern, the southernmost population, N. m. atristriatus (Peñasco least chipmunk), is imperiled and a candidate for federal listing as a subspecies. We conducted a phylogeographic analysis across the N. minimus range to assess genomic differentiation and distinctiveness of the N. m. atristriatus population. Additionally, we leveraged the historical component of sampling to conduct a temporal analysis of N. minimus genetic diversity and also considered climate change effects on range persistence probability by projecting a species distribution model into the IPCC5 RCP 2.6 and 8.5 scenarios. We identified three geographically structured groups (West, North, and South) that were supported by both mitochondrial and nuclear data. N. m. atristriatus grouped within a unique South subclade but were not reciprocally monophyletic from N. m. operarius, and nuclear genome analyses did not separate N. m. atristriatus, N. m. caryi, and N. m. operarius. Thus, while least chipmunks in the Southwest represent an evolutionary significant unit, subspecies distinctions were not supported and listing of the Peñasco population as a Distinct Population Segment of N. m. operarius may be warranted. Our results also support consideration of populations with North and West mitogenomes as two additional evolutionary significant units. We found that N. minimus genetic diversity declined by ~87% over the last century, and our models predicted substantial future habitat contraction, including the loss of the full contemporary ranges of N. m. atristriatus, N. m. arizonensis, and N. m. chuskaensis.

Misinterpretation of Genomic Data Matters for Endangered Species Listing: The Sub-specific Status of the Peñasco Least Chipmunk (Neotamias minimus atristriatus)

“…the clustering analyses, nuclear phylogenomic tree, and mitogenome haplotype network unequivocally grouped N. m. atristriatus with N. m operarius and N. m. caryi in the southern clade"; and 2) "Neither mitochondrial nor nuclear datasets identified reciprocally monophyletic diversity between N. m. atristriatus and the geographically proximate N. m. operarius and N. m. caryi" (Puckett et al, 2021, p. 10;13; emphases added by us). We refute the interpretation, principal conclusions, and taxonomic recommendations of Puckett et al (2021;as outlined above). In this paper we identify four broad conceptual issues that led to errant recommendations: (1) interpretation of subspecies and diagnosability, (2) inappropriate use of reciprocal monophyly as a criterion for subspecies, (3) importance of geographic isolation, and (4) error in hypothesis testing and misinterpretation of results.…”

“…This will necessitate an improvement in how scientists translate technical jargon for knowledge-users, and will ensure that the scientific interpretation of results accurately reflects the limitations of the genomic data or analyses. As an example of these persistent issues, we discuss the results, interpretation and conservation-related recommendations from a recently published phylogenomic study of chipmunks, which bear on a pending decision of U.S. federal protections under the Endangered Species Act (ESA; Puckett et al, 2021).…”

“…There are currently 21 subspecies of least chipmunks that reflect a complex history of differentiation and diverse ecological and biogeographical associations (Verts and Carraway, 2001). The main focus of Puckett et al (2021) was to evaluate the taxonomic validity of the Peñasco least chipmunk (N. m. atristriatus), a geographically isolated subspecies at the southernmost extent of the species' range, and which has been extirpated from most of its historical distribution (Hope and Frey, 2000;Frey and Boykin, 2007;McKibben and Frey, 2020). The taxon was described as a species by Vernon Bailey, a seminal mammalian taxonomist and naturalist, on basis of cranial and pelage characteristics (Bailey, 1913).…”

“…A thorough revision of the genus may show some other species to which it is more nearly related, but its range is widely separated from that of any other small species" (Bailey, 1913, p. 130). Neotamias m. atristriatus is not merely isolated from other populations, but is the most highly isolated of any least chipmunk population with a minimum distance of 200 km from the nearest population across unsuitable intervening habitat (see Puckett et al, 2021; Figure 1). This taxon is currently listed as Endangered within the State of New Mexico (NMDGF, 2016) and has been proposed to be listed as endangered under the ESA at the taxonomic level of subspecies (USFWS, 2021).…”

“…This taxon is currently listed as Endangered within the State of New Mexico (NMDGF, 2016) and has been proposed to be listed as endangered under the ESA at the taxonomic level of subspecies (USFWS, 2021). Puckett et al (2021) performed a series of genomic data analyses of target-captured nuclear exons (DNA that codes for gene functions and which may or may not be subject to selection Luikart et al, 2018). They reported their data as 513 single nucleotide polymorphisms (SNPs) or 259 concatenated exon sequence loci, depending on the analysis.…”