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From Desert to Rainforest: Phenotypic Variation in Functionally Important Traits of Bushy-Tailed Woodrats (Neotoma cinerea) Across Two Climatic Extremes

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Abstract

Changes in body size inversely related to ambient temperatures have been described in woodrats (Neotoma) over time scales ranging from decades to millennia. However, climate-mediated variation in other traits has not been evaluated, and the effects of precipitation have been overlooked. We assessed variation in skull morphology among bushy-tailed woodrats (Neotoma cinerea) over two sampling transects spanning coastal rainforest and interior desert environments to determine whether skull morphology varied with climate. We also tested whether previously described size-temperature relationships could be generalized to our study populations. In both transects, linear measurements of functionally significant traits differed between coastal and interior populations. Geometric morphometric analyses of shape confirmed some of those differences and revealed additional patterns of skull variation. Variation in some linear measurements, including body size, was predicted by climate. However, body and skull size, as well as measurements of skull components, displayed varying responses. Although longitudinal patterns of body size variation supported Bergmann’s rule, skull size variation was only weakly associated with climate. The strongest phenotypic responses to climate were those of auditory, dental, and palatal skull traits. Altogether, our findings suggest that geographic variation in temperature and precipitation mediated selective heterogeneity and plasticity in skull traits associated with food processing and sensory organs in N. cinerea. This was consistent with our expectation of resource-dependent phenotypic variation among populations in environments with highly contrasting climatic regimes.

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References

  • Anderson DR (2008) Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York

    Book  Google Scholar 

  • Anderson EW, Borman MM, Krueger WC (1998) The Ecological Provinces of Oregon: A Treatise on the Basic Ecological Geography of the State. Oregon Agricultural Experiment Station, Corvallis

    Google Scholar 

  • Barciova L (2009) Advances in insectivore and rodent systematics due to geometric morphometrics. Mammal Rev 39:80–91

    Article  Google Scholar 

  • Barnosky AD (2005) Effects of Quaternary climatic change on speciation in mammals. J Mammal Evol 12:247–264

    Article  Google Scholar 

  • Blois JL, Hadly EA (2009) Mammalian response to Cenozoic climatic change. Annu Rev Earth Planet Sci 37:8.1–8.28

    Article  Google Scholar 

  • Brown JH (1968) Adaptation to environmental temperature in two species of woodrats, Neotoma cinerea and N. albigula. Misc Publ Mus Zool Univ Mich 135:1–48

    Google Scholar 

  • Brown JH, Lee AK (1969) Bergmann’s rule and climatic adaptation in woodrats (Neotoma). Evolution 23:329–338

    Article  Google Scholar 

  • Butler PM (1983) Evolution and mammalian dental morphology. J Biol Buccal 11:285–302

    CAS  Google Scholar 

  • Endler J (1977) Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton

    Google Scholar 

  • Escherich PC (1981) Social biology of the bushy-tailed woodrat, Neotoma cinerea. Univ Calif Publ Zool 110:1–132

    Google Scholar 

  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    Article  PubMed  CAS  Google Scholar 

  • Goheen JR, Swihart RK, Robis JH (2003) The anatomy of a range expansion: changes in cranial morphology and rates of energy extraction for North American red squirrels from different latitudes. Oikos 102:33–44

    Article  Google Scholar 

  • Goodall C (1991) Procrustes methods in the statistical analysis of shape. J R Stat Soc, Ser B 53:285–339

    Google Scholar 

  • Goswami A, Polly PD (2010) The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia). PloS ONE 5:1–8

    Google Scholar 

  • Gotthard K, Nylin S (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3–17

    Article  Google Scholar 

  • Grinnell J, Swarth HS (1913). An account of the birds and mammals of the San Jacinto area of southern California. Univ Calif Publ Zool 10:197–406

    Google Scholar 

  • Hall ER (1981) Mammals of North America. Wiley, New York

    Google Scholar 

  • Hanken J, Hall BK (1993) Mechanisms of skull diversity and evolution. In: Hanken J, Hall BK (eds) The Skull, Vol. 3: Functional and Evolutionary Mechanisms. The University of Chicago Press, Chicago, pp 1–36

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hijmans RJ, Guarino L, Cruz M, Rojas E (2001) Computer tools for spatial analysis of plant genetic resources data : 1. DIVA-GIS. Plant Genet Res News 127:15–19

    Google Scholar 

  • Hooper E (1940) Geographical variation in bushy-tailed woodrats. Univ Calif Publ Zool 42:407–424

    Google Scholar 

  • Hornsby AD (2009) Molecular and morphological variation in Neotoma cinerea. Master’s thesis, University of Nevada, Reno

  • Hornsby AD, Matocq MD (2012) Differential regional response of the bushy-tailed woodrat (Neotoma cinerea) to late Quaternary climate change. J Biogeogr

  • Jackson ST, Betancourt JL, Lyford ME, Gray ST, Rylander KA (2005) A 40,000-year woodrat-midden record of vegetational and biogeographical dynamics in north-eastern Utah, USA. J Biogeogr 32:1085–1106

    Article  Google Scholar 

  • Klingenberg CP (2010) Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 11:623–635

    PubMed  CAS  Google Scholar 

  • Lee AK (1963) The adaptations to arid environments in wood rats of the genus Neotoma. Univ Calif Publ Zool 64:57–96

    Google Scholar 

  • Liao J, Zhang Z, Liu N (2007) Effects of altitudinal change on the auditory bulla in Ochotona daurica (Mammalia, Lagomorpha). J Zool Syst Evol Res 45:151–154

    Article  Google Scholar 

  • Lyman RL, O’Brien MJ (2005) Within-taxon morphological diversity in late-Quaternary Neotoma as a paleoenvironmental indicator, Bonneville Basin, Northwestern Utah, USA. Quaternary Res 63:274–282

    Article  Google Scholar 

  • MacLeod N, Forey P (2002) Morphology, shape, and phylogenetics. In: MacLeod N, Forey P (eds) Morphology, Shape and Phylogeny. Taylor & Francis, London, pp 1–7

    Chapter  Google Scholar 

  • Marcus LF (1990) Traditional morphometrics. In: Rohlf FJ, Bookstein FL (eds) Proceedings of the Michigan Morphometrics Workshop, special publication no. 2. The University of Michigan Museum of Zoology, Ann Arbor, pp 77–122

  • Mares MA (1993) Desert rodents, seed consumption, and convergence. BioScience 43:372–379

    Article  Google Scholar 

  • Marroig G, Shirai LT, Porto A, de Oliveira FB, De Conto V (2009) The evolution of modularity in the mammalian skull II: evolutionary consequences. Evol Biol 36:136–148

    Article  Google Scholar 

  • Maser C, Mate BR, Franklin JF, Dyrness CT (1981) Natural History of Oregon Coast Mammals, USDA Forest Service General Technical Report PNW-133. Pacific Northwest Forest and Range Experiment Station, Portland

    Google Scholar 

  • Matocq MD (2009) A microarray’s view of life in the desert: adding a powerful evolutionary genomics tool to the packrat’s midden. Mol Ecol 18:2310–2312

    Article  PubMed  Google Scholar 

  • Mayr E (1963) Animal Species and Evolution. Harvard University Press, Cambridge

    Google Scholar 

  • McEachern MB, Eagles-Smith CA, Efferson CM, Van Vuren DH (2006) Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes. Oikos 113:440–448

    Article  Google Scholar 

  • Menegaz RA, Sublett SV, Figueroa SD, Hoffman TJ, Ravosa MJ (2009) Phenotypic plasticity and function of the hard palate in growing rabbits. Anat Rec 292: 277–284

    Article  Google Scholar 

  • Monteiro LR, Duarte LC, dos Reis SF (2003) Environmental correlates of geographical variation in skull and mandible shape of the punare rat Thrichomys apereoides (Rodentia: Echimyidae). J Zool 261:47–57

    Article  Google Scholar 

  • Nummela S (1995) Scaling of the mammalian middle ear. Hear Res 85:18–30

    Article  PubMed  CAS  Google Scholar 

  • Parichy DM (2005) Variation and developmental biology: prospects for the future. In: Hallgrimsson B, Hall BK (eds) Variation. Elselvier Academic Press Amsterdam, pp 475–491

    Google Scholar 

  • Patton JL, Brylski PV (1987) Pocket gophers in alfalfa fields: causes and consequences of habitat-related body size variation. Am Nat 130:493–506

    Article  Google Scholar 

  • Patton JL, Huckaby DG, Alvarez-Castaneda ST (2008) The evolutionary history and a systematic revision of woodrats of the Neotoma lepida group. Univ Calif Publ Zool 135:1–411

    Google Scholar 

  • Pergams ORW, Lawler JJ (2009) Recent and widespread rapid morphological change in rodents. PloS ONE 4:e6452

    Article  PubMed  Google Scholar 

  • Porto A, de Oliveira FB, Shirai LT, De Conto V, Marroig G (2009) The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol Biol 36:118–135

    Article  Google Scholar 

  • Price LW (1978) Mountains of the Pacific Northwest, USA: a study in contrasts. In: Mountain Geoecology and Land-use Implications: Proceedings of the Symposium of the International Geographical Union Commision on High-altitude Geoecology. Arct Alp Res 10: 465–478

  • Russell AP, Bauer AM (2005) Variation in structure and its relationship to function: correlation, explanation, and extrapolation. In: Hallgrimsson B, Hall BK (eds) Variation. Elselvier Academic Press, Amsterdam, pp 399–428

    Google Scholar 

  • Samuels JX (2009) Cranial morphology and dietary habits of rodents. Zool J Linn Soc 156:864–888

    Article  Google Scholar 

  • Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370

    Article  PubMed  CAS  Google Scholar 

  • Smith FA (1992) Evolution of body size among woodrats from Baja California, Mexico. Funct Ecol 6:265–273

    Article  Google Scholar 

  • Smith FA (1995) Scaling of digestive efficiency with body mass in Neotoma. Funct Ecol 9:299–305

    Article  Google Scholar 

  • Smith FA (1997) Neotoma cinerea. Mammal Species 564:1–8

    Article  Google Scholar 

  • Smith FA, Betancourt JL (1998) Response of bushy-tailed woodrats (Neotoma cinerea) to late Quaternary climatic change in the Colorado Plateau. Quaternary Res 50:1–11

    Article  Google Scholar 

  • Smith FA, Betancourt JL (2003) The effect of Holocene temperature fluctuations on the evolution and ecology of Neotoma (woodrats) in Idaho and northwestern Utah. Quaternary Res 59:160–171

    Article  Google Scholar 

  • Smith FA, Betancourt JL (2006) Predicting woodrat (Neotoma) responses to anthropogenic warming from studies of the palaeomidden record. J Biogeogr 33:2061–2076

    Article  Google Scholar 

  • Smith FA, Betancourt JL, Brown JH (1995) Evolution of body size in the woodrat over the past 25,000 years of climate change. Science 270:2012–2014

    Article  CAS  Google Scholar 

  • Smith FA, Browning H, Shepherd UL (1998) The influence of climatic change on the body mass of woodrats Neotoma in an arid region of New Mexico, USA. Ecography 21:140–148

    Article  Google Scholar 

  • Smith FA, Crawford DL, Harding LE, Lease HM, Murray IW, Raniszewski A, Youberg KM (2009) A tale of two species: extirpation and range expansion during the late Quaternary in an extreme environment. Glob Planet Chang 65:122–133

    Article  Google Scholar 

  • Taylor GH (1999) The Climate of Oregon: From Rain Forest to Desert. Oregon State University Press, Corvallis

    Google Scholar 

  • Travis J (1994) Evaluating the adaptive role of morphological plasticity. In: Wainwright PC, Reilly SM (eds) Ecological Morphology. The University of Chicago Press, Chicago, pp 99–122

    Google Scholar 

  • Ungar PS (2010) Mammal Teeth: Origin, Evolution, and Diversity. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Verts BJ, Carraway LN (1998) Land Mammals of Oregon. University of California Press, Berkeley

    Google Scholar 

  • Walsberg GE (2000) Small mammals in hot deserts: some generalizations revisited. BioSci 50:109–120

    Article  Google Scholar 

  • Webster DB, Webster M (1975) Auditory systems of Heteromyidae: functional morphology and evolution of the middle ear. J Morphol 146:343–376

    Article  PubMed  CAS  Google Scholar 

  • Webster DB, Webster M (1980) Morphological adaptations of the ear in the rodent family Heteromyidae. Am Zool 20:247–254

    Google Scholar 

  • Yom-Tov Y, Geffen E (2006) Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 148:213–218

    Article  PubMed  Google Scholar 

  • Zakrzewski RJ (1993) Morphological change in woodrat (Rodentia: Cricetidae) molars. In: Martin RA, Barnosky AD (eds) Morphological Change in Quaternary Mammals of North America. Cambridge University Press, Cambridge, pp 392–407

    Chapter  Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric Morphometrics for Biologists: A Primer. Elselvier Academic Press, London

    Google Scholar 

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Acknowledgements

Funding was provided by the Oregon State University Undergraduate Research, Innovation, Scholarship and Creativity grant. Portions of this investigation were completed through the University of California Museum of Vertebrate Zoology (MVZ) research internship program. We thank the curatorial staff of the MVZ for their assistance and helpful comments, especially Chris Conroy. We thank all other museum curators for providing access to specimens.

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  1. Gerardo A. Cordero

    Present address: Department of Ecology, Evolution and Organismal Biology, Iowa State University, 253 Bessey Hall, Ames, IA, 50011, USA

Authors and Affiliations

  1. Oregon State University, Environmental Sciences, 2046 Cordley Hall, Corvallis, OR, 97331, USA

    Gerardo A. Cordero

  2. Museum of Vertebrate Zoology, University of California, Berkeley, 3101 Valley Life Sciences Building, Berkeley, CA, 94720, USA

    Gerardo A. Cordero

  3. Department of Fisheries and Wildlife, Oregon State University, 104 Nash Hall, Corvallis, OR, 97331, USA

    Clinton W. Epps

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  1. Gerardo A. Cordero
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Correspondence to Gerardo A. Cordero.

Appendix

Appendix

Table 5 Museuma specimens of N. cinerea, categorized by coastal and interior climatic zones of the Cascades (CSD) and Klamath (KM) transects, used in morphometric analyses
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Table 6 Principle component eigenvectors for axes one and two in principal component analyses of linear morphometric measurementsa
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Table 7 Summary statistics of linear morphometric measurementsa not used in climate-morphology analyses
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Table 8 Statistical tests for correlation among climatica and geographic variables
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Table 9 Proportion of variation explained (R 2) in linear morphometric charactersa by climaticb and geographic variables, as assessed by linear regression
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Cordero, G.A., Epps, C.W. From Desert to Rainforest: Phenotypic Variation in Functionally Important Traits of Bushy-Tailed Woodrats (Neotoma cinerea) Across Two Climatic Extremes. J Mammal Evol 19, 135–153 (2012). https://doi.org/10.1007/s10914-012-9187-0

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