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MOLECULAR PHYLOGENETICS OF WESTERN DEER MICE (PEROMYSCUS): TAXONOMIC AND BIOGEOGRAPHIC IMPLICATIONS.

The genus Peromyscus comprises over 50 species of native small mammals with a composite distribution spanning virtually all of North America. Of the 13 recognized groups in the genus (Carleton, 1989), none is more widely distributed or extensively studied than the Peromyscus maniculatus species group. As currently recognized, the P. maniculatus group contains five species, with P. maniculatus being the most common and having the largest distribution (from the Atlantic to Pacific seaboards and from the Canadian taiga through central Mexico [Hall, 1981]). Each of the other four species is peripherally distributed, with Peromyscus polionotus inhabiting sandy soils in the southeastern United States, Peromyscus melanotis occurring at higher elevations in southeastern Arizona and central Mexico, Peromyscus keeni (Hogan et al., 1993) populating the coastal deciduous forests of the Pacific Northwest, and Peromyscus sejugis restricted to Santa Cruz and San Diego Islands in the Gulf of California and considered threatened by the Government of Mexico (Alvarez-Castafieda, 2001; Secretaria de Medio Ambiente y Recursos Naturales [SEMARNAT], 2010).

Monophyly of the P. maniculatus group and the systematic relationships of P. maniculatus, P. polionotus, and P. melanotis have been well resolved based on morphologic, cytogenetic, and molecular data (reviewed by Chirhart et al., 2005). However, the phylogenetie relationships and phylogeographie history of P. sejugis and P. keeni remain problematic. Allozymic (Avise et al., 1979) and cytogenetic data (Gunn and Greenbaum, 1986; Smith et al., 2000) clearly associate P. keeni and P. sejugis with P. maniculatus, but the divergence of these species was apparently too recent for the evolution of synapomorphies in these characters, thus yielding an unresolved trichotomy explainable by alternative phylogenetic hypotheses. Preliminary data comparing variation at the ND3-ND4L-ND4 region of the mitochondrial genome (Hogan et al., 1997) and at 12 microsatellite loci (Chirhart et al., 2005) suggest that P. sejugis and P. keeni shared a common, coastally distributed ancestor after divergence from a P. maniculatus stock. The corresponding "ancestral continuity" hypothesis (Chirhart et al., 2005) suggests that the distinction and current distributions of P. sejugis and P. keeni resulted from the extinction of their common ancestor from the intervening geographic area. Alternatively, P. keeni and P. sejugis may have speciated as independent peripheral isolates from a P. maniculatus stock, with their genetic similarities reflecting coincidental founder effects and genetic drift-based retention of ancestral character states rather than a true sister-group relationship. Further confounding this situation, molecular data (Hogan et al., 1997; Dragoo et al., 2006; Walker et al., 2006) associate populations of P. maniculatus from Baja California with P. sejugis rather than with those of P. maniculatus from the central and northern United States. These data suggest that western P. maniculatus as currently recognized circumscribes more than one evolutionarily distinct species.

The current taxonomy of P. maniculatus (Hall, 1981) recognizes four widespread mainland subspecies in the Baja California-California region (Fig. 1). Peromyscus maniculatus coolidgei is restricted to the southern Baja California peninsula whereas the other three subspecies are more-broadly distributed. The collective distributions of Peromyscus maniculatus sonoriensis and Peromyscus maniculatus gambelii include the northern peninsula of Baja California, southern California, central Oregon, and south-central Washington. Peromyscus maniculatus rubidus is strictly coastal and ranges from the northern boundary of the San Francisco Bay to the Oregon-Washington border. Neither variation in karyotypes nor allozymes (Calhoun et al., 1988) distinguished these subspecies as distinct lineages, and analysis of mtDNA restriction fragment length polymorphisms (Lansman et al., 1983) also provided insufficient evidence concerning the validity of the currently recognized subspecies of westernmost deer mice. Whereas each of these character sets is prone to underestimating genomic divergence, sequence variation across the ND3-ND4L-ND4 region has proven to reflect recent evolutionary events within the P. maniculatus species group. Sequence variation across the ND3-ND4L-ND5 region of the mtDNA has been documented to be entirely concordant with chromosomal, allozymic, and morphological differences in establishing the recognition of P. keeni as specifically distinct from sympatric populations of P. maniculatus (Allard and Greenbaum, 1988; Hogan et al., 1997; Chirhart et al., 2001). Analysis of a broad geographic sampling of sequence variation associated with this region of the mitochondrial genome should therefore be expected to reveal otherwise cryptic evolutionary divisions within westernmost P. maniculatus and potentially elucidate the geographically unexpected genetic similarity of P. sejugis (and the P. maniculatus from Baja California) and P. keeni.

This study was designed to: 1) identify the approximate geographic boundary of the Baja California-P sejugis genetic association; 2) determine the relationship of the Baja California-P sejugis association to northwestern and central P. maniculatus and to P. keeni; and 3) assess the intraspecific taxonomy of P. maniculatus along westernmost North America. To yield this improved understanding of the partitioning of biodiversity among deer mice in this region, we obtained sequences of the ND3-ND4L-ND4 region (1, 439 base pairs [bp]) of the mitochondrial genome for P. maniculatus from California, Oregon, and Washington (Fig. 1) and compared them to reference sequences for P. keeni, P. sejugis, and P. maniculatus from Baja California (P. m. gambelii and P. m. coolidgei), Colorado (Peromyscus maniculatus rufinus), and Washington (Peromyscus maniculatus austerus).

Materials and Methods-Sample Collection-We obtained P maniculatus from the following collecting sites; to reflect geographic proximity, collecting sites within an approximately 5-mi radius of each other were combined into single localities (Fig. 1). California: (locality 1) San Diego County (Co.), Camp Pendleton (n = 22); (locality 2) San Bernadino Co., 2.1 mi S Boulder Bay (n = 3); 6 mi S, 3 mi E Big Bear City (n = 7); Heart Bar Campground (n = 18); (locality 3) Madera Co., 25 mi N, 4 mi E Fresno (n = 22); (locality 4) Kern Co., 9 mi NNE Johannesburg (n = 5); (locality 5) Humboldt Co., 8 mi E Arcata (n = 11); Oregon: (locality 6) Benton Co., 9 mi E Alsea (n = 13); (locality 7) Harney Co., 28 mi S, 6 mi E Burns (n = 6); and Washington: (locality 8) Gray's Harbor Co., 3 mi N, 1 mi E Grisdale, Satsop Work Camp (n = 43); (locality 9) Okanogan Co., Varden Creek, 7.8 mi W Mazama (n = 24). Specimens from localities 1-7 were collected in 1979 and those from localities 8 and 9 were collected in 1984.

Reference sequences were obtained from GenBank for P. sejugis (both Santa Cruz and San Diego islands; GenBank accession numbers U40253.1, U40255.1), P. keeni (U40062.1, U40063.1), P. m. rufinus (U40250), P. m. austerus (U40249), P. m. coolidgei (U40251.1), and P. m. gambelii (DQ077697) from Baja California, Mexico. These sequences represent either the most common or sole haplotype reported in one of several studies (Hogan et al., 1997; Chirhart et al., 2001; Walker et al., 2006).

DNA Isolation, Polymerase Chain Reaction (PCR), and Sequencing-The method of Sambrook et al. (1989) was used to isolate genomic DNA from frozen (-80[degrees]C) liver or spleen tissues. Amplification with PCR and sequencing of the 1, 439-bp fragment of the mitochondrial ND3-ND4L-ND4 genes, as well as tRN[A.sup.Arg] and the 3' end of tRN[A.sup.Gly], generally followed the techniques of Arevalo et al. (1994). The primers used for PCR amplification and sequencing included PI', Marg, ND4L, and Nap2 (Arevalo et al., 1994). Amplification reactions were conducted with the following reagents and concentrations: 1 [micro]L DNA (approximately 100 ng), 12.3 [micro]L [H.sub.2]O, 2.5 [micro]L of 10X PCR Buffer II (PE Applied Biosystems, Foster City, California), 2.5 [micro]L of 25 mM Mg[Cl.sub.2], 0.5 [micro]L BSA, 4 [micro]L of 8 mM dNTPs (Amersham Pharmacia Biotech, Piscataway, New Jersey), 1.0 [micro]L (of a 10 [micro]M stock) of both forward and reverse primers, and 0.2 [micro]L Taq (Takara, Japan). Amplifications proceeded in three stages including an initial denaturation cycle at 95[degrees]C for 5 min followed by 35 cycles of 1 min each at 95[degrees]C, 50[degrees]C, and 72[degrees]C and concluded with an extension cycle of 10 min at 72[degrees]C. The ExoSap-IT procedure (ExoSAP, US Biochemical, Cleveland, Ohio) was used to remove excess primers and nucleotides from PCR amplification products.

Each sequencing reaction was performed with a Big Dye sequencing kit (PE Applied Biosystems) following the manufacturer's protocol, and sequences were obtained on an Applied Biosystems 377 automated sequencer. Fragments were sequenced in both directions; sequence alignments and the formation of contigs were conducted using the program Sequencher 4.1.1 (Gene Codes Corporation, Ann Arbor, MI). Each unique sequence was scored as an individual haplotype.

Distance Analyses-Uncorrected p-distances (PAUP* version 4.0b10; Swofford, 2002) were obtained to estimate the percent sequence divergences of the haplotypes among individuals from within collecting localities and the mean divergences for all pairs of haplotypes between the localities and to the reference samples.

Phylogenetic Analyses-Phylogenetic analyses with maximum parsimony (MP) and maximum likelihood (ML) were conducted in PAUP* (Swofford, 2002). Bayesian inference (BI) was performed in MrBayes version 3.2 (Ronquist et al., 2012). For the ML and BI analyses, MODELTEST 3.06 (Posada and Crandall, 1998) was used to select the DNA substitution model based on the Akaike Information Criterion. The model selected for these analyses was TVM+I+G. A corresponding sequence of P. melanotis (Hogan et al., 1997; Chirhart et al., 2001) from Hidalgo, Mexico (GenBank accession number U40247) was used as the outgroup for all analyses.

A heuristic search with tree bisection and reconnection branch swapping, 10 random additions, and the parameters provided for the TVM+I+G was used for the ML analysis. The branch and bound option with 1, 000 bootstraps was used for both MP and ML (TVM+I+G model). We used BI to calculate posterior probabilities. Two separate runs were performed, each consisting of four chains (1 cold and 3 hot), 1 million generations sampled every 1, 000 generations, and a 25% burn-in. The standard of split frequencies was below 0.01 and values of the potential scale reduction factor were either 1.0 or close to 1.0. Chain convergence was also checked with TRACER version 1.5 (http://tree.bio.ed.ac.uk/software/tracer).

Results-Haplotype Distributions-The nine populations sampled exhibited a total of 36 different haplotypes (Table 1). Eighteen of these occurred only within and among populations of P. maniculatus gambelii (localities 1-3). Fifteen of these haplotypes were unique to a single locality whereas one haplotype was shared among all three of these localities and two others were present at localities 2 and 3. Of the 18 haplotypes distributed within and among localities representing P. m. austerus (locality 8), Peromyscus maniculatus artemisiae (locality 9), P. m. rubidus (localities 5 and 6), and P. m. sonoriensis (localities 4 and 7), two were shared between two localities; the rest occurred at single localities only.

Sequence Divergence-Sequence divergence, as represented by uncorrected pairwise P-values, among individuals within collecting localities was low and ranged from 0.0008 to 0.0098. Corresponding mean divergences computed for all pairs of haplotypes between localities and to the reference samples are reported in Table 2. The haplotype for P. melanotis was essentially equidistant (mean = 0.073 [+ or -] 0.003) from those of P. keeni, P. sejugis, and all P. maniculatus sampled. All of the remaining Pvalues, however, indicate that deer mice from Southern California (Table 2 localities 1-3, representing P. maniculatus gambelii) are genetically associated with the reference specimens from Baja California (P. m. coolidgei and P. m. gambelii). Alternatively, the deer mice from eastern and northwestern California, Oregon, and Washington (Table 2 localities 4-9, representing the P. maniculatus subspecies austerus, artemisiae, rubidus, and sonoriensis) are associated with the reference samples from central (P. m. rufinus, Colorado) and northwestern P. maniculatus (P. m. austerus from Washington). The mean sequence divergence between these two assemblages was 0.037 [+ or -] 0.002 whereas that among the gambelii and coolidgei haplotypes was 0.008 - 0.008 and that among the austerus, artemisiae, rubidus, and sonoriensis haplotypes was 0.009 [+ or -] 0.002. The P. keeni haplotypes were slightly more similar to those of gambelii and coolidgei (0.038 - 0.001) than to those of austerus, artemisiae, rubidus, and sonoriensis (0.044 [+ or -] 0.002).

Phylogenetics-Due to the large number of haplotypes and the small sequence divergences among the haplotypes, only a Bayesian analysis was employed for the entire (per-haplotype) data set. Two major clades supported by posterior probabilities of 1.00 and 0.97, respectively (Fig. 2), were identified. One contained the P. maniculatus reference haplotypes (P. m. austerus and P. m. rufinus) as well as the haplotypes from localities 4-9 representing P. m. austerus, P. m. artemisiae, P. m. rubidus, and P. m. sonoriensis (western and northern Washington, eastern and western Oregon, and northern and eastern California). The other major clade included the reference samples of P. maniculatus from Baja California (P. m. gambelii and P. m. coolidgei), both island samples of P. sejugis, and localities 1-3 from Southern California. Except for the two samples of P. sejugis, there was little geographic structure within either of the two major clades. Placement of the reference haplotypes of P. keeni was more equivocal and appeared as very weakly associated with the Southern California-Baja California-P. sejugis clade.

Based on the minimal sequence divergences among the haplotypes within localities and the results of the phylogenetic analysis for the entire data set, we created a truncated data set to enable more-extensive phylogenetic analyses. This data set included a single, randomly chosen haplotype for each of the localities and the reference haplotypes. The BI and MP analyses of the truncated data set yielded the same topology (Fig. 3) as did the analysis for the entire data set, with the same two highly supported major clades and P. keeni weakly associated with the Southern and Baja California-P sejugis clade. The ML analysis of the truncated data set (not shown) differed only by placing P. keeni as an unsupported trichotomy relative to the two, well-supported major clades.

Discussion-Previous studies have suggested that the deer mice from Baja California or Southern California (or both) are genetically distinct from all other populations of P. maniculatus (as recognized by Musser and Carleton, 2005). A survey of mtDNA restriction fragment length polymorphisms (Lansman et al., 1983) identified a deer mouse assemblage from Southern California united by a set of closely related haplotypes that were distantly related to 47 other haplotypes for P. maniculatus from central and northwestern North America. Hogan et al. (1997) found that the ND3-ND4L-ND4 mtDNA sequence of a reference specimen (P. m. coolidgei) from Baja California del Sur was more-closely related to P. sejugis and P. keeni than to subspecies of P. maniculatus (P. m. austerus from Vancouver Island and P. m. rufinus from Colorado). Analyses of complete cytochrome b gene sequences (Dragoo et al., 2006; Gering et al., 2009; Kalkvik et al., 2012) also placed deer mice from Southern and Baja California in a clade with P. keeni, thus leading Dragoo et al. (2006) to suggest that these populations of P. maniculatus represent a distinct species.

In combination with ND3-ND4L-ND4 sequence data for eight populations of deer mice from Baja California (Walker et al., 2006), the analyses presented here confirm the genetic distinction of the populations of deer mice from Southern and Baja California and support their specific distinction from P. maniculatus. The mean genetic distance to P. keeni was essentially identical (0.037 and 0.038, respectively) for the Southern and Baja California deer mice (P. m. gambelii and P. m. coolidgei) and for those from eastern and northwestern California, oregon, Washington, and Colorado (P. m. austerus, artemisiae, rubidus, rufinus, and sonoriensis, respectively). Despite the small genetic distance between P. keeni and P. maniculatus, Allard and Greenbaum (1988) and Hogan et al. (1993) documented morphological and nonoverlapping chromosomal distinction at multiple localities of sympatry. All of the phylogenetic analyses recovered the Southern and Baja California haplotypes as a highly supported clade separate from the other P. maniculatus and P. keeni.

Our data indicate that the northern boundary of the Southern-Baja California clade resides in the region between localities 3 and 5 (Fig. 1) and is likely coincident with the San Francisco Bay and the associated Sacramento and San Joaquin River drainages. These physiographic features mark an abrupt transition in the climate and altitude of coastal California and discontinuous distributions of numerous genera and species of rodents (Hooper, 1944) and other terrestrial vertebrates (Wake, 1997; Rodriguez-Robles et al., 1999; Maldonado et al., 2001; Feldman and Spicer, 2002; Matocq, 2002; Ernest et al., 2003). Morphologic distinction between P. m. gambelii (from south of the San Francisco Bay) and P. m. rubidus (from north of the San Francisco Bay) also corresponds to this geographic divide (Hooper, 1944), and Kalkvik et al. (2012) found that the deer mice from Southern and Baja California occupy a significantly different environmental space than do those from north of the San Francisco Bay. The eastern boundary of the Southern-Baja California clade is likely coincident with the Sierra Nevada Mountains. Considering all of the available data (Hooper, 1944; Landsman et al., 1983; Hogan et al., 1986; Dragoo et al., 2006; Walker et al., 2006; Kalkvik et al., 2012, this study), the phylogenetic species concept, and taxonomic priority, we recommend that the deer mouse assemblage including all populations of P. m. coolidgei and those of P. m. gambelii from south of the San Francisco Bay and west of the Sierra Nevada mountains, be recognized as Peromyscus gambelii.

Retention of the specific distinction of P. sejugis relative to the deer mice from Baja California was extensively considered by Walker et al. (2006). Despite the low level of mtDNA divergence between P. sejugis and the deer mice from Southern and Baja California (Table 2 and Walker et al., 2006), the two populations of P. sejugis are morphologically and genetically distinct from mainland deer mice. The original description of the species (Burt, 1932) characterized P. sejugis as being larger than P. maniculatus from the Baja Peninsula, and both populations of P. sejugis differ from mainland deer mice by fixation of a unique inversion of chromosome 13 (Smith et al., 2000). In addition, P. sejugis displays distinct mtDNA haplotypes (Walker et al., 2006) and allele frequency differences at three microsatellite loci, with one being fixed for a unique allele (Chirhart et al., 2005); both the mtDNA and microsatellite analyses recover the two populations of P. sejugis as a unique and highly supported clade. Given its genetic and morphological distinctness, insular allopatry, and threatened status, we agree with Walker et al. (2006) that P. sejugis is best considered to retain its specific recognition.

Our recommendations engender three unresolved distributional-taxonomic questions relative to the westernmost deer mice. The northern boundary of P. gambelii needs to be confirmed and precisely located. Additionally, as the distribution of P. m. gambelii from north of the San Francisco Bay and the Sacramento and San Joaquin River drainages (Fig. 1) has not been critically examined, it is not clear to which clade (species and subspecies) these populations belong. And because the Sierra Nevada Mountains diminish in extreme southern California, it is not known if the Southern-Baja California clade (P. gambelii) extends into northeastern-most Baja California and southwestern Arizona (into the range of P. m. sonoriensis; Fig. 1). Resolving these issues will require targeted sampling and comparative analyses of populations in the respective geographic regions.

Both the ancestral continuity and independent peripheral isolate hypotheses for the origin of P. keeni and P. gambelii-P. sejugis are consistent with isolation and subsequent diversification associated with Pleistocene glaciation, and the genetic data are consistent with such a recent divergence. However, a distinct signal of sister-group relationship would be expected had these two lineages shared a history of common ancestry after divergence from a P. maniculatus central stock. While our BI and MP analyses are consistent with previous reports (Hogan et al., 1997; Chirhart et al., 2005; Dragoo et al., 2006; Gering et al., 2009; Kalkvik et al., 2012) that cluster P. keeni with the deer mice from Southern and Baja California, support for this association is weak (Figs. 2 and 3) and the ML analysis leaves P. keeni as an unresolved trichotomy relative to P. maniculatus and the P. gambelii-P. sejugis clade. We interpret this ambiguous result as more consistent with the expectations of coincidental founder effects and with genetic drift in independent peripheral isolation as the explanation for the origin of the P. keeni and P. gambelii/P. sejugis clades.

This work was supported by National Institutes of General Medical Sciences grant GM 27014 (to IFG), National Science Foundation grant DEB 9615163 (to RLH), and Texas A&M University Faculty minigrant FMG 99-054. Various former undergraduate and graduate students assisted in the animal and tissue collection. Tissues for the mice from San Diego County were kindly provided by Adam Richman. We thank J. Hayes, Eric Schall, and Lindsey Virdell for laboratory assistance and Jessica Light for logistical assistance and helpful comments on the manuscript. The sequence data constituted a portion of the Ph.D. dissertation of MLW. The animal use in this research was conducted in accordance with the Guide for Care and Use of Laboratory Animals (U.S. National Research Council, 2011) as approved in Texas A&M University animal use protocols 92-1054 and 2000-275.

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Submitted 25 October 2016. Accepted 24 April 2017.

Associate Editor was Celia Lopez-Gonzalez

Ira F. Greenbaum, * Scott E. Chirhart, Mindy L. Walker, Rodney L. Honeycutt

Department of Biology, Texas A&M University, College Station, TX 77843-3258 (IFG, SEC, MLW)

Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, 77843-3258 (RLH)

Present address of SEC: Department of Biology, Centenary College of Louisiana, 2911 Centenary Boulevard, Shreveport, LA 71134

Present address of MLW: Department of Environmental Science, University of Evansville, 1800 Lincoln Avenue, Evansville, IN 47714

Present address of RLH: Natural Science Division, Pepperdine University, Malibu, CA 90263

* Correspondent: i-greenbaum@tamu.edu

Caption: Fig. 1-Map showing the locations of the populations sampled in this study for genetic analyses and the ranges of the respective subspecies of P. maniculatus (based on Hall 1981). Specific collection localities and collection dates are listed in text.

Caption: Fig. 2-Bayesian tree for for species/subspecies of Peromyscus using the entire data set (ND3-ND4L-ND4, 1, 439 base pairs) analyzed in this study. Numbers at the tips are collection localities. Numbers above the branches are the respective posterior probabilities; branches without numbers had posterior probabilities less than 0.90. Specific collection localities and collection dates are listed in text.

Caption: Fig. 3-Bayesian-MP tree for Peromyscus samples using the truncated data set (single randomly chosen haplotype for each of the localities and the reference haplotypes). Numbers at the tips are localities. Numbers above the branches are the respective posterior probabilities and bootstrap values; branches without numbers had posterior probabilities less than 0.90, bootstrap values less than 90, or both. Specific collection localities and collection dates are listed in text.
Table 1--Frequency distribution of haplotypes (listed by
GenBank Accession number) recovered from deer mice at the
localities sampled in this study. Specific collection localities and
collection dates are listed in text.

Haplotype    1      2      3      4     5

KC764374    0.18
KC764375    0.05
KC764376    0.14
KC764377    0.41   0.18   0.27
KC764378    0.05
KC764379    0.09
KC764380    0.04
KC764381           0.03
KC764382           0.07
KC764383           0.03
KC764384           0.03
KC764385           0.11
KC764386           0.07
KC764387           0.11
KC764388           0.11
KC764389           0.14   0.09
KC764390           0.11   0.36
KC764391                  0.27
KC764392                         0.2
KC764393                         0.8
KC764394                               0.64
KC764395                               0.36
KC764396
KC764397
KC764398
KC764399
KC764400
KC764401
KC764402
KC764403
KC764404
KC764405
KC764406
KC764407
KC764408
KC764409

Haplotype    6      7      8      9

KC764374
KC764375
KC764376
KC764377
KC764378
KC764379
KC764380
KC764381
KC764382
KC764383
KC764384
KC764385
KC764386
KC764387
KC764388
KC764389
KC764390
KC764391
KC764392
KC764393
KC764394                         0.17
KC764395           0.17
KC764396    0.46
KC764397    0.15
KC764398    0.08
KC764399    0.31
KC764400           0.5
KC764401           0.33
KC764402                  0.42
KC764403                  0.58
KC764404                         0.08
KC764405                         0.25
KC764406                         0.04
KC764407                         0.17
KC764408                         0.21
KC764409                         0.08

Table 2--Mean percent sequence divergences (uncorrected
p-distances) between the haplotypes of the deer mice for the reference
samples (A-E) and to those from each of the localities. C-N refers
to reference deer mice from Colorado and Washington (P. m. austerus
and P. m. rufinus) and Baja refers to references deer mice from Baja
California (P. m. gambelii and P. m. coolidgei). Specific collection
localities and collection dates are listed in text.

                                  A       B       C       D       E

A   P. melanotis                 --
B   P. maniculatus (C-N)        0.078    --
C   P. keeni                    0.074   0.044    --
D   P. sejugis                  0.072   0.047   0.038    --
E   P. maniculatus (Baja)       0.069   0.045   0.040   0.022    --
1   San Diego Co.               0.070   0.043   0.038   0.017   0.011
2   San Bernardino Co.          0.069   0.040   0.037   0.017   0.013
3   Fresno                      0.069   0.040   0.036   0.017   0.013
4   Johannesburg                0.070   0.010   0.043   0.041   0.039
5   Arcata                      0.077   0.016   0.046   0.042   0.041
6   Alsea                       0.074   0.013   0.043   0.041   0.041
7   Burns (Oregon)              0.078   0.015   0.048   0.043   0.042
8   Satsop                      0.073   0.013   0.044   0.047   0.043
9   Varden Creek (Washington)   0.074   0.012   0.044   0.043   0.041

                                  1       2       3       4       5

A   P. melanotis
B   P. maniculatus (C-N)
C   P. keeni
D   P. sejugis
E   P. maniculatus (Baja)
1   San Diego Co.                --
2   San Bernardino Co.          0.005    --
3   Fresno                      0.004   0.004    --
4   Johannesburg                0.038   0.036   0.035    --
5   Arcata                      0.035   0.035   0.034   0.008    --
6   Alsea                       0.036   0.035   0.034   0.012   0.009
7   Burns (Oregon)              0.037   0.036   0.034   0.012   0.008
8   Satsop                      0.040   0.038   0.037   0.014   0.014
9   Varden Creek (Washington)   0.036   0.035   0.034   0.008   0.006

                                  6       7       8     9

A   P. melanotis
B   P. maniculatus (C-N)
C   P. keeni
D   P. sejugis
E   P. maniculatus (Baja)
1   San Diego Co.
2   San Bernardino Co.
3   Fresno
4   Johannesburg
5   Arcata
6   Alsea                        --
7   Burns (Oregon)              0.011    --
8   Satsop                      0.007   0.013    --
9   Varden Creek (Washington)   0.007   0.008   0.009   --
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Author:Greenbaum, Ira F.; Chirhart, Scott E.; Walker, Mindy L.; Honeycutt, Rodney L.
Publication:Southwestern Naturalist
Geographic Code:1U900
Date:Jun 1, 2017
Words:5385
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