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Therya

versión On-line ISSN 2007-3364

Therya vol.14 no.1 La Paz ene. 2023  Epub 31-Jul-2023

https://doi.org/10.12933/therya-23-2243 

Special contributions

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

Susette Castañeda-Rico1  2  3  * 

Cody W. Edwards1  3 

Melissa T. R. Hawkins4 

Jesús E. Maldonado1  2  3 

1 Smithsonian-Mason School of Conservation, Front Royal, VA, U.S.A. Email: susetteazul@gmail.com, castanedaricos@si.edu (SC-R), cedward7@gmu.edu (CWE), maldonadoj@si.edu (JEM).

2 Center for Conservation Genomics, Smithsonian National Zoo and Conservation Biology Institute, Washington DC, U.S.A.

3 Department of Biology, George Mason University, Fairfax, VA, U.S.A.

4 Department of Vertebrate Zoology, Division of Mammals, National Museum of Natural History, Washington DC, U.S.A. Email: hawkinsmt@si.edu (MTRH).


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.

Keywords: Historical DNA; genomics; mitogenomes; museum specimens; Peromyscus, Pliocene-Pleistocene; ultraconserved elements

Resumen

El ratón de Hooper Peromyscus hooperi, es el único miembro del grupo de especies que lleva su mismo nombre. Es una especie endémica de México que se encuentra restringida a las zonas de transición de pastizales en los estados de Coahuila, Zacatecas y San Luis Potosí. Estudios previos en los que se han analizado genes mitocondriales y nucleares (Cytb, Adh1-I2, Fgb-I7 y Rbp3) no han podido resolver las relaciones filogenéticas de esta especie poco conocida. Sin embargo, se ha sugerido que P. hooperi podría ser la especie hermana de P. crinitus, y estar cercanamente relacionada con P. melanotis, P. polionotus, P. maniculatus, P. keeni, P. leucopus, P. gossypinus, P. eremicus, P. californicus y Osgoodomys banderanus. Con base en datos morfológicos, cariotipos y aloenzimas, no se ha podido determinar si esta especie se encuentra más estrechamente relacionada con el subgénero Haplomylomys o Peromyscus. Sin embargo, las características únicas de P. hooperi (e. g., falo, cariotipo) han sido reconocidas, por lo que se ha mantenido en su propio grupo de especies. Con el objetivo de proveer nueva evidencia sobre la posición filogenética de P. hooperi, utilizamos el método de captura por hibridación y secuenciación masiva para obtener miles de elementos ultraconservados y el genoma mitocondrial de un ejemplar colectado en 1896 por Nelson y Goldman en Coahuila, México. Además, analizamos datos genómicos de 21 especies de neotominos. Contrario a estudios previos, encontramos altos valores de soporte en el nodo que posiciona a P. hooperi como la especie hermana del clado que incluye a Podomys floridanus, Neotomodon alstoni, Habromys simulatus, H. ixtlani, Peromyscus mexicanus, P. megalops, P. melanophrys, P. perfulvus, P. aztecus, P. attwateri, P. pectoralis y P. boylii. Datamos la divergencia de P. hooperi de su grupo hermano hace aproximadamente 3.98 millones de años, después de la divergencia de P. crinitus y de otros peromiscinos hace aproximadamente 4.31 millones de años, ambos eventos durante el Plioceno. Nuestro estudio es un claro ejemplo de que analizar datos a nivel del genoma mejoran la señal filogenética, independientemente del número de taxones, para especies cuyas relaciones filogenéticas son conflictivas o se encuentran poco resueltas como en el caso de P. hooperi. Sin embargo, recomendamos que futuros estudios genómicos incluyan un muestreo taxonómico más amplio, sobre todo de miembros del subgénero Haplomylomys, para confirmar las relaciones filogenéticas de P. hooperi y el estatus genético de sus poblaciones.

Introduction

Two of the most important naturalists from the turn of the 20th Century were Edward William Nelson and Edward Alphonso Goldman. They contributed greatly to our knowledge, understanding, and documentation of the biota in the United States and México (López-Medellin and Medellin 2016, https://sova.si.edu/record/SIA.FARU7364). The scientific material collected by both naturalists continues to be used as a rich resource in the systematic revision of many groups of birds and mammals (López-Medellin and Medellin 2016). Nelson and Goldman’s biological surveys encompassed all of the states in México and lasted 14 years (1892 to 1906). In 1896, Nelson and Goldman conducted field work in Coahuila, México where they collected three individuals, later recognized as Peromyscus hooperi. These specimens were deposited and remain housed at the Smithsonian Institution’s National Museum of Natural History in Washington DC.

Peromyscus hooperi is a monotypic species, endemic to México and only known from portions of the states of Coahuila, Zacatecas, and San Luis Potosí (Álvarez-Castañeda 2002). This species is sympatric with P. eremicus, P. melanophrys, and P. pectoralis in the states of Coahuila and Zacatecas (Schmidly et al. 1985). Its preferred habitat is the grassland transition zone, a mixture of desert scrub and grassland vegetation (Schmidly et al. 1985; Lee and Schmidly 1977). Its present fragmented and restricted distribution is considered a relict of a much larger historical distribution (Schmidly et al. 1985).

Peromyscus hooperi is poorly represented in mammal collections and little is known about its current status in their restricted distribution; however, it is not protected by the Mexican government (Norma Oficial Mexicana - 059 - 2020, Secretaría de Medio Ambiente y Recursos Naturales 2010) and is classified as Least Concern by the International Union for Conservation of Nature - IUCN - (accessed on August 2022, Álvarez-Castañeda 2016). The species resembles P. eremicus, P. merriami, and P. pectoralis in cranial and external characters but differs in the karyotype (Lee and Schmidly 1977; Schmidly et al. 1985). Fuller et al. (1984) and Schmidly et al. (1985) found that the karyotype of P. hooperi is very similar to P. crinitus, P. simulus, Osgoodomys banderanus and northern populations of P. boylii. However, P. hooperi has been described as a medium size mouse for the genus, with a long and bicolored tail (light grayish brown above and whitish below) with short hair. The upper parts, including face and top of head, are grayish with faint to moderate wash brown; lateral line is faint and near light buff; underparts are cream; and hind feet and lower legs are whitish. The skull contains large auditory bullae, and the first two upper and lower molars lack mesolophs. The glans penis is small but wide with a long protractile tip, and the baculum is long and slender with a cartilaginous tip (Lee and Schmidly 1977). The karyotype (2n = 48, FN = 52) comprises three pairs of biarmed autosomes and 20 pairs of acrocentric acrosomes (Lee and Schmidly 1977; Schmidly et al. 1985).

The taxonomic affinity of Hooper’s deer mouse has been problematic (Carleton 1989). Based on a series of morphological characters (i. e., cranial characteristics, accessory lophs, and styles of the anterior molars, structure of the hyoid, and number and placement of the mammae) it was suggested to be closely related to the subgenus Haplomylomys (Lee and Schmidly 1977). However, based on the anatomy of the phallus, it was more similar to species representing the subgenus Peromyscus (Lee and Schmidly 1977; Schmidly et al. 1985). Therefore, P. hooperi was characterized as an intermediate form between these two subgenera (Lee and Schmidly 1977; Fuller et al. 1984; Schmidly et al. 1985). Peromyscus hooperi currently is recognized as the sole member of the Peromyscus hooperi species group (Schmidly et al. 1985; Carleton 1989), based on morphological characters, karyotypes, allozymes, and mtDNA - cytochrome b (Cytb; Carleton 1989; Musser and Carleton 1993, 2005; Hogan et al. 1993; Dawson 2005; Bradley et al. 2007).

Bradley et al. (2007) used Cytb sequence data to conduct a phylogenetic analysis of the genus Peromyscus. They recovered strong nodal support for a sister group relationship between P. hooperi and P. crinitus with Maximum Parsimony (MP), however, using Maximum Likelihood (ML) and Bayesian Inference (BI) they did not resolve this relationship. In turn, this clade was sister to a clade including P. melanotis, P. polionotus, P. maniculatus, P. keeni, P. leucopus, P. gossypinus, P. eremicus, P. californicus, and Osgoodomys banderanus. Platt et al. (2015), included Cytb and three nuclear genes - Adh1-I2, Fgb-I7 and Rbp3, and concluded that the phylogenetic position of P. hooperi remains uncertain due to a lack of support values and the different placement between ML and BI analyses.

An additional problem for the systematic classification of the species within Peromyscus is the very definition of the genus. Several revisions and classifications have recognized subgenera - sensu lato - (Osgood 1909; Hooper and Musser 1964; Hooper 1968) and genera - sensu stricto - (Carleton 1980; Carleton 1989; Musser and Carleton 2005) within 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. However, hereafter, we recognized the genus Peromyscus as paraphyletic, including Habromys, Megadontomys, Neotomodon, Osgoodomys, and Podomys at the generic level (sensu stricto).

Uncertainty of the phylogenetic position of P. hooperi based on previous studies necessitates a revaluation using additional sequence data. To accomplish this, we used genome-wide data, including several thousand nuclear ultraconserved elements and whole mitochondrial genomes from a museum voucher specimen of P. hooperi collected by Nelson and Goldman combined with data from previous studies. These data provide new evidence about the phylogenetic placement of P. hooperi and its time of divergence from other peromyscines.

Materials and methods

Sample collection and laboratory methods. We used a museum specimen sample of Peromyscus hooperi - USNM 79619 - (ca. 2 mm2 of dry skin) deposited at the Smithsonian Institution’s National Museum of Natural History; and collected by E. W. Nelson and E. A. Goldman on August 14, 1896 from Carneros, Coahuila, México. We followed strict protocols to avoid contamination during sampling, as described in McDonough et al. (2018) and Castañeda-Rico et al. (2020). All pre-PCR steps were performed in a laboratory dedicated to processing ancient and historical DNA at the Center for Conservation Genomics, Smithsonian National Zoo and Conservation Biology Institute, Washington, DC. A silica column extraction protocol (McDonough et al. 2018) was used to extract DNA. We quantified DNA with a Qubit 4 fluorometer (Thermo Fisher, Waltham, MA) using a 1x dsDNA HS assay and visualized DNA with a TapeStation 4200 System (Agilent Technologies, Santa Clara, CA) using High Sensitivity D1000 reagents. A dual-indexed library was prepared using the SRSLY PicoPlus NGS library prep kit (Claret Bioscience, LLC), according to the manufacturer’s protocol. We performed dual indexing PCR with TruSeq-style indices (Meyer and Kircher 2010) using Kapa HiFi HotStart Uracil+ (Roche Sequencing), following the manufacturer’s protocol. This library was amplified with 12 cycles of PCR. We then pooled three PCRs from the same library before cleaning to increase DNA fragment representation. We cleaned the indexed library using 1.6X solid-phased reversible immobilization (SPRI) magnetic beads (Rohland and Reich 2012), quantified concentration using a Qubit 4 fluorometer, and inspected size ranges and quality with a TapeStation 4200 System (conditions as mentioned above). Target-enrichment was performed to capture ultraconserved elements (UCE) and mitogenomes using the myBaits® UCE Tetrapods 5Kv1 kit (Daicel Arbor Biosciences) following the myBaits protocol v3, and the myBaits® Mito kit (Daicel Arbor Biosciences) for the house mouse Mus musculus panel, following the myBaits protocol v4. We amplified post-enrichment UCE and mitogenome libraries with 18 cycles of PCR using Kapa HiFi HotStart Ready Mix (Roche Sequencing), following the manufacturer’s protocol. A 1.6X SPRI magnetic bead clean-up was performed subsequently. We again quantified and visualized the enriched libraries using a Qubit 4 fluorometer and a TapeStation 4200 System, respectively (conditions as mentioned above). Finally, captured libraries were sequenced on a partial lane of a NovaSeq 6000 SP PE 2 x 150 base pairs (bp; Illumina, Inc., San Diego, CA, US) at the Oklahoma Medical Research Foundation, Oklahoma City (combined with samples from unrelated projects).

In addition to the data generated in this study, we also reanalyzed previously published data including the following: UCEs and full mitogenomes from Castañeda-Rico et al. (2020, 2022), as well as Cytb gene sequences from Bradley et al. (2007), Platt et al. (2015), and Sullivan et al. (2017; Table 1 and Appendix 1).

Ultraconserved elements. We analyzed the raw data following the PHYLUCE v1.6.7 pipeline with the default parameters (Faircloth 2016 https://github.com/faircloth-lab/phyluce). Illumiprocessor 2.10 (Faircloth 2013) and Trim Galore 0.6.5 (https://github.com/FelixKrueger/TrimGalore) were used to trim adapters, barcode regions and low-quality bases. Reads were assembled into contigs using Trinity 2.8.5 (Grabherr et al. 2011), and identified contigs matching UCE loci in the 5K UCE probe set (https://github.com/faircloth-lab/uce-probe-sets). A monolithic FASTA file was produced to extract sequences from each sample. We aligned FASTA sequences using MAFFT 7.4 (Katoh and Standley 2013; Nakamura et al. 2018) and performed edge trimming. The resulting alignments were filtered to test them for various degrees of missing data (matrix completeness): 65 % matrix (35 % of the taxa missing for each UCE locus), 75 % matrix (25 % of taxa missing), 85 % matrix (15 % of taxa missing), 90 % matrix (10% of taxa missing), and 95 % matrix (5 % of taxa missing). Samples included in this dataset are shown in Table 1. We quantified informative sites with the PHYLUCE script phyluce_align_get_informative_sites.py. All of these analyses were performed on the Smithsonian Institution High Performance Computing Cluster (Smithsonian Institution, https://doi.org/10.25572/SIHPC).

Table 1 Specimens examined in this study using UCE and mitogenomes with species name, accession number collection/ID study (Smithsonian Institution’s National Museum of Natural History USNM, Museum of Texas Tech University TK, and TTU associated, Museo de Zoología "Alfonso L. Herrera" Facultad de Ciencias UNAM MZFC, and University of Michigan Museum of Zoology -UMMZ), reference (the study from which the sequences were obtained or reanalyzed), GenBank BioProject, and GenBank accession numbers. 

Species Number Scientific Collection/ID Reference UCE (GenBank BioProject) Mitogenome (GenBank number)
Peromyscus hooperi USNM79619/USNM79619 This study PRJNA880321 OP432689
Peromyscus boylii This study MZ433362
Peromyscus maniculatus This study MH260579
Peromyscus leucopus This study BK010700
Peromyscus megalops USNM340233/USNM340233 Castañeda-Rico et al. (2022) PRJNA838631 ON528115
Peromyscus attwateri TTU143738/TK185663 Castañeda-Rico et al. (2022) PRJNA838631 ON528112
Peromyscus aztecus USNM569848/USNM569848 Castañeda-Rico et al. (2022) PRJNA838631 ON528113
Peromyscus polionotus USNM585473/USNM585473 Castañeda-Rico et al. (2022) PRJNA838631 ON528117
Peromyscus crinitus TTU146966/TK193714 Castañeda-Rico et al. (2022) PRJNA838631 ON528114
Podomys floridanus TTU97866/TK92501 Castañeda-Rico et al. (2022) PRJNA838631 ON528118
Neotomodon alstoni TTU82668/TK93098 Castañeda-Rico et al. (2022) PRJNA838631 ON528110
Onychomys leucogaster TTU146304/TK171574 Castañeda-Rico et al. (2022) PRJNA838631 ON528111
Reithrodontomys mexicanus TTU138428/TK178510 Castañeda-Rico et al. (2022) PRJNA838631 ON528119
Isthmomys pirrensis USNM565924/USNM565924 Castañeda-Rico et al. (2022) PRJNA838631 ON528108
Neotoma mexicana TTU104969/TK150189 Castañeda-Rico et al. (2022) PRJNA838631 ON528109
Peromyscus mekisturus UMMZ88967/UMMZ88967 Castañeda-Rico et al. (2020) PRJNA606805 MT078818
Peromyscus melanophrys MZFC3907/MQ1229 Castañeda-Rico et al. (2020) PRJNA606805 MT078816
Peromyscus perfulvus /MCP119 Castañeda-Rico et al. (2020) PRJNA606805 MT078817
Peromyscus pectoralis MZFC10465/FCR176 Castañeda-Rico et al. (2020) PRJNA606805 MT078819
Peromyscus mexicanus MZFC11150/MRM030 Castañeda-Rico et al. (2020) PRJNA606805
Habromys simulatus MZFC10104/HBR031 Castañeda-Rico et al. (2020) PRJNA606805

We conducted a Maximum Likelihood (ML) analysis using RAxML 8.12 (Stamatakis 2014) with a GTRGAMMA site rate substitution model and 20 ML searches for the phylogenetic tree for each of the aforementioned data matrices (i. e., 65 % to 95 % matrices). Nonparametric bootstrap replicates were generated using the -N autoMRE option which runs until convergence was reached. We reconciled the best fitting ML tree with the bootstrap replicate to obtain the final phylogenetic tree with support values using the -f b command.

We estimated the best evolutionary model of nucleotide substitution in jModelTest 2.1.1 (Guindon and Gascuel 2003; Darriba et al. 2012) using the Akaike Information Criterion (AIC). The TVW+G model was selected as the best fitting model with the following parameters: base frequencies A = 0.2988, C = 0.2013, G = 0.2026, T = 0.2972; nst = 6; and gamma shape = 0.1070. A Bayesian Inference analysis (BI) using MrBayes 3.2.6 (Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003) was performed on the 90 % matrix. The BI analyses comprised two independent runs with 50 million generations, sampling trees and parameters every 1,000 generations with four Markov-chains Monte Carlo (MCMC), three heated and one cold. We visualized output parameters using Tracer v1.7.1 (Rambaut et al. 2018) to check for convergence between runs and we discarded the first 25 % of the trees as burn-in.

A species tree analysis under the multispecies coalescent (MSC) model with ASTRAL-III v.5.7.8 (Zhang et al. 2018) was performed on the 90 % matrix. The local posterior probability - LPP - (Sayyari and Mirarab 2016) was used as branching support. We used the uce2speciestree pipeline script (Campana 2019 https://github.com/campanam/uce2speciestree) to generate input files for ASTRAL. This script uses RAxML to infer individual gene trees under the GTRGAMMA substitution model, and 100 bootstrap replicates.

Mitogenomes. FASTQ files were analyzed using FastQC v0.11.5 (Andrews 2010, www.bioinformatics.babraham.ac.uk/projects/fastqc). Adapter sequences and low-quality reads were removed using the default parameters (Phred:20, mean min-len:20) in Trim Galore 0.6.5 (https://github.com/FelixKrueger/TrimGalore). Exact duplicates were removed (-derep1,4) using Prinseq-lite v0.20.4 (Schmieder and Edwards 2011). We mapped the resulting high-quality reads to the closest available reference genome (Peromyscus crinitus - GenBank accession number KY707308), using the Geneious algorithm in Geneious Prime® 2021.2.2 (https://www.geneious.com) with default parameters (Medium-Low sensitivity, Maximum mismatches = 20 %, Maximum gaps = 10 %). A consensus sequence was generated with Geneious Prime® 2021.2.2 (https://www.geneious.com), using 4X as the lowest coverage to call a base, and aligned them using MAFFT 7.45 plug-in (Katoh and Standley 2013). We transferred annotations from the reference to rule out the presence of nuclear copies of mitochondrial genes (NUMTs), and translated all protein-coding genes to check for frame shifts or stop codons.

We aligned sequences with MAFFT 7.45 plug-in (Katoh and Standley 2013) in Geneious Prime® 2021.2.2 (https://www.geneious.com). Samples included in this dataset are listed in Table 1. A BI analysis was conducted on a partitioned dataset using MrBayes 3.2.6 (Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003). The best model and partition scheme were estimated using PartitionFinder 2.1.1 (Lanfear et al. 2016). Our search was limited to the models available in MrBayes, with linked, corrected Akaike Information Criterion (AICc) and greedy parameters. The data block was defined by gene, tRNA, rRNA and D-loop selection. We conducted two independent runs with 50 million generations, sampling trees and parameters every 1,000 generations with four MCMC and parameters as mentioned above, to perform the BI analysis. Convergence between runs was checked using Tracer v1.7.1 (Rambaut et al. 2018), and the first 25 % of the trees was discarded as burn-in.

We performed a ML analysis using the concatenated dataset in RAxML 8.12 (Stamatakis 2014) with a GTRGAMMA site rate substitution model. Clade support was assessed by bootstrapping with the -N autoMRE option for a bootstrap convergence criterion. The -f b option was used to reconcile the best fitting ML tree with the bootstrap replicate to obtain the final phylogenetic tree (as mentioned above). DNA damage patterns were evaluated for the P. hooperi sample with mapDamage2.0 (Jónsson et al. 2013) using -- rescale option.

Cytochrome b. We analyzed Cytb sequences extracted from the mitogenome that was generated in this study and from mitogenomes published by Sullivan et al. (2017) and Castañeda-Rico et al. (2020, 2022). We also used the Cytb sequences published by Bradley et al. (2007) and Platt et al. (2015) in order to compare the phylogenetic position of P. hooperi using genome-wide data as well as a single mitochondrial gene. The Cytb dataset allowed us to include more species within the genus Peromyscus and representatives of the genera Habromys, Megadontomys, Neotomodon, Osgoodomys, Podomys, Isthmomys, Onychomys, Reithrodonyomys, Neotoma, Ochrotomys, Baiomys, Ototylomys, Tylomys, Nyctomys, Oryzomys and Sigmodon. Samples included in this dataset are shown in Table 1 and Appendix 1.

The Cytb dataset was analyzed as follows: we performed alignment using MAFFT 7.45 plug-in (Katoh and Standley 2013) in Geneious Prime® 2021.2.2 (https://www.geneious.com). We estimated the best evolutionary model of nucleotide substitution in jModelTest 2.1.1 (Guindon and Gascuel 2003; Darriba et al. 2012) using the AIC method. The TPM3uf+I+G model was selected as the best fitting model with the following parameters: base frequencies A = 0.3896, C = 0.3336, G = 0.0500, T = 0.2267; nst = 6; proportion of invariable sites = 0.4080; and gamma shape = 0.6220. A BI analysis was run using MrBayes 3.2.6 (Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003) as mentioned above for UCE and mitogenome datasets. We used Tracer v1.7.1 (Rambaut et al. 2018) to check for convergence between runs, and the first 25 % of the trees was discarded as burn-in.

Divergence times estimation. Molecular dates of divergence were estimated in BEAST2 v2.6.6 (Bouckaert et al. 2019) using the mitogenome dataset. First, we obtained the best model and partition scheme in PartitionFinder 2.1.1 (Lanfear et al. 2016). The search was limited to the models available in BEAST, linked branch lengths, AICc model selection, and greedy schemes search. The data block was defined by codon position, tRNA, rRNA and D-loop selection, and the result was incorporated in the dating analysis. The BEAST analysis was performed under an uncorrelated lognormal relaxed molecular clock model. 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 al.1996; Wright et al. 2020]). Two independent runs of 50 million iterations were performed, each was sampled every 1,000 iterations. We checked convergence statistics for Effective Sample Sizes (ESS) using Tracer v1.7.1 (Rambaut et al. 2018) and a 25 % of burn-in was performed on each run. We used LogCombiner v2.6.6 to combine trees and TreeAnnotator v2.6.2 to get a consensus tree with node height distribution (both packages available in BEAST). All phylogenetic and ultrametric dated trees from the UCE, mitogenome and Cytb datasets were visualized in FigTree 1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/). All analyses were performed on the Smithsonian Institution High Performance Computing Cluster (Smithsonian Institution https://doi.org/10.25572/SIHPC).

Results

Following the PHYLUCE v1.6.7 pipeline, we recovered 1,087 UCE loci (raw data are available in GenBank under BioProject PRJNA880321), and a complete mitogenome of 16,288 bp (GenBank accession number OP432689) from the P. hooperi sample. The average number of paired-end reads and fragment size after trimming were 13,075,112 reads and 67 bp long, respectively. The lowest-quality bases were detected at the end of the reads. We also recovered between 1,353 and 3,859 UCE loci from the reanalyzed samples. The average number of paired-end reads and fragment size after trimming for those samples ranged from 1,811,856 to 21,093,430 reads, and from 94 to 222 bp, respectively.

Ultraconserved Elements phylogenies. We recovered 9,840 contigs for P. hooperi after Trinity assemblies. The mean, minimum, and maximum length for contigs were 242, 201, and 3,784 bp, respectively. The incomplete matrix contained 4,406 UCE loci (n = 18, average = 3,136, min = 1,087, max = 3,859). A total of 1,087 UCE loci were obtained for P. hooperi with a mean, minimum, and maximum length of 235, 201, and 636 bp, respectively. The 65 % matrix contained 3,681 UCE loci (UL) with an average of 13.80 informative sites per locus (IS), the 75 % matrix (UL = 2,974, IS = 14.18, the 85 % matrix (UL = 1,514, IS = 14.29), the 90 % matrix (UL = 677, IS = 14.07), and the 95 % matrix (UL = 168, IS = 14.30).

The datasets representing various levels of matrix completeness yielded the same ML topology with high support values for all branches (Figure 1, phylogenetic trees obtained from the 65 %, 75 %, 85 %, and 95 % matrices are not shown). The BI tree topology, based on the 90 % matrix, showed the same topology with high posterior probability values for all branches (Figure 1). Both, ML and BI trees placed P. hooperi as sister to the clade containing Podomys floridanus, Neotomodon alstoni, P. mexicanus, P. megalops, P. melanophrys, P. perfulvus, P. aztecus, Habromys simulatus, P. attwateri, and P. pectoralis. The species tree supported, with high LPP values, the same phylogenic position of P. hooperi (Figure 1, based on the 90 % matrix). The only difference among the species tree and the concatenated ML and BI trees, was the relationship between P. mexicanus and P. megalops. These two species are sisters in the ML and BI trees but not in the species tree, where P. megalops is sister to the clade containing P. mexicanus, P. melanophrys, P. perfulvus, P. aztecus, Habromys simulatus, P. attwateri, and P. pectoralis.

Figure 1 (a) Bayesian Inference and Maximum Likelihood phylogenies based on a 90 % matrix UCE with 677 loci. Nodal support is provided with posterior probability/bootstrap values. (b) Species tree based on a 90 % matrix UCE with 677 loci. Nodal support is provided with local posterior probability values. The blue block highlights the phylogenetic position of Peromyscus hooperi

Mitogenome phylogenies. The final alignment included 21 taxa and was 16,272 bp in length. BI and ML analyses, with six partitions, provided slightly different topologies (Figure 2). However, both analyses supported (pp = 1, bootstrap = 76) the placement of P. hooperi as sister to the clade including Podomys floridanus, Neotomodon alstoni, P. mexicanus, P. megalops, P. melanophrys, P. perfulvus, P. boylii, P. aztecus, Habromys ixtlani, P. attwateri, and P. pectoralis. The phylogenetic position of P. crinitus changed across phylogenies (Figure 2), as did the position of the clade containing Podomys floridanus + Neotomodon alstoni. However, the BI tree yielded higher support values. The DNA damage analysis showed a weak signal of damage, typical of historical DNA (Appendix 2).

Cytochrome b phylogeny. The alignment included 64 taxa, 154 sequences, and was 1,143 bp in length. The BI analysis placed P. hooperi sister to the clade containing P. maniculatus, P. polionotus, P. keeni, P. melanotis, P. leucopus, and P. gossypinus (Appendix 3). However, the branch support value for this phylogenetic position was low (pp = 0.53). The two samples of P. hooperi, one sequenced in this study (USNM 79619) and the other by Bradley et al. (2007; TTU 104425, GenBank accession number DQ973103) clustered together with high support (pp = 1).

Divergence time estimation of Peromyscus hooperi. The mitochondrial divergence dating analysis, with six data partitions, estimated a Pliocene divergence time for P. hooperi around 3.98 mya (95 % HPD: 3.57 to 4.47 mya; Figure 3). The divergence of P. crinitus was dated ca. 4.31 mya (95 % HPD: 3.80 to 4.70 mya), the split of the clade including P. leucopus + (P. polionotus + P. maniculatus) at ca. 4.49 mya (95 % HPD: 4.03 - 5.02 mya), and the divergence of the genus Peromyscus was dated ca. 5.21 mya (95 % HPD: 4.79 - 5.71 mya).

Figure 2 Mitogenome phylogenies based on Bayesian Inference (a) and Maximum Likelihood (b). Nodal support is provided with posterior probability and bootstrap values, respectively. The blue block highlights the phylogenetic position of Peromyscus hooperi

Discussion

The biological expeditions undertaken by Nelson and Goldman in México were arguably among the most important ever achieved by two naturalists for a single country (López-Medellin and Medellin 2016; Guevara 2021; https://sova.si.edu/record/SIA.FARU7364). 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. 2021, 2022; Castañeda-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). In the mitogenome analyses, P. boylii (subgenus Peromyscus) and H. ixtlani joined the sister group of P. hooperi (Figure 1, 2). However, our results do not agree with those of Bradley et al. (2007), who found low support for P. hooperi as sister to P. crinitus (subgenus Peromyscus, Peromyscus crinitus species group), and both species sister to a clade including P. melanotis, P. polionotus, P. maniculatus, P. keeni, and P. leucopus (subgenus Peromyscus, Peromyscus leucopus and maniculatus species groups), P. gossypinus, P. eremicus, and P. californicus (subgenus Haplomylomys, Peromyscus californicus and eremicus species groups), and Osgoodomys banderanus. Platt et al. (2015) showed that P. hooperi could be related with the same species suggested by Bradley et al. (2007), although P. polionotus and P. keeni were not included in their study. However, the phylogenetic position of P. hooperi remained uncertain due to lack of strong nodal support in both of these previous studies.

Figure 3 Dated whole mitochondrial genome phylogeny. Dates are provided in millions of years. The horizontal bars and numbers below the branches show the 95 % Highest Posterior Density. The blue block highlights the phylogenetic position of Peromyscus hooperi

Our phylogenomic analyses strongly support the placement of P. hooperi with the Peromyscus mexicanus, megalops, aztecus, melanophrys, and truei species groups (all within the subgenus Peromyscus). We did include three out of the five species groups studied by Bradley et al. (2007). We analyzed the only member of the Peromyscus crinitus species group in the nuclear and mitogenome dataset, and members of the Peromyscus maniculatus and leucopus species group only in the mitogenome dataset; but we did not find that P. hooperi is closely related to any of those groups as previously suggested. Despite the novel data generated here, denser taxon sampling is still required to better confirm and/or determine the closest relative of P. hooperi. For example, phylogenetic relationships between P. hooperi and members of the subgenus Haplomylomys still require further testing. However, despite this limitation, here we have provided strong nodal support for P. hooperi for the first time.

The Cytb analysis (Appendix 3) confirmed the identity of the P. hooperi specimen used in this study (USNM 79619), placing it in the same clade with the only other P. hooperi Cytb sequence available (Bradley et al. 2007, TTU 104425 and GenBank accession number DQ973103). In addition, the phylogenetic position of the species in this analysis is similar to Bradley et al. (2007) and Platt et al. (2015). We found that P. hooperi is most closely related to the Peromyscus leucopus and maniculatus species groups but with a low support (pp = 0.53); therefore, its phylogenetic position is not resolved. In conclusion, we confirmed that the phylogenetic position of the Hooper’s deer mouse cannot be resolved using only Cytb sequences or a few genes, as Platt et al. (2015) documented. Our results demonstrate that genome-wide data allow a better resolution of the phylogenetic relationships of phylogenetically problematic species.

Our divergence times estimations indicated that the crown of Peromyscus was estimated ca. 5.21 mya (95 % HPD: 4.79 to 5.71 mya), and the diversification of the genus occurred ca. 4.49 mya (95 % HPD: 4.03 to 5.02 mya), both events during the Pliocene. We dated the split of P. hooperi during the Pliocene at ca. 3.98 mya (95 % HPD: 3.57 to 4.47 mya), following the split from P. crinitus at ca. 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. 5.32 mya (95 % HPD: 4.85 to 5.98 mya), and the origin of P. crinitus at ca. 4.62 mya (95 % HPD: 4.05 to 5.28 mya), using mitogenomes. Our results also show that the Peromyscus hooperi, crinitus, maniculatus, and leucopus species groups were among the first to diverge within the genus Peromyscus (Figure 3), followed by the Peromyscus megalops, mexicanus, melanophrys, boylii, aztecus, and truei species groups, together with Neotomodon, Podomys, and Habromys. Based on our results and those of previous studies (e. g.,Hibbard 1968; Riddle et al. 2000; Dawson 2005; Castañeda-Rico et al. 2014, 2022; Platt et al. 2015; Sawyer et al. 2017; León-Tapia et al. 2021), we suggest the Pliocene and Pleistocene as the time when speciation and diversification events took place within peromyscines, potentially associated with climatic cycles related to numerous vicariant and dispersal events.

Previous phylogenetic studies of the genus Peromyscus that analyzed single or few genes, provided older divergence times estimations (e. g.,Castañeda-Rico et al. 2014; Platt et al. 2015; Cornejo-Latorre et al. 2017; Bradley et al. 2019). For example, Platt et al. (2015), using Cytb, estimated the origin of Peromyscus and its diversification, during the Miocene, at approximately 8 mya and 5.71 mya, respectively; and the divergence of P. hooperi at ca. 5.2 mya, during the early Pliocene. However, estimates of the time to the most recent common ancestor (TMRCA) calculated from individual or few genes can be overestimated (Duchêne et al. 2011).

The evolutionary uniqueness of P. hooperi is supported by our results and previous studies by Fuller et al. (1984) and Schmidly et al. (1985) who found that this species does not fit well with either of the subgenera Haplomylomys or Peromyscus. We hypothesize that P. hooperi will remain the sole member of the Peromyscus hooperi group as first proposed by Schmidly et al. (1985) and later supported by Carleton (1989) based on the morphological, karyotypic, and allozyme evidence.

The genetic and morphological uniqueness of P. hooperi, as well as its restricted distribution to grassland transition zones should make this a species of special concern for conservation. In addition, Schmidly et al. (1985) stated that P. hooperi is a relictual, monotypic species without close living relatives, and its survival is jeopardized/threatened by the fragile conditions of its habitat in central Coahuila as a result of overgrazing. During the last 21 years, habitat shifts from native grasslands to crops zones have increased with agricultural intensification, grain-fed cattle feedlots, and new land use policies in the Mexican states of Durango, Sinaloa, Chihuahua, Nuevo León, and particularly Coahuila where P. hooperi is mostly distributed (Galván-Miyoshi et al. 2015; Bonilla-Moheno and Aide 2020). We recommend that future studies conduct population genetic analyses to determine the genetic diversity and structure of the different populations of P. hooperi. This species remains poorly known and potentially threatened by habitat loss, therefore new information is needed to determine an appropriate conservation strategy and category.

Acknowledgements

We wish to specially thank the specimen collectors, collection managers, curators and all museum staff of the Smithsonian Institution’s National Museum of Natural History (NMNH) that granted the destructive sampling of the Peromyscus hooperi museum specimen; and the Museum of Texas Tech University (TTU), the University of Michigan Museum of Zoology (UMMZ), and the Museo de Zoología “Alfonso L. Herrera”, Facultad de Ciencias, UNAM (MZFC) that granted previous sample loans. We also would like to thank the Associate Editor and two anonymous reviewers that provided comments that greatly improved the quality of this manuscript.

This manuscript is dedicated to Dr. Alfred L. Gardner (Al) for his significant contributions to the field Mammalogy through his numerous publications, research, and teachings, especially for the long-lasting impact that he has made on Mexican Mammalogy. We sincerely thank him for his invaluable help and enthusiasm to support students, researchers, and colleagues not only from Latin America but from all around the world.

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0Associated editor: Jake Esselstyn and Giovani Hernández Canchola

Appendix 1

Specimens examined in this study using Cytb gene. We show the name of the species, reference (the study from which the sequences were obtained or reanalyzed), and GenBank accession number. 

Species Study Mitogenome (GenBank number) Cytb (GenBank number)
Onychomys leucogaster Castañeda-Rico et al. (2020) KU168563 (To extract Cytb)
Habromys ixtlani Sullivan et al. (2017) KY707304 (To extract Cytb)
Isthmomys pirrensis Sullivan et al. (2017) KY707312 (To extract Cytb)
Neotoma mexicana Sullivan et al. (2017) KY707300 (To extract Cytb)
Neotomodon alstoni Sullivan et al. (2017) KY707310 (To extract Cytb)
Peromyscus attwateri Sullivan et al. (2017) KY707299 (To extract Cytb)
Peromyscus aztecus Sullivan et al. (2017) KY707306 (To extract Cytb)
Peromyscus crinitus Sullivan et al. (2017) KY707308 (To extract Cytb)
Peromyscus megalops Sullivan et al. (2017) KY707305 (To extract Cytb)
Peromyscus mexicanus Sullivan et al. (2017) KY707303 (To extract Cytb)
Peromyscus pectoralis Sullivan et al. (2017) KY707309 (To extract Cytb)
Peromyscus polionotus Sullivan et al. (2017) KY707301 (To extract Cytb)
Podomys floridanus Sullivan et al. (2017) KY707302 (To extract Cytb)
Reithrodontomys mexicanus Sullivan et al. (2017) KY707307 (To extract Cytb)
Sigmodon hispidus Sullivan et al. (2017) KY707311 (To extract Cytb)
Baiomys taylori Bradley et al. (2007) AF548469
Habromys ixtlani Bradley et al. (2007) DQ861395 DQ000482
Habromys ixtlani Bradley et al. (2007) DQ973099
Isthmomys pirrensis Bradley et al. (2007) DQ836299
Megadontomys cryophilus Bradley et al. (2007) DQ861373
Megadontomys thomasi Bradley et al. (2007) AY195795
Neotoma mexicana Bradley et al. (2007) AF294345
Neotomodon alstoni Bradley et al. (2007) AY195796 AY195797 DQ861374
Nyctomys sumichrasti Bradley et al. (2007) AY195801
Ochrotomys nuttalli Bradley et al. (2007) AY195798
Onychomys arenicola Bradley et al. (2007) AY195793
Oryzomys palustris Bradley et al. (2007) DQ185382
Osgoodomys banderanus Bradley et al. (2007) AF155383 DQ000473
Ototylomys phyllotis Bradley et al. (2007) AY009789
Peromyscus attwateri Bradley et al. (2007) AF155384 AF155385
Peromyscus aztecus Bradley et al. (2007) U89968
Peromycus beatae Bradley et al. (2007) AF131921 AF131922 AF131914
Peromyscus boylii Bradley et al. (2007) AF155386 AF155392 AF155388
Peromyscus californicus Bradley et al. (2007) AF155393
Peromyscus crinitus Bradley et al. (2007) AY376413 DQ861378
Peromyscus crinitus Bradley et al. (2007) EF028168
Peromyscus difficilis Bradley et al. (2007) AY376419 AY376415 AY387488
Peromyscus eremicus Bradley et al. (2007) AY195799 AY322503
Peromyscus eremicus Bradley et al. (2007) DQ973100
Peromyscus evides Bradley et al. (2007) U89970
Peromyscus furvus Bradley et al. (2007) AF271032 AF271012 AF271005
Peromycus gossypinus Bradley et al. (2007) DQ973101 DQ973102
Peromyscus gratus Bradley et al. (2007) AY322507 AY376421 AY376422
Peromyscus guatemalensis Bradley et al. (2007) EF028171 EF028172
Peromyscus gymnotis Bradley et al. (2007) EF028169 EF028170 EF028169
Peromyscus hooperi Bradley et al. (2007) DQ973103
Peromyscus hylocetes Bradley et al. (2007) U89976 DQ000481
Peromyscus keeni Bradley et al. (2007) X89787 AF119261
Peromyscus leucopus Bradley et al. (2007) AF131926 DQ000483
Peromyscus leucopus Bradley et al. (2007) DQ973104
Peromyscus levipes Bradley et al. (2007) AF131928 AY322509 AF155396
Peromyscus madrensis Bradley et al. (2007) AF155397
Peromyscus maniculatus Bradley et al. (2007) DQ000484 AY322508
Peromyscus maniculatus Bradley et al. (2007) DQ973111
Peromyscus mayensis Bradley et al. (2007) DQ836300 DQ836301
Peromyscus megalops Bradley et al. (2007) DQ000475
Peromyscus melanocarpus Bradley et al. (2007) EF028173
Peromyscus melanophrys Bradley et al. (2007) AY322510 AY376424
Peromyscus melanophrys Bradley et al. (2007) DQ973105
Peromyscus melanotis Bradley et al. (2007) AF155398
Peromyscus mexicanus Bradley et al. (2007) AY376425
Peromyscus mexicanus Bradley et al. (2007) EF028174
Peromyscus nasutus Bradley et al. (2007) AF155399 AY376426
Peromyscus nudipes Bradley et al. (2007) AY041200
Peromyscus oaxacensis Bradley et al. (2007) U89972
Peromyscus ochraventer Bradley et al. (2007) DQ973106
Peromyscus pectoralis Bradley et al. (2007) AF155400 AY322511 AY376427
Peromyscus perfulvus Bradley et al. (2007) DQ000474
Peromyscus polionotus Bradley et al. (2007) X89792
Peromyscus polius Bradley et al. (2007) AF155403
Peromyscus sagax Bradley et al. (2007) AF155404
Peromyscus schmidlyi Bradley et al. (2007) AY322520 AF155405 AY370610
Peromyscus simulus Bradley et al. (2007) AF131927
Peromyscus spicilegus Bradley et al. (2007) AY322512 DQ000480
Peromyscus spicilegus Bradley et al. (2007) DQ973107
Peromyscus stephani Bradley et al. (2007) AF155411
Peromyscus stirtoni Bradley et al. (2007) DQ973108
Peromyscus truei Bradley et al. (2007) AY376433 AF108703 AY376428
Peromyscus winkelmanni Bradley et al. (2007) AF131930 U89983
Peromyscus zarhynchus Bradley et al. (2007) AY195800
Podomys floridanus Bradley et al. (2007) DQ973109 DQ973110
Reithrodontomys megalotis Bradley et al. (2007) AF176248
Reithrodontomys mexicanus Bradley et al. (2007) AY859447
Sigmodon hispidus Bradley et al. (2007) AF155420
Tylomys nudicaudatus Bradley et al. (2007) AF307839
Isthmomys pirrensis Platt II et al. (2015) FJ214681
Peromyscus crinitus Platt II et al. (2015) FJ214684
Peromyscus eremicus Platt II et al. (2015) AY322503
Peromyscus evides Platt II et al. (2015) FJ214685
Peromyscus levipes Platt II et al. (2015) DQ000477
Peromyscus mexicanus Platt II et al. (2015) JX910118
Peromyscus nudipes Platt II et al. (2015) FJ214687
Peromyscus ochraventer Platt II et al. (2015) JX910119
Peromyscus spicilegus Platt II et al. (2015) FJ214669
Reithrodontomys fulvescens Platt II et al. (2015) AF176257
Reithrodontomys sumichrasti Platt II et al. (2015) AF176256
Reithrodontomys mexicanus Platt II et al. (2015) AY859453

Appendix 2

Comparison of C  T terminal deamination patters of Peromyscus hooperi (USNM 79619).

Appendix 3

Bayesian phylogenetic tree based on mtDNA Cytb sequence data. Nodal support is provided with posterior probability values. The blue block highlights the phylogenetic position of Peromyscus hooperi.

Received: September 12, 2022; Revised: October 25, 2022; Accepted: November 30, 2022

*Corresponding author: https://orcid.org/0000-0002-4301-3579

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