Conservation genetics and phylogeny of the Arizona shrew in the "Sky Islands" of the Southwestern United States

Authors

  • Jesús Eduardo Maldonado Center for Conservation and Evolutionary Genetics, National Zoological Park/National Museum of Natural History, Smithsonian Institution
  • Sarah Young Albert R. Mann Library, Cornell University
  • Lee H Simons Nevada Fish and Wildlife Office
  • Sheridan Stone US Army Garrison
  • Lillian D Parker Center for Conservation and Evolutionary Genetics, National Zoological Park/National Museum of Natural History, Smithsonian Institution Department of Environmental Science and Policy, George Mason University
  • Jorge Ortega Reyes Instituto Politécnico Nacional

Keywords:

Arizona shrew, haplotype diversity, mitochondrial cytochrome-b, sky islands.

Abstract

Introduction: Little is known about the phylogenetic relationships and population genetic structure of the Arizona shrew (Sorex arizonae), a small mammal restricted to a few mountainous areas in the southwestern United States and northern Mexico. Information on genetic variability is needed, as the species is restricted to sky islands, which are small and often locally fragmented habitats.Methods: Using mitochondrial cytochrome-b sequences and 12 microsatellite loci, we assessed genetic differentiation among 64 individuals from four mountain ranges in Arizona and New Mexico: Animas, Chiricahua, Huachuca, and Santa Rita ranges.Results: We found a unique haplotype for the Animas population, while the other mountain ranges shared a common haplotype but they also each had a unique haplotype at lower frequencies. F-statistics indicate that significant population differentiation has occurred among the Chiricahua and Animas populations compared with the other two populations. The FST statistics revealed high levels of genetic differentiation between the Chiricahua and Animas populations, compared to the other two populations that show lower but significant FST values. Nevertheless, the STRUCTURE analysis using microsatellite markers did not show significant differentiation between Chiricahua and Animas but it did detect strong signatures of differentiation between the cluster formed by these two populations and Huachuca and Santa Rita. Phylogenetic analysis using cytochrome-b sequences confirmed that the Arizona shrew is most closely related to S. trowbridgii among North American shrews that have been sequenced for the mtDNA cytochrome-b region to date. Both species are placed in a monophyletic group sister to a clade consisting of Nearctic shrews.Discussion and conclusions: Our results suggest that the S. arizonae populations have high levels of differentiation in comparison to other North American shrews. We also detected high levels of population genetic structure with both mtDNA and microsatellite although the pattern between them is different. Given the inherent vulnerability of these naturally isolated populations with their locally fragmented distributions, the genetic data support a need for conservation focused on protection of suitable habitats. As our fieldwork indicates, suitable habitats include mid- to high-elevation riparian zones and upland areas, including ridgelines and mountaintop saddles with having sufficient moisture, vegetation, and soil development to provide cover and a food base for shrews.

References

Avise, J. C., J. Arnold, R. M. Ball, Jr., E. Bermingham, T. Lamb, J. E. Neigel, C. A. Reeb, and N. C. Saunders. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18:489-522.

Bickham, J. W, C. C. Wood, and J. C. Patton. 1995. Biogeographic implications of cytochrome b sequences and allozymes in sockeye (Oncorhynchus nerka). Journal of Heredity 86:140–144

Brant, S. V., and G. Orti. 2002. Molecular phylogeny of short-tailed shrews, Blarina (Insectivora: Soricidae). Molecular Phylogenetics and Evolution 22:163-173.

Brünner, H., N. Lugon-Moulin, F. Balloux, L. Fumagalli, and J. Hausser. 2002. A taxonomical re-evaluation of the Valais chromosome race of the common shrew Sorex araneus (Insectivora: Soricidae). Acta Theriologica 47:245–275.

Carraway, L. N. 2007. Shrews (Eulypotyphla: Soricidae) of Mexico. Monographs of the Western North American Naturalist 3:1–91.

Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9:1657-1659.

Crick, H. Q. P. 2004. The impact of climate change on birds. Ibis 146:48-56.

Darriba, D., G. LTaboada, R. Doallo, and D. Posada. 2012. JModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772.

DeChaine, E. G., and A. P. Martin. 2005. Marked genetic divergence among Sky Island populations of Sedum lanceolatum (Crassulacea) in the Rocky Mountains. American Journal of Botany 92:477-486.

Demboski, J. R., and J. A. Cook. 2001. Phylogeography of the dusky shrew, Sorex monticolus (Insectivora: Soricidae): insight into deep and shallow history in northwestern North America. Molecular Ecology 10:1227-1240.

Demboski, J. R., and J. A. Cook. 2003. Phylogenetic diversification within shrews of the Sorex cinereus group (Soricidae). Journal of Mammalogy 84:144-158.

Diersing, V. A., and D. F. Hoffmeister. 1977. Revision of the shrew Sorex merriami and a description of a new species of the subgenus Sorex. Journal of Mammalogy 58:321-333.

Earl, D. A., and B. M. vonHoldt. 2012. Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genetics Resources 4: 359-361.

Esteva, M., F. A. Cervantes, S. V. Brant, and J. A. Cook. 2010. Molecular phylogeny of long-tailed shrews (genus Sorex) from Mexico and Guatemala. Zootaxa 2615:47-65.

Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology 14: 2611-2620.

Excoffier, L., P. Smouse, and J. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479-491.

Fumagalli, L., P. Taberlet, D. T. Steward, L. Gielly, J. Hausser, and P. Vogel. 1999. Molecular phylogeny and evolution of Sorex shrews (Soricidae: Insectivora) inferred from mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 11:222-235.

George, S. B. 1988. Systematics, historical biogeography, and evolution of the genus Sorex. Journal of Mammalogy 69:443-461.

George, S. B. 1989. Sorex trowbridgii. Mammalian Species 337:1-5.

Hanski, I. 1994. Population biological consequences of body size in Sorex. Pp. 15-26 in Advances in the biology of shrews (Merritt, J. F., G. L. Kirkland, Jr., and R. K. Rose, eds.). Special Publication of Carnegie Museum of Natural History, Chicago.

Hellborg, L., C. W. Walker, E. K. Rueness, J. E. Stacy, I. Kojola, H. Valdmann, C. Vila, B. Zimmermann, K. S. Jakobsen, and H. Ellegren. 2002. Differentiation and levels of genetic variation in northern European lynx (Lynx lynx) populations revealed by microsatellites and mitochondrial DNA analysis. Conservation Genetics 3:97-111.

Hoffmeister, D. F. 1986. Mammals of Arizona. The University of Arizona Press. Tucson, EE. UU.

Junge, J. A., and R. S. Hoffmann. 1981. An annotated key to the long-tailed shrews (genus Sorex) of the United States and Canada, with notes on Middle American Sorex. Occasional Papers of the Museum of Natural History, The University of Kansas 94:1-48.

Kimura, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16:111-120.

Knowles, L. L. 2001. Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in the montane grasshoppers. Molecular Ecology 10:691-701.

Madison, D. R., and W. P. Madison. 2000. MacClade 4. Analysis of Phylogeny and Character Evolution. Sinauer Associates, Inc. Publishers. Sunderland, EE. UU.

Maldonado, J. E., C. Vila, and R. K. Wayne. 2001. Tripartite genetic subdivision in the ornate shrew (Sorex ornatus). Molecular Ecology 10:127-147.

Maldonado, J. E., F. Hertel, and C. Vila. 2004. Discordant patterns of morphological variation in genetically divergent populations of ornate shrews (Sorex ornatus). Journal of Mammalogy 85:886-896.

Maldonado, J. E., J. Leonard, G. A. Miranda, J. Ortega, R. K. Wayne, and R. J. Aguilera. 2006. Ten polymorphic microsatellite loci for the endangered Buena Vista Lake shrew (Sorex ornatus relictus). Molecular Ecology Notes 6:349-352.

Marshall, J. T. 1957. Birds of the pine-oak woodland in southern Arizona and adjacent Mexico. Pacific Coast Avifauna, No. 32, Cooper Ornithological Society. Berkeley, EE. UU.

Mascheretti, S., M. B. Rogatcheva, I. Gunduz, K. Fredga, and J. B. Searle. 2003. How did pygmy shrews colonize Ireland? Clues from a phylogenetic analysis of mitochondrial cytochrome b sequences. Proceedings of Biological Sciences 270:1593-1599.

Masta, S. E. 2000. Phylogeography of the jumping spider Habronattus pugillis (Araneae: Salticidae): Recent vicariance of sky island populations? Evolution 54:1699-1711.

McAliley, L. R., M. B. O’Neill, and R. J. Baker. 2007. Molecular evidence for genetic subdivisions in the desert shrew, Notiosorex crawfordi. The Southwestern Naturalist 52:410–417

Moritz, C. 1994. Defining Evolutionary Significant Units for conservation. Trends in Ecology and Evolution 9:373-375.

Mouchaty,S.K., A. Gullberg, A. Janke, and U. Arnason. 2000. T he phylogenetic position of the Talpidae within eutheria based on analysis of complete mitochondrial sequences. Molecular Biology and Evolution 17:60-67.

Nishida, F. H., W. J. Sundberg, J. A. Menge, J. S. States, R. E. Tulloss, and B. J. Cifuentes. 1992. Studies in the mycoflora of the Chiricahua Mountains. I. Preliminary report on species distribution, ecology, and biogeographical affinities. Pp. 35-39 in Chiricahua Mountains Research Symposium, Proceedings (Barton, A. M., and S. Sloane, eds.). Southwest Parks and Monument Association, Tucson, EE. UU.

Ohdachi, S. D., R. Masuda, H. Abe, J. Adachi, N. E. Dokuchaev, V. Haukisalmi, and M. C. Yoshida. 1997. Phylogeny of Eurasian soricine shrews (Insectivora, Mammalia) inferred from the mitochondrial cytochrome b gene sequences. Zoological Sciences 14:527-532.

Ohdachi, S. D., N. E. Dokuchaev, M. Hasegawa, and R. Masuda. 2001. Intraspecific phylogeny and geographical variation of Northeastern Asiatic Sorex shrews based on the mitochondrial cytochrome b sequences. Molecular Ecology 10:2199-2213.

Ohdachi, S. D., M. A. Iwasa, V. A. Nesterenko, H. Abe,R. Masuda, and W. Haberl. 2004. Molecular phylogenetics of Crocidura shrews (Insectivora) in East and Central Asia. Journal of Mammalogy 85:396–403.

Ohdachi, S. D., M. Hasegawa, M. A. Iwasa, P. Vogel, T. Oshida, L. K. Lin, and H. Abe. 2006. Molecular phylogenetics of the soricid shrews (Mammalia) based on mitochondrial cytochrome b gene sequences: with special reference to the Soricinae. Journal of Zoology (London) 270:177-191.

Ortega, J., S. Young, L. H. Simons, and J. E. Maldonado. 2005. Characterization of six microsatellite loci for Sorex arizonae. Molecular Ecology Notes 5:851-853.

Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.

Raymond, M., and F. Rousset. 1995. GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.

Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.

Ronquist, F., and J. P. Huelsenbeck. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.

Rousset, F. 1996. Equilibrium Values of Measures of Population Subdivision for Stepwise Mutation Processes. Genetics 142:1357-1362.

Saitou, N., and M. Nei. 1987. The neighbor-joining method: A new method for reconstruction phylogenetic trees. Molecular Biology and Evolution 4:406-425.

Sambrook, I., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Second edition. Cold Spring Harbor Laboratory Press. New York, EE. UU.

Schneider, S., D. Roessli, and L. Excoffier. 2000. Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva. Geneva, Switzerland.

Sikes, R. S., W. L. Gannon, and the Animal Care and Use Committee ofthe American Society ofMammalogists. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92:235-253.

Simons, L. H., and D. F. Hoffmeister. 2003. Sorex arizonae. Mammalian Species 732:1-3.

Simons, L. H. and J. E. Maldonado. 2007. Genetics of Arizona Shrew (Sorex arizonae). Final Report on Heritage Grants-in-Aid Project Number I99023. Arizona Game and Fish Department. Phoenix, EE. UU.

Simons, L. H., R. C. Szaro, and S. C. Belfit. 1990. Distribution of Notiosorex crawfordi and Sorex arizonae along an elevational gradient. Journal of Mammalogy 71:634-640.

Simons, L. H., and W. E. Van Pelt. 1999. Occurrence of Sorex arizonae and other shrews (Insectivora) in southern Arizona. The Southwestern Naturalist 44:334-342.

Sipe, T. W., and R. A. Browne. 2004. Phylogeography of masked (Sorex cinereus) and smoky shrew (Sorex fumeus) in the southern Appalachian. Journal of Mammalogy 85:875-885.

Swofford, D. L. 2001. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0 b10. Sinauer Associates Inc. Sunderland, EE. UU.

Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitution in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10:512-526.

Warshall, P. 1986. Biogeography of high peaks of the Pinalenos. Environmental Data Book, U.S. Forest Service, Coronado National Forest, by Maricopa Audubon Society. Phoenix, EE. UU.

Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.

Woodman, N., J. Matson, and I. Castro-Arellano. 2008. Sorex arizonae. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. . Downloaded on 13 October 2014

Published

2015-04-13

Issue

Section

Articles