Morphological differentiation of Peromyscus leucopus and P. maniculatus in East Texas

Authors

  • Jessica E Light Department of Ecology and Conservation Biology, Texas A&M University. http://orcid.org/0000-0001-6462-3045
  • Lelila Siciliano-Martina Interdisciplinary Program in Ecology & Evolutionary Biology, Texas A&M University. Department of Biology, Texas State University
  • Emma Dohlanik Department of Ecology and Conservation Biology, Texas A&M University.
  • Grace Vielleux Department of Ecology and Conservation Biology, Texas A&M University
  • David Hafner Museum of Southwestern Biology, University of New Mexico
  • A Michelle Lawing Department of Ecology and Conservation Biology, Texas A&M University. Interdisciplinary Program in Ecology & Evolutionary Biology, Texas A&M University
  • Ira Greenbaum Interdisciplinary Program in Ecology & Evolutionary Biology, Texas A&M University Interdisciplinary Program in Ecology & Evolutionary Biology, Texas A&M University

Keywords:

Balcones fault zone, geometric morphometrics, species differentiation, traditional morphometrics.

Abstract

The white-footed deer mouse (Peromyscus leucopus) and the North American deer mouse (P. maniculatus) are widely distributed throughout North America, often with overlapping distributions. These species are believed to be sympatric east of the Balcones fault zone in Texas, but records from natural history collections indicate that P. maniculatus is not common from this region. Given that these two species are notoriously difficult to differentiate morphologically, it is possible that specimens have been incorrectly identified and that P. maniculatus may be rare or not present in East Texas. This study aims to determine if P. leucopus and P. maniculatus can be differentiated morphologically east of the Balcones fault zone in Texas. Cranial and external characters from genetically identified specimens representing each species were analyzed using traditional and geometric morphometric methods. Morphological analyses revealed that genetically identified specimens of P. leucopus and P. maniculatus from east of the Balcones fault zone could be differentiated using a suite of morphological characters. Many of the specimens of P. leucopus used in this study were originally misidentified, suggesting that P. maniculatus is rare in East Texas.

Author Biography

Jessica E Light, Department of Ecology and Conservation Biology, Texas A&M University.

Department of Ecology and Conservation BiologyAssociate Profssor

References

ADAMS, D. C., M. L. COLLYER, AND A. KALIONTZOPOULOU. 2020. Geomorph: Software for geometric morphometric analyses. R package version 3.2.1. https://cran.r-project.org/package=geomorph.

ADAMS, D. C., F. J. ROHLF, AND D. E. SLICE. 2004. Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 71:5–16.

AQUADRO, C. F., AND J. C. PATTON. 1980. Salivary amylase variation in Peromyscus: use in species identification. Journal of Mammalogy 61:703–707.

BEDFORD, N. L., AND H. E. HOEKSTRA. 2015. The natural history of model organisms: Peromyscus mice as a model for studying natural variation. Elife 4:e06813.

BENEDICT, B. D., A. A. CASTELLANOS, AND J. E. LIGHT. 2019. Phylogeographic assessment of the Heermann’s kangaroo rat (Dipodomys heermanni). Journal of Mammalogy 100:72–91.

BERENS, J. D. 2015. Morphological differences and diversity of small mammal species. Master’s Thesis. Department of Environmental and Conservation Sciences, North Dakota State University, U.S.A.

BERL, J. L., E. A. FLAHERTY, B. J. DANIELSON, K. F. KELLNER, AND R. K. SWIHART. 2017. Winter ecology of prairie deer mice (Peromyscus maniculatus bairdii) in cultivated habitats: Implications for agricultural ecosystem services. Agriculture, Ecosystems & Environment 249:130–136.

BRADLEY, R. D., J. Q. FRANCES. R. N. PLATT II, T. J. SONIAT, D. ALVAREZ, AND L. L. LINDSEY. 2019. Mitochondrial DNA sequence data indicate evidence for multiple species within Peromyscus maniculatus. Special Publications of the Museum of Texas Tech University 70:1–59.

BRENO, M., H. LEIRS, AND S. VAN DONGEN. 2011. Traditional and geometric morphometrics for studying skull morphology during grown in Mastomys natalensis (Rodentia: Muridae). Journal of Mammalogy 92:1395–1406.

BRUSEO, J. A., S. H. VESSEY, AND J. S. GRAHAM. 1999. Discrimination between Peromyscus leucopus noveboracensis and Peromyscus maniculatus nubiterrae in the field. Acta Theriologica 44:151–160.

CAMARGO, N. F., L. F. MACHADO, A. F. MENDONCA, AND E. M. VIEIRA. 2019. Cranial shape predicts arboreal activity in Sigmodontinae rodents. Journal of Zoology 308:128–138.

CHILDS, J. E., T. G. KSIAZEK, C. F. SPIROPOULOU, J. W. KREBS, S. MORZUNOV, G. O. MAUPIN, K. L. GAGE, P. E ROLLIN, J. SARISKY, R. E ENSCORE, AND J. K. FREY. 1994. Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. Journal of Infectious Diseases 169:1271–1280.

CHOATE, J. R. 1973. Identification and recent distribution of white-footed mice (Peromyscus) in New England. Journal of Mammalogy 54:41–49.

CHOATE, J. R., R.C. DOWLER, AND J. E. KRAUS. 1979. Mensural Discrimination between Peromyscus leucopus and P. maniculatus (Rodentia) in Kansas. Southwestern Association of Naturalists Stable 24:249–258.

COOK, J. A., AND J. E. LIGHT. 2019. The emerging role of mammal collections in 21st century mammalogy. Journal of Mammalogy 100:733–750.

CROUX, C., AND G. HAESBROECK. 2000. Principal component analysis based on robust estimators of the covariance or correlation matrix: influence functions and efficiencies. Biometrika 87:603–618.

DALQUEST, W. W., AND F. B. STANGL, JR. 1983. Identification of seven species of Peromyscus from Trans-Pecos Texas by characters of the lower jaw. Occasional Papers The Museum Texas Tech University 90:1–12.

DAVIS, W. B., AND D. J. SCHMIDLY. 1994. The Mammals of Texas. Texas Parks and Wildlife Press, Austin, Texas.

DICE, L. R. 1940. Ecologic and genetic variability within species of Peromyscus. The American Naturalist 74:212–221.

DOS REIS, S. F., L. M. PESSOA, AND R. E. STRAUSS. 1990. Application of size-free canonical discriminant analysis to studies of geographic differentiation. Brazilian Journal of Genetics 13:509–520.

DRAGOO, J. W., J. A. LACKEY, K. E. MOORE, E. P. LESSA, J. A. COOK, AND T. L. YATES. 2006. Phylogeography of the deer mouse (Peromyscus maniculatus) provides a predictive framework for research on hantaviruses. Journal of General Virology 87:1997-2003.

DREBOT, M.A., I. GAVRILOVSKAYA, E. R. MACKOW, Z. CHEN, R. LINDSAY, A. J. SANCHEZ, S. T. NICHOL, AND H. ARTSOB. 2001. Genetic and serotypic characterization of Sin Nombre-like viruses in Canadian Peromyscus maniculatus mice. Virus Research 75:75–86.

FELDHAMER, G. A., J. E. GATES, AND J. H. HOWARD. 1983. Field identification of Peromyscus maniculatus and P. leucopus in Maryland: reliability of morphological characters. Acta Theriologica 27:417–423.

GEHLBACH, F. R. 1991. The east-west transition zone of terrestrial vertebrates in central Texas: a biogeographical analysis. Texas Journal of Science 43:415–427.

GERING, E. J., J. C. OPAZO, AND J. F. STORZ. 2009. Molecular evolution of cytochrome b in high- and low-altitude deer mice (genus Peromyscus). Heredity 102: 226–235.

GOULD, S. J. 1966. Allometry and size in ontogeny and phylogeny. Biological Review 41:587–640.

GREENBAUM, I. F., S. E. CHIRHART, M. L. WALKER, AND R. L. HONEYCUTT. 2017. Molecular phylogenetics of western deer mice (Peromyscus): taxonomic and biogeographic implications. The Southwestern Naturalist 62:129–137.

GREENBAUM, I. F., R. L. HONEYCUTT, AND S. E. CHIRHART. 2019. Taxonomy and phylogenetics of the Peromyscus maniculatus species group. Pp. 559–575 in From field to laboratory: a memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.). Special Publications, Museum of Texas Tech University 71:xi+1–911.

GRIECO, T. M., AND O. T. RIZK. 2010. Cranial shape varies along an elevation gradient in Gambel’s white-footed mouse (Peromyscus maniculatus gambelii) in the Grinnell Resurvey Yosemite Transect. Journal of Morphology 271:897–909.

HALL, E.R. 1981. The Mammals of North America. 2nd edition. John Wiley & Sons, Inc., New York, U.S.A.

HARNEY, B. A., AND R. D. DUESER. 1987. Vertical stratification of activity of two Peromyscus species: an experimental analysis. Ecology 68:1084–1091.

HOLMES, M. W., G. K. BOYKINS, R. C. BOWIE, AND E. A. LACEY. 2016. Cranial morphological variation in Peromyscus maniculatus over nearly a century of environmental change in three areas of California. Journal of Morphology 277:96–106.

KALKVIK, H. M., I. J. STOUT, T. J. DOONAN, AND C. L. PARKINSON. 2012. Investigating niche and lineage diversification in widely distributed taxa: phylogeography and ecological niche modeling of the Peromyscus maniculatus species group. Ecography 35:54-64.

KAMLER, J. F., D. S. PENNOCK, C. WELCH, AND R. J. PIEROTTI. 1998. Variation in morphological characteristics of the white-footed mouse (Peromyscus leucopus) and the deer mouse (P. maniculatus) under allotopic and syntopic conditions. The American Midland Naturalist 140:170–179.

KING, J. A. 1968. Biology of Peromyscus (Rodentia). Special Publication No. 2. The American Society of Mammalogists, Stillwater, Oklahoma.

KIRKLAND, G. L., AND J. N. LAYNE (eds.). 1989. Advances in the study of Peromyscus (Rodentia). Texas Tech University Press, Lubbock, Texas.

KOH, H. S., AND R. L. PETERSON. 1983. Systematic studies of deer mice, Peromyscus maniculatus Wagner (Cricetidae, Rodentia): Analysis of age and secondary sexual variation in morphometric characters. Canadian Journal of Zoology 61:2618–2628.

LARSON, S. R., X. LEE, AND S. M. PASKEWITZ. 2018. Prevalence of tick-borne pathogens in two species of Peromyscus mice common in northern Wisconsin. Journal of Medical Entomology 55:1002–1010.

LAWING, A. M., AND P.D. POLLY. 2010. Geometric morphometrics: Recent applications to the study of evolution and development. Journal of Zoology 280:1–7.

LEWARCH, C.L., AND H. E. HOEKSTRA. 2018. The evolution of nesting behaviour in Peromyscus mice. Animal Behaviour 139:103–115.

LINDQUIST, E. S., C. F. AQUADRO, D. MCCLEARN, AND K. J. MCGOWAN. 2003. Field identification of the mice Peromyscus leucopus noveboracensis and P. maniculatus gracilis in central New York. Canadian Field Naturalist 117:184–189.

LUCID, M. K. AND J. A. COOK. 2007. Cytochrome-b haplotypes suggest an undescribed Peromyscus species from the Yukon. Canadian Journal of Zoology 85:916–919.

MCLEAN, B. S., K. C. BELL, J. L. DUNNUM, B. ABRAHAMSON, J. P. COLELLA, E. R. DEARDORFF, J. A. WEBER, A. K. JONES, F. SALAZAR-MIRALLES, AND J. A. COOK. 2016. Natural history collections-based research: progress, promise, and best practices. Journal of Mammalogy 97:287–297.

MILLER, S. E., L. N. BARROW, S. M. EHLMAN, J. A. GOODHEART, S. E. GREIMAN, H. L. LUTZ, T. M. MISIEWICZ, S. M. SMITH, M. TAN, C. J. THAWLEY, J. A. COOK, AND J. E. LIGHT. 2020. Building natural history collections for the 21st century and beyond. Bioscience 70:674–687.

MILLIEN, V., R. LEDEVIN, C. BOUÉ, AND A. GONZALEZ. 2017. Rapid morphological divergence in two closely related and co-occurring species over the last 50 years. Evolutionary Ecology 31:847–64.

MUSSER, G. G., AND M. D. CARLETON. 1993. Family Muridae. In “Mammal Species of the World†(D. E. Wilson and D. M. Reeder, eds.). pp. 501-755. Smithsonian Institution Press, Washington, DC.

MYERS, P., B. L. LUNDRIGAN, B. W. GILLEPSIE, AND M. L. ZELDITCH. 1996. Phenotypic plasticity in skull and dental morphology in the prairie deer mouse (Peromyscus maniculatus bairdii). Journal of Morphology 229:229–237.

OLIVER, J., R. G. MEANS, S. KOGUT, M. PRUSINSKI, J. J. HOWARD, L. J. LAYNE, F. K. CHU, A. REDDY, L. LEE, AND D. J. WHITE. 2006. Prevalence of Borrelia burgdorferi in small mammals in New York State. Journal of Medical Entomology 43:924–935.

OSGOOD, W. H. 1909. Revision of the mice of the American genus Peromyscus. North American Fauna 28:1–285.

PALAS, J. S., O. A. SCHWARTZ, AND A. M. VIVAS. 1992. Identification of Iowa Peromyscus using external measurements and salivary amylase. Prairie Naturalist 24:273–277.

PERGAMS, O. R. W., AND M. V. ASHLEY. 1999. Rapid morphological change in Channel Island deer mice. Evolution 53:1573–1581.

PERGAMS, O. R. W., AND R. C. LACY. 2008. Rapid morphological and genetic change in Chicago-area Peromyscus. Molecular Ecology 17:450–463.

PLATT, R. N., B. R. AMMAN, M. S. KEITH, C. W. THOMPSON, AND R. D. BRADLEY. 2015. What is Peromyscus? Evidence from nuclear and mitochondrial DNA sequences suggests the need for a new classification. Journal of Mammalogy 96:708–719.

RAND, P. W., E. H. LACOMBE, R. P. SMITH JR., S. M. RICH, C. W. KILPATRICK, C. A. DRAGONI, AND D. CAPORALE. 1993. Competence of Peromyscus maniculatus (Rodentia: Cricetidae) as a reservoir host for Borrelia burgdorferi (Spirochaetares: Spirochaetaceae) in the wild. Journal of Medical Entomology 30:614–618.

R CORE TEAM. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

REED, A. W., P. K. KENNEDY, M. L. BECK, AND M. L. KENNEDY. 2004. Using morphologic characters to identify Peromyscus in sympatry. The American Midland Naturalist 152:190–195.

RICH, S. M., C. W. KILPATRICK, J. L. SHIPPEE, AND K. L. CROWELL. 1996. Morphological differentiation and identification of Peromyscus leucopus and P. maniculatus in Northeastern North America. Journal of Mammalogy 77:985–991.

RIDENHOUR, B. J., AND M. J. CRAMER. 2015. Differentiation of white-footed mice (Peromyscus leucopus) and deer mice (Peromyscus maniculatus) of the upper Midwest using PCR melt curve analysis. Conservation Genetics Resources 7:29–31.

ROHLF, F. J. 2001. TPSDig2: a program for landmark development and analysis.

ROHLF, F. J. AND L. F. MARCUS. 1993. A revolution in morphometrics. Trends in Ecology & Evolution 8:129–132.

ROHLF, F. J. AND D. SLICE. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology 39:40–59.

ROWSEY, D. M., L. R. HEANEY, AND S. A. JANSA. 2019. Tempo and mode of mandibular shape and size evolution reveal mixed support for incumbency effects in two clades of island-endemic rodents (Muridae: Murinae). Evolution 73:1411–1427.

SCHMALJOHN, A. L., D. LI, D. L. NEGLEY, D. S. BRESSLER, M. J. TURELL, G. W. KORCH, M. S. ASCHER, AND C. S. SCHMALJOHN. 1995. Isolation and initial characterization of a newfound hantavirus from California. Virology 206:963–972.

SCHMIDLY, D. J. 1983. Texas Mammals East of the Balcones Fault Zone. Texas A&M University Press, College Station, Texas.

SCHMIDLY, D. J., AND R. D. BRADLEY. 2016. The Mammals of Texas. The University of Texas Press, Austin, Texas.

SEIFERT, V. A., B. J. CLARKE, J. P. CROSSLAND, AND L. T. BEMIS. 2016. A method to distinguish morphologically similar Peromyscus species using extracellular RNA and high-resolution melt analysis. Analytical Biochemistry 508:65–72.

SLICE, D. E. 2007. Geometric morphometrics. Annual Review of Anthropology 36:261–281.

SMITH, H. M., AND H. K. BUECHNER. 1947. The influence of the Balcones Escarpment on the distribution of amphibians and reptiles in Texas. Bulletin of the Chicago Academy of Sciences 8:1–16.

SMITH, M. F., AND J. L. PATTON. 1991. Variation in mitochondrial cytochrome b sequence in natural populations in South American akodontine rodents (Muridae: Sigmodontidae). Molecular Biology and Evolution 8:85–103.

SONG, J. W., L. J. BAEK, J. W. NAGLE, D. SCHLITTER, AND R. YANAGIHARA. 1996. Genetic and phylogenetic analyses of hantaviral sequences amplified from archival tissues of deer mice (Peromyscus maniculatus nubiterrae) captured in the eastern United States. Archives of Virology 141:959–967.

STEPHENS, R. B., E. M. ANDERSON, S. R. WENDT, AND J. K. MEECE. 2014. Field identification of sympatric Peromyscus leucopus noveboracensis and P. maniculatus gracilis in Wisconsin from external characters. The American Midland Naturalist 171:139–146.

STERNBURG, J. E., AND A. FELDHAMER. 1997. Mensural discrimination between sympatric Peromyscus leucopus and Peromyscus maniculatus in southern Illinois. Acta Theriologica 42:1–13.

STROMBERG, M. R. 1979. Field identification of Peromyscus leucopus and P. maniculatus with discriminant analysis. Transactions of the Wisconsin Academy of Sciences, and Arts Letters 67:159–164.

TESSIER, N., S. NOËL, AND F. J. LAPOINTE. 2004. A new method to discriminate the deer mouse (Peromyscus maniculatus) from the white-footed mouse (Peromyscus leucopus) using species-specific primers in multiplex PCR. Canadian Journal of Zoology 82:1832–1835.

THOMPSON, T. G., AND W. CONLEY. 1983. Discrimination of coexisting species of Peromyscus in south-central New Mexico. Southwestern Naturalist 28:199–209.

VENABLES, W. N., AND RIPLEY, B. D. 2002. Modern Applied Statistics with S. Fourth Edition. Springer, New York.

WILKINSON, L. 1997. Systat 7.0 for Windows. SPSS, Inc., Chicago, Illinois.

WOLFF, J.O. 1996. Coexistence of white-footed mice and deer mice may be mediated by fluctuating environmental conditions. Oecologia 108:529–533.

ZELDITCH, M. L., D. L. SWIDERSKI, AND H. D. SHEETS. 2012. Geometric morphometrics for biologists: a primer. San Diego, CA: Elsevier Academic Press.

ZHENG, Z., B. S. ARBOGAST, AND G. J. KENAGY. 2003. Historical demography and genetic structure of sister species: deermice (Peromyscus) in the North American temperate rain forest. Molecular Ecology 12:711-724.

Downloads

Published

2021-05-09

Issue

Section

Special Contribution