Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-02T20:26:07.776Z Has data issue: false hasContentIssue false

Investigating (a)symmetry in a small mammal's response to warming and cooling events across western North America over the late Quaternary

Published online by Cambridge University Press:  15 May 2019

Meghan A. Balk*
Affiliation:
Bio5 Institute, University of Arizona, Tucson, Arizona 85721, USA
Julio L. Betancourt
Affiliation:
Water Mission Area, National Research Program, United States Geological Survey, Reston, VA 20192, USA
Felisa A. Smith
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA
*
*Corresponding author e-mail address: [email protected] (M.A. Balk).

Abstract

Many mammalian populations conform spatially and temporally to Bergmann's rule. This ecogeographic pattern is driven by selection for larger body masses by cooler temperatures and smaller ones by warming temperatures. However, it is unclear whether the response to warming or cooling temperatures is (a)symmetrical. Studies of the evolutionary record suggest that mammals evolve smaller body sizes more rapidly than larger ones, suggesting that it may be “easier” to adapt to warming climates than cooling ones. Here, we examine the potential asymmetrical response of mammals to past temperature fluctuations. We use the fossil midden record of the bushy-tailed woodrat, Neotoma cinerea, a well-studied animal that generally conforms to Bergmann's rule, to test the ability of populations to respond to warming versus cooling climate throughout its modern range in western North America over the late Quaternary. We quantified the response to temperature change, as characterized by the Greenland Ice Sheet Project 2 temperature record, using N. cinerea presence/absence and “darwins.” Our results show that populations within the modern range of N. cinerea show little difference between warming and cooling events. However, northern, peripheral populations are absent during older, cooler periods, possibly due to climate or taphonomy. Our study suggests adaptation in situ may be an underestimated response to future climate change.

Type
Research Article
Copyright
Copyright © University of Washington. Published by Cambridge University Press, 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alley, R.B., 2000. The Younger Dryas cold interval as viewed from central Greenland. Quaternary Science Reviews 19, 213226.Google Scholar
Alley, R.B., Marotzke, J., Nordhaus, W.D., Ovepeck, J.T., Peteet, D.M., Pielke, R.A. Jr., Pierrehumbert, R.T., et al. , 2003. Abrupt climate change. Science 299, 20052010.Google Scholar
Barnosky, A.D., Hadly, E.A., Bell, C.J., 2003. Mammalian response to global warming on varied temporal scales. Journal of Mammalogy 84, 354368.Google Scholar
Bell, G., Gonzalez, A., 2011. Adaptation and evolutionary rescue in metapopulations experiencing environmental deterioration. Science 332, 13271330.Google Scholar
Bergmann, C., 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien 3, 595708.Google Scholar
Betancourt, J.L., Devender, T.R.V., Martin, P.S., 1990. Packrat Middens: The last 40,000 Years of Biotic Change. University of Arizona Press, Tucson, AZ.Google Scholar
Blois, J.L., Hadly, E.A., 2009. Mammalian response to Cenozoic climatic change. Annual Reviews of Earth and Planetary Science 37, 181208.Google Scholar
Bradsahw, W.E., Holzapfel, C.M., 2006. Evolutionary response to rapid climate change. Science 312, 14771478.Google Scholar
Brown, J.H., Lee, A.K., 1969. Bergmann's rule and climate adaptation in woodrats (Neotoma). Evolution 23, 329338.Google Scholar
Ceballos, G., Ehrlich, P.R., Barnosky, A.D., García, A., Pringle, R.M., Palmer, T.M., 2015. Accelerated modern human-induced species losses: entering the sixth mass extinction. Science Advances 1, e1400253.Google Scholar
Chen, I.-C., Hill, J.K., Ohlemüller, R., Roy, D.B., Thomas, C.D., 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333, 10241026.Google Scholar
Clark, P.U., Shakun, J.D., Baker, P.A., Bartlein, P.J., Brewer, S., Brook, E., Carlson, A.E., et al. , 2013. Global climate evolution during the last deglaciation. Proceedings of the National Academy of Sciences USA 109, E1135E1142.Google Scholar
Cook, B.I., Wolkovich, E.M., Davies, T.J., Ault, T.R., Betancourt, J.L., Allen, J.M., Bolmgren, K., et al. , 2012. Sensitivity of spring phenology to warming across temporal and spatial climate gradients in two independent databases. Ecosystems 15, 12831294.Google Scholar
Cuffey, K.M., Clow, G.D., 1997. Temperature, accumulation, and ice sheet elevation in central Greenland through the last deglacial transition. Journal of Geophysical Research 102, 2638326396.Google Scholar
Ellis, E.C., Goldewijk, K.K., Siebert, S., Lightman, D., Ramankutty, N., 2010. Anthropogenic transformation of the biomes, 1700 to 2000. Global Ecology and Biogeography 19, 589606.Google Scholar
Evans, A.R., Jones, D., Boyer, A.G., Brown, J.H., Costa, D.P., Ernest, S.K.M., Fitzgerald, E.M.G., et al. , 2012. The maximum rate of mammal evolution. Proceedings of the National Academy of Sciences USA 109, 41874190.Google Scholar
Fairbanks, R.G., Mortlock, R.A., Chiu, T.-C., Cao, L., Kaplan, A., Guilderson, T.P., Fairbanks, T.W., et al. , 2005. Radiocarbon calibration curve spanning 0 to 50,000 years BP based on paired 230Th/ 234U/ 238U and 14C dates on pristine corals. Quaternary Sceince Reviews 24, 17811796.Google Scholar
Finley, R.B., 1958. The woodrats of Colorado. University of Kansas Publications, Museum of Natural History 10, 213552.Google Scholar
Gingerich, P.D., 1983. Rates of evolution: effects of time and temporal scaling. Science 222, 159161.Google Scholar
Graham, R.W., 1986. Response of mammalian communities to environmental changes during the late Quaternary. In: Diamond, J., Case, T.J. (Eds.), Community Ecology. Harper and Row, New York, pp. 300313.Google Scholar
Hall, E.R., 1981. The Mammals of North America. Wiley, New York.Google Scholar
Harris, A.H., 1984a. Neotoma in the late Pleistocene of New Mexico and Chihuahua. In: Genoways, H.H., Dawson, M.R. (Eds.), Contributions ot Quaternary Vertebrate Paleontology: A Volume in Memorial to John E. Guilday. Special Publications of the Carnegie Museum of Natural History. Carnegie Museum of Natural History, Pittsburgh, PA, pp. 1538.Google Scholar
Harris, A.H., 1984b. Two new species of late Pleistocene woodrats (cricetidae: Neotoma) from New Mexico. Journal of Mammalogy 65, 560566.Google Scholar
Harris, A.H., 1993. Quaternary vertebrates of New Mexico. New Mexico Museum of Natural History and Science Bulletin 2, 179197.Google Scholar
Haugen, T.O., Vøllestad, L.A., 2000. Population differences in early life-history traits in grayling. Journal of Evolutionary Biology 13, 897905.Google Scholar
Hetem, R.S., Fuller, A., Maloney, S.K., Mitchell, D., 2014. Responses of large mammals to climate change. Temperature 1, 115127.Google Scholar
Hof, C., Levinsky, I., Araújo, M.B., Rahbek, C., 2011. Rethinking species’ ability to cope with rapid climate change. Global Change Biology 17, 29872990.Google Scholar
Hoffmann, A.A., Sgro, C.M., 2011. Climate change and evolutionary adaptation. Nature 470, 479485.Google Scholar
Huntley, B., 2007. Evolutionary response to climatic change? Heredity 98, 247248.Google Scholar
Jackson, S.T., Overpeck, J.T., 2000. Responses of plant populations and communities to environmental changes of the late Quaternary. Paleobiology 26, 194220.Google Scholar
Jouzel, J., Masson-Delmotte, V., Cattani, O., Dreyfus, G., Falourd, S., Hoffmann, G., Minster, B., et al. , 2007. Orbital and millennial Antarctic climate variability over the past 800,000 years. Science 317, 793796.Google Scholar
Lenoir, J., Svenning, J.-C., 2015. Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography 38, 1528.Google Scholar
Lyons, S.K., 2003. A quantitative assessment of the range shifts of Pleistocene mammals. Journal of Mammalogy 84, 385402.Google Scholar
Lyons, S.K., 2005. A quantitative model for assessing community dynamics of Pleistocene mammals. American Naturalist 165, E168E185.Google Scholar
MacDonald, G.M., Moser, K.A., Bloom, A.M., Porinchu, D.F., Potito, A.P., Wolfe, B.B., Edwards, T.W.D., Petel, A., Orme, A.R., Orme, A.J., 2008. Evidence of temperature depression and hydrological variations in the eastern Sierra Nevada during the Younger Dryas stade. Quaternary Research 70, 131140.Google Scholar
Mayr, E., 1956. Geographical character gradients and climatic adaptation. Evolution 10, 105108.Google Scholar
McCain, C.M., King, S.R.B., 2014. Body size and activity times mediate mammalian responses to climate change. Global Change Biology 20, 17601769.Google Scholar
McLaughlin, J.F., Hellmann, J.J., Boggs, C.L., Ehrilch, P.R., 2002. Climate change hastens population extinctions. Proceedings of the National Academy of Sciences USA 99, 60706074.Google Scholar
Meyer, H.W., 1992. Lapse rates and other variables applied to estimating paleoaltitudes from fossil floras. Palaeogeography, Palaeoclimatology, Palaeoecology 99, 7199.Google Scholar
Millien, V., Lyons, S.K., Olson, L., Smith, F.A., Wilson, A.B., Yom-Tov, Y., 2006. Ecotypic variation in the context of global climate change: revisiting the rules. Ecology Letters 9, 853869.Google Scholar
Murray, I.W., Smith, F.A., 2012. Estimating the influence of the thermal environment on activity patterns of the desert woodrat (Neotoma lepida) using temperature chronologies. Canadian Journal of Zoology 90, 11711180.Google Scholar
Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change. Annual Reviews of Ecological and Evolutionary Systems 37, 637639.Google Scholar
Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 3742.Google Scholar
Porinchu, D.F., MacDonald, G.M., Bloom, A.M., Moser, K.A., 2003. Late Pleistocene and early Holocene climate and limnological changes in the Sierra Nevada, California, USA inferred from midges (Insecta: Diptera: Chironomidae). Palaeogeography, Palaeoclimatology, Palaeoecology 198, 403422.Google Scholar
Potito, A.P., Porinchu, D.F., MacDonald, G.M., Moser, K.A., 2006. A late Quaternary chironomid-inferred temperature record from the Sierra Nevada, California, with connections to northeast Pacific sea surface temperatures. Quaternary Research 66, 356363.Google Scholar
Raup, D.M., 1979. Biases in the fossil record of species and genera. Bulletin of Carnegie Museum of Natural History 13, 8591.Google Scholar
Reinemann, S.A., Porinchu, D.F., Bloom, A.M., Mark, B.G., Box, J.E., 2009. A multi-proxy paleolimnological reconstruction fo Holocene climate conditions in the Great Basin, United States. Quaternary Research 72, 347358.Google Scholar
Reinemann, S.A., Porinchu, D.F., MacDonald, G.M., Mark, B.G., DeGrand, J.Q., 2014. A 2000-yr reconstruction of air temperature in the Great Basin of the United States with specific reference to the Medieval Climatic Anomaly. Quaternary Research 82, 309317.Google Scholar
Reznick, D.N., Shaw, F.H., Rodd, F.H., Shaw, R.G., 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275, 19341937.Google Scholar
Rowe, R.J., Terry, R.C., 2014. Small mammal responses to environmental change: integrating past and present dynamics. Journal of Mammalogy 95, 11571174.Google Scholar
Salzer, M.W., Bunn, A.G., Hughes, N.E.G.K., 2013. Five millennia of paleotemperature from tree-rings in the Great Basin, USA. Climate Dynamics 42, 15171526.Google Scholar
Salzer, M.W., Kipfmueller, K.F., 2005. Reconstructed temperature and precipitation on a millennial timescale from tree-rings in the southern Colorado Plateau, U.S.A. Climatic Change 70, 465487.Google Scholar
Sandel, B., Arge, L., Dalsgaard, B., Davies, R.G., Gaston, K.J., Sutherland, W.J., Svenning, J.-C., 2011. The influence of Late Quaternary climate-change velocity on species endemism. Science 334, 660664.Google Scholar
Scholander, P.F., Hock, R., Walters, V., Irving, L., 1950. Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biological Bulletin 99, 259271.Google Scholar
Selwood, K.E., McGeoch, M.A., MacNally, R., 2015. The effects of climate change and land-use change on demographic rates and population viability. Biological Reviews 90, 837853.Google Scholar
Smith, F.A., 1995. Scaling of digestive efficiency with body mass in Neotoma. Functional Ecology 9, 299305.Google Scholar
Smith, F.A., 1997. Neotoma cinerea. Mammalian Species 564, 18.Google Scholar
Smith, F.A., Betancourt, J.L., 2003. The effect of Holocene temperature fluctuations on the evolution and ecology of Neotoma (woodrats) in Idaho and northwestern Utah. Quaternary Research 59, 160171.Google Scholar
Smith, F.A., Betancourt, J.L., 2006. Predicting woodrat (Neotoma) responses to anothropogenic warming from studies of the palaeomidden record. Journal of Biogeography 33, 20612076.Google Scholar
Smith, F.A., Betancourt, J.L., Brown, J.H., 1995. Evolution of body size in the woodrat over the past 25,000 years of climate change. Science 270, 20122014.Google Scholar
Smith, F.A., Browning, H., Shepherd, U.L., 1998. The influence of climate change on the body mass of woodrats Neotoma in an arid region of New Mexico, USA. Ecography 21, 140148.Google Scholar
Smith, F.A., Brown, J.H., Haskell, J.P., Lyons, S.K., Alroy, J., Charnov, E.L., Dayan, T., et al. , 2004. Similarity of mammalian body size across the taxonomic hierarchy and across space and time. The American Naturalist 163(5), 672691.Google Scholar
Stocker, T.F., Qin, D., Plattner, G.K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, B., Midgley, B.M. (Eds.), 2013. Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.Google Scholar
Thompson, J.N., 1998. Rapid evolution as an ecological process. Trends in Ecology & Evolution 13, 329332.Google Scholar
Verts, B.J., Carraway, L.N., 2002. Neotoma lepida. Mammalian Species 699, 112.Google Scholar
Viau, A.E., Gajewski, K., Sawada, M.C., Fines, P., 2006. Millennial-scale temperature variations in North America during the Holocene. Journal of Geophysical Research 111, D09102.Google Scholar
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.-M., Hoegh-Guldberg, O., Bairlein, F., 2002. Ecological responses to recent climate change. Nature 416, 389395.Google Scholar
Williams, J.W., Jackson, S.T., 2007. Novel climates, no-analog communities, and ecological surprises. Frontiers in Ecology and the Environment 5, 475482.Google Scholar
Williams, J.W., Grimm, E.C., Blois, J.L, Charles, D.F. 2018. The Neotoma Paleoecology Database, a multiproxy, international community-curated data resource. Quaternary Research 89, 156177.Google Scholar
Supplementary material: File

Balk et al. supplementary material

Tables S1-S4

Download Balk et al. supplementary material(File)
File 180.4 KB
Supplementary material: File

Balk et al. supplementary material

Balk et al. supplementary material 1

Download Balk et al. supplementary material(File)
File 77.4 KB