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

Abstract

Hooper’s deer mouse, Peromyscus hooperi, is the sole member of the Peromyscus hooperi species group.  This species is endemic to México where it is restricted to the grassland transition zone in the states of Coahuila, Zacatecas, and San Luis Potosí.  Previous studies using mitochondrial and nuclear genes (Cytb, Adh1-I2, Fgb-I7 and Rbp3) did not resolve the phylogenetic relationships of this relatively poorly known species.  It was hypothesized that P. hooperi is sister to P. crinitus, and these two taxa are related to P. melanotis, P. polionotus, P. maniculatus, P. keeni, P. leucopus, P. gossypinus, P. eremicus, P. californicus, and Osgoodomys banderanus.  Based on morphological characters, karyotypes, and allozymes, P. hooperi does not align with either subgenera Haplomylomys or Peromyscus.  However, its unique characteristics (e. g., phallus, karyotype) have been recognized, and therefore it has been retained as its own species group.  To better resolve the phylogenetic placement of P. hooperi, we performed target-enrichment and high-throughput sequencing and obtained several thousand nuclear ultraconserved elements and a complete mitogenome from a specimen collected in 1896 by Nelson and Goldman in Coahuila, México.  We compared these data with 21 other species of neotomines using genome-wide data.  Contrary to previous studies, we found high nodal support for the placement of P. hooperi as sister to a clade that includes Podomys floridanus, Neotomodon alstoni, Habromys simulatus, H. ixtlani, Peromyscus mexicanus, P. megalops, P. melanophrys, P. perfulvus, P. aztecus, P. attwateri, P. pectoralis, and P. boylii.  We dated a Pliocene divergence of P. hooperi from its sister group at approximately 3.98 mya, and after the split of P. crinitus at ca. 4.31 mya from other peromyscines.  We demonstrated that genome-wide data improve the phylogenetic signal, independently of taxon sampling, for a phylogenetically problematic species such as P. hooperi.  We recommend that future genomic studies expand taxon sampling, including members of the subgenus Haplomylomys, to confirm the phylogenetic relationships of P. hooperi and the genetic status of its populations.