RESEARCH PAPER
A tale of four bears: Environmental signal on the phylogeographical patterns within the extant Ursus species
Carlos Luna-Aranguré,
Jorge Soberón,
Ella Vázquez-Domínguez,
Carlos Luna-Aranguré
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México
Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Unidad de Posgrado, Ciudad de México, México
Search for more papers by this authorJorge Soberón
Natural History Museum and Biodiversity Research Center, Department of Evolutionary Biology, University of Kansas, Lawrence, KS, USA
Search for more papers by this authorCorresponding Author
Ella Vázquez-Domínguez
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México
Correspondence
Ella Vázquez-Domínguez, Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Ciudad de México, México.
Email: [email protected]
Search for more papers by this authorCarlos Luna-Aranguré,
Jorge Soberón,
Ella Vázquez-Domínguez,
Carlos Luna-Aranguré
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México
Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Unidad de Posgrado, Ciudad de México, México
Search for more papers by this authorJorge Soberón
Natural History Museum and Biodiversity Research Center, Department of Evolutionary Biology, University of Kansas, Lawrence, KS, USA
Search for more papers by this authorCorresponding Author
Ella Vázquez-Domínguez
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México
Correspondence
Ella Vázquez-Domínguez, Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Ciudad de México, México.
Email: [email protected]
Search for more papers by this authorHandling Editor: Jenny McGuire
Abstract
Aim
Assessing the relevance of niche evolution in the diversification patterns and geographical distribution of species driven by climate remains a challenge. We apply an integrative approach to evaluate the role of the environment on the phylogeography of bear species, incorporating fossil data to characterize the changes in the ecological niche through time. We evaluate our approach with the four extant species of bears within Ursus, the best represented taxon in the fossil record of the family Ursidae.
Location
Eurasia and North America.
Taxa
Asian black bear, Ursus thibetanus; American black bear, U. americanus; Brown bear, U. arctos; and Polar bear, U. maritimus.
Methods
We built a genetic and a geographical database from all published mitochondrial DNA sequences and of species occurrence records. We defined the most significant climatic variables based on each species ecological realm using correlation matrices, and characterized the ecological niches and existing environmental conditions with ellipsoid models. We inferred their current and Last Glacial Maximum (LGM) ecological niche modellings (ENMs) and compared the results with the fossil record. We estimated the times of divergence (d-loop sequences) of lineages and applied a phyloclimatespace approach to discern the phylogeographical patterns along each species’ ecological space.
Results
Ecological niche modelling showed wider niches for U. thibetanus and U. americanus encompassing higher temperature and precipitation, while U. arctos and U. maritimus showed an opposite pattern. LGM models were consistent with the fossil record, predicting 55%–89% of the fossil occurrences (within their suitability areas). The phyloclimatespace revealed different degrees of environmental signal in the lineages’ phylogeographical patterns and ecological trajectories associated with LGM climatic conditions. Results indicated habitat tracking and ecological expansion since the LGM towards more extreme precipitation and temperature conditions for three species, except U. maritimus that showed ecological niche reduction.
Main Conclusions
Incorporating fossil information from the LGM improved our characterization and interpretation of ecological models, by enabling definition of the limits of the climatic conditions explored by the species in the past. Our approach also provided insights about the existing set of environmental conditions shaping the ecological niche divergence of Ursus bears. We were able to depict key features of the lineages’ evolutionary history, ecology and distribution, revealing the dynamics of niche occupation and the environmental signal on the phylogeographical patterns of Ursus.
Open Research
DATA AVAILABILITY STATEMENT
All the data used in the study comes from freely available databases (GBIF, Fossilworks, WorldClim, GenBank). The datasets we built are available from the Dryad Digital Repository at https://doi.org/10.5061/dryad.dncjsxkvw
Supporting Information
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| jbi13752-sup-0001-AppendixS1.pdfPDF document, 1.8 MB |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Aiello-Lammens, M. E., Boria, R. A., Radosavljevic, A., Vilela, B., & Anderson, R. P. (2015). SpThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography, 38, 541–545. https://doi.org/10.1111/ecog.01132
- Allen, J. R., Hickler, T., Singarayer, J. S., Sykes, M. T., Valdes, P. J., & Huntley, B. (2010). Last glacial vegetation of northern Eurasia. Quaternary Science Reviews, 29(19–20), 2604–2618. https://doi.org/10.1016/j.quascirev.2010.05.031
- Alvarado-Serrano, D. F., & Knowles, L. L. (2014). Ecological niche models in phylogeographic studies: Applications, advances and precautions. Molecular Ecology Resources, 14, 233–248. https://doi.org/10.1111/1755-0998.12184
- Anderson, R. P., Lew, D., & Peterson, A. T. (2003). Evaluating predictive models of species’ distributions: Criteria for selecting optimal models. Ecological Modelling, 162, 211–232. https://doi.org/10.1016/S0304-3800(02)00349-6
- Anijalg, P., Ho, S. Y., Davison, J., Keis, M., Tammeleht, E., Bobowik, K., & Markov, N. I. (2017). Large-scale migrations of brown bears in Eurasia and to North America during the Late Pleistocene. Journal of Biogeography, 45, 394–405.
- Ashrafzadeh, M. R., Kaboli, M., & Naghavi, M. R. (2016). Mitochondrial DNA analysis of Iranian brown bears (Ursus arctos) reveals new phylogeographic lineage. Mammalian Biology, 81, 1–9. https://doi.org/10.1016/j.mambio.2015.09.001
- Baca, M., Popović, D., Stefaniak, K., Marciszak, A., Urbanowski, M., Nadachowski, A., & Mackiewicz, P. (2016). Retreat and extinction of the Late Pleistocene cave bear (Ursus spelaeus sensu lato). The Science of Nature, 103, 92. https://doi.org/10.1007/s00114-016-1414-8
- Bartoń, K. A., Zwijacz-Kozica, T., Zięba, F., Sergiel, A., & Selva, N. (2019). Bears without borders: Long-distance movement in human-dominated landscapes. Global Ecology and Conservation, 17, e00541. https://doi.org/10.1016/j.gecco.2019.e00541
- Baryshnikov, G. (2010). Middle Pleistocene Ursus thibetanus (Mammalia, carnivora) from Kudaro caves in the Caucasus. Proceedings of the Zoological Institute of the Russian Academy of Sciences, 314, 67–79.
- Blonder, B. (2017). Hypervolume concepts in niche-and trait-based ecology. Ecography, 40, 1–13.
- Bocherens, H., Stiller, M., Hobson, K. A., Pacher, M., Rabeder, G., Burns, J. A., … Hofreiter, M. (2011). Niche partitioning between two sympatric genetically distinct cave bears (Ursus spelaeus and Ursus ingressus) and brown bear (Ursus arctos) from Austria: Isotopic evidence from fossil bones. Quaternary International, 245, 238–248. https://doi.org/10.1016/j.quaint.2010.12.020
- Bon, C., Caudy, N., de Dieuleveult, M., Fosse, P., Philippe, M., Maksud, F., … Elalouf, J.-M. (2008). Deciphering the complete mitochondrial genome and phylogeny of the extinct cave bear in the Paleolithic painted cave of Chauvet. Proceedings of the National Academy of Sciences, 105, 17447–17452. https://doi.org/10.1073/pnas.0806143105
- Brady, E. C., Otto-Bliesner, B. L., Kay, J. E., & Rosenbloom, N. (2013). Sensitivity to glacial forcing in the CCSM4. Journal of Climate, 26, 1901–1925. https://doi.org/10.1175/JCLI-D-11-00416.1
- Brooke, Z. M., Bielby, J., Nambiar, K., & Carbone, C. (2014). Correlates of research effort in carnivores: Body size, range size and diet matter. PLoS ONE, 9(4), e93195. https://doi.org/10.1371/journal.pone.0093195
- Castro-Insua, A., Gómez-Rodríguez, C., Wiens, J. J., & Baselga, A. (2018). Climatic niche divergence drives patterns of diversification and richness among mammal families. Scientific Reports, 8(1), 8781. https://doi.org/10.1038/s41598-018-27068-y
- Collevatti, R. G., Terribile, L. C., Diniz-Filho, J. A., & Lima-Ribeiro, M. S. (2015). Multi-model inference in comparative phylogeography: An integrative approach based on multiple lines of evidence. Frontiers in Genetics, 17, 6–31. https://doi.org/10.3389/fgene.2015.00031
- Collins, W. D., Bitz, C. M., Blackmon, M. L., Bonan, G. B., Bretherton, C. S., Carton, J. A., … Smith, R. D. (2006). The community climate system model version 3 (CCSM3). Journal of Climate, 19, 2122–2143. https://doi.org/10.1175/JCLI3761.1
- Dabney, J., Knapp, M., Glocke, I., Gansauge, M.-T., Weihmann, A., Nickel, B., … Meyer, M. (2013). Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proceedings of the National Academy of Sciences, 110, 15758–15763. https://doi.org/10.1073/pnas.1314445110
- Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). JModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9, 772–772. https://doi.org/10.1038/nmeth.2109
- de Lima, N. E., Lima-Ribeiro, M. S., Tinoco, C. F., Terribile, L. C., & Collevatti, R. G. (2014). Phylogeography and ecological niche modelling, coupled with the fossil pollen record, unravel the demographic history of a Neotropical swamp palm through the Quaternary. Journal of Biogeography, 41, 673–686. https://doi.org/10.1111/jbi.12269
- de Smith, M. J., Goodchild, M. F., & Longley, P. (2018). Geospatial analysis: a comprehensive guide to principles, techniques and software tools ( 6th ed.). de Smith, Goodchild, Longley and Associates (www.spatialanalysisonline.com). England, UK: The Winchelsea Press, The Book Depository LTD.
- de Souza Muñoz, M. E., De Giovanni, R., de Siqueira, M. F., Sutton, T., Brewer, P., Pereira, R. S., … Canhos, V. P. (2011). openModeller: A generic approach to species’ potential distribution modelling. GeoInformatica, 15, 111–135. https://doi.org/10.1007/s10707-009-0090-7
- Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. https://doi.org/10.1093/molbev/mss075
- Ellis, E. C. (2018). Anthropocene: A very short introduction (Vol. 558). Oxford, UK: Oxford University Press.
10.1093/actrade/9780198792987.001.0001 Google Scholar
- Faurby, S., & Araújo, M. B. (2018). Anthropogenic range contractions bias species climate change forecasts. Nature Climate Change, 8, 252–256. https://doi.org/10.1038/s41558-018-0089-x
- Goslee, S. C., & Urban, D. L. (2007). The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software, 22, 1–19.
- Guevara, L., Morrone, J. J., & León-Paniagua, L. (2018). Spatial variability in species' potential distributions during the Last Glacial Maximum under different Global Circulation Models: Relevance in evolutionary biology. Journal of Zoological Systematics and Evolutionary Research, 2018, 1–14.
- Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. https://doi.org/10.1093/sysbio/syq010
- Hardin, G. (1960). The competitive exclusion principle. Science, 131(3409), 1292–1297. https://doi.org/10.1126/science.131.3409.1292
- Hassanin, A. (2015). The role of Pleistocene glaciations in shaping the evolution of polar and brown bears. Evidence from a critical review of mitochondrial and nuclear genome analyses. Comptes Rendus Biologies, 338, 494–501.
- Hasumi, H., & Emori, S. (2004). K-1 coupled GCM (MIROC) description. Tokyo, Japan: Center for Climate System Research, University of Tokyo.
- Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978. https://doi.org/10.1002/joc.1276
- Holt, R. D. (2014). Evolution of the ecological niche. In J. B. Losos (Ed.), The Princeton guide to evolution (pp. 288–297). Princeton, NJ: Princeton University Press.
- Hutchinson, G. E. (1978). An introduction to population ecology. Yale, NH: Yale University Press.
- IUCN. (2017). The IUCN Red List of Threatened Species. Version 2017–3. Retrieved from http://www.iucnredlist.org
- Jiménez, L., Soberón, J., Christen, J. A., & Soto, D. (2019). On the problem of modeling a fundamental niche from occurrence data. Ecological Modelling, 397, 74–83. https://doi.org/10.1016/j.ecolmodel.2019.01.020
- Johnson, H. E., Lewis, D. L., Verzuh, T. L., Wallace, C. F., Much, R. M., Willmarth, L. K., & Breck, S. W. (2018). Human development and climate affect hibernation in a large carnivore with implications for human-carnivore conflicts. Journal of Applied Ecology, 55, 663–672. https://doi.org/10.1111/1365-2664.13021
- Kalkvik, H. M., Stout, I. J., Doonan, T. J., & Parkinson, C. L. (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.
- Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., … Drummond, A. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
- Khaliq, I., Fritz, S. A., Prinzinger, R., Pfenninger, M., Böhning-Gaese, K., & Hof, C. (2015). Global variation in thermal physiology of birds and mammals: Evidence for phylogenetic niche conservatism only in the tropics. Journal of Biogeography, 42, 2187–2196. https://doi.org/10.1111/jbi.12573
- Knapp, M., Rohland, N., Weinstock, J., Baryshnikov, G., Sher, A., Nagel, D., … Hofreiter, M. (2009). First DNA sequences from Asian cave bear fossils reveal deep divergences and complex phylogeographic patterns. Molecular Ecology, 18, 1225–1238. https://doi.org/10.1111/j.1365-294X.2009.04088.x
- Krause, J., Unger, T., Noçon, A., Malaspinas, A.-S., Kolokotronis, S.-O., Stiller, M., … Hofreiter, M. (2008). Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. BMC Evolutionary Biology, 8, 220. https://doi.org/10.1186/1471-2148-8-220
- Kumar, V., Lammers, F., Bidon, T., Pfenninger, M., Kolter, L., Nilsson, M. A., & Janke, A. (2017). The evolutionary history of bears is characterized by gene flow across species. Scientific Reports, 7, 46487. https://doi.org/10.1038/srep46487
- Kutschera, V. E., Bidon, T., Hailer, F., Rodi, J. L., Fain, S. R., & Janke, A. (2014). Bears in a forest of gene trees: Phylogenetic inference is complicated by incomplete lineage sorting and gene flow. Molecular Biology and Evolution, 31, 2004–2017. https://doi.org/10.1093/molbev/msu186
- Lefort, V., Longueville, J. E., & Gascuel, O. (2017). SMS: Smart model selection in PhyML. Molecular Biology and Evolution, 34, 2422–2424. https://doi.org/10.1093/molbev/msx149
- Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. https://doi.org/10.1093/bioinformatics/btp187
- Liu, S., Lorenzen, E. D., Fumagalli, M., Li, B. O., Harris, K., Xiong, Z., … Wang, J. (2014). Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell, 157, 785–794. https://doi.org/10.1016/j.cell.2014.03.054
- Lomolino, M. V., Riddle, B. R., Whittaker, R. J., & Brown, J. H. (2010). Biogeography. Sunderland, MA: Sinauer.
- Losos, J. B. (2008). Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters, 11, 995–1003. https://doi.org/10.1111/j.1461-0248.2008.01229.x
- McLellan, B., & Reiner, D. C. (1980). A review of bear evolution. International Conference of Bear Reasearch and Management 9 (pp. 85–96).
- Miller, E. T., Zanne, A. E., & Ricklefs, R. E. (2013). Niche conservatism constrains Australian honeyeater assemblages in stressful environments. Ecology Letters, 16, 1186–1194. https://doi.org/10.1111/ele.12156
- Münzel, S. C., Rivals, F., Pacher, M., Döppes, D., Rabeder, G., Conard, N. J., & Bocherens, H. (2014). Behavioural ecology of Late Pleistocene bears (Ursus spelaeus, Ursus ingressus): Insight from stable isotopes (C, N, O) and tooth microwear. Quaternary International, 339, 148–163. https://doi.org/10.1016/j.quaint.2013.10.020
- Obbard, M. E., Cattet, M. R., Howe, E. J., Middel, K. R., Newton, E. J., Kolenosky, G. B., & Greenwood, C. J. (2016). Trends in body condition in polar bears (Ursus maritimus) from the Southern Hudson Bay subpopulation in relation to changes in sea ice. Arctic Science, 2, 15–32.
- Osorio-Olvera, L., Barve, V., & Soberón, J. (2017). Nichetoolbox: From getting biodiversity data to evaluating species distribution models in a friendly GUI environment. R package version 0.2.0.0. Retrieved from https://github.com/luismurao/ntbox
- Peterson, A. T., Papeş, M., & Soberón, J. (2008). Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modelling, 213, 63–72. https://doi.org/10.1016/j.ecolmodel.2007.11.008
- Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modeling, 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
- Pigeon, K. E., Stenhouse, G., & Côté, S. D. (2016). Drivers of hibernation: Linking food and weather to denning behaviour of grizzly bears. Behavioral Ecology and Sociobiology, 70, 1745–1754. https://doi.org/10.1007/s00265-016-2180-5
- Puckett, E. E., Etter, P. D., Johnson, E. A., & Eggert, L. S. (2015). Phylogeographic analyses of American black bears (Ursus americanus) suggest four glacial refugia and complex patterns of postglacial admixture. Molecular Biology and Evolution, 32, 2338–2350.
- Raia, P., Passaro, F., Fulgione, D., & Carotenuto, F. (2011). Habitat tracking, stasis and survival in Neogene large mammals. Biology Letters, 8, 64–66.
- Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904.
- Rangel, T. F., Edwards, N. R., Holden, P. B., Diniz-Filho, J. A. F., Gosling, W. D., Coelho, M. T. P., … Colwell, R. K. (2018). Modeling the ecology and evolution of biodiversity: Biogeographical cradles, museums, and graves. Science, 361(6399), eaar5452. https://doi.org/10.1126/science.aar5452
- Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
- Richards, C. L., Carstens, B. C., & Knowles, L. L. (2007). Distribution modelling and statistical phylogeography: An integrative framework for generating and testing alternative biogeographical hypotheses. Journal of Biogeography, 34, 1833–1845. https://doi.org/10.1111/j.1365-2699.2007.01814.x
- Rolland, J., Silvestro, D., Schluter, D., Guisan, A., Broennimann, O., & Salamin, N. (2018). The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity. Nature Ecology and Evolution, 2, 459–464. https://doi.org/10.1038/s41559-017-0451-9
- Saupe, E. E., Barve, N., Owens, H. L., Cooper, J. C., Hosner, P. A., & Peterson, A. T. (2017). Reconstructing ecological niche evolution when niches are incompletely characterized. Systematic Biology, 67, 428–438. https://doi.org/10.1093/sysbio/syx084
- Schliep, K. P. (2010). phangorn: Phylogenetic analysis in R. Bioinformatics, 27, 592–593.
- Schluter, D., Price, T., Mooers, A. Ø., & Ludwig, D. (1997). Likelihood of ancestor states in adaptive radiation. Evolution, 51, 1699–1711. https://doi.org/10.1111/j.1558-5646.1997.tb05095.x
- Segurado, P. A. G. E., Araújo, M. B., & Kunin, W. E. (2006). Consequences of spatial autocorrelation for niche-based models. Journal of Applied Ecology, 43, 433–444. https://doi.org/10.1111/j.1365-2664.2006.01162.x
- Smith, B. T., Bryson, R. W. Jr, Houston, D. D., & Klicka, J. (2012). An asymmetry in niche conservatism contributes to the latitudinal species diversity gradient in New World vertebrates. Ecology Letters, 15, 1318–1325. https://doi.org/10.1111/j.1461-0248.2012.01855.x
- Soberón, J. (2007). Grinnellian and Eltonian niches and geographic distributions of species. Ecology Letters, 10, 1115–1123. https://doi.org/10.1111/j.1461-0248.2007.01107.x
- Soberón, J., & Nakamura, M. (2009). Niches and distributional areas: Concepts, methods, and assumptions. Proceedings of the National Academy of Sciences, 106, 19644–19650. https://doi.org/10.1073/pnas.0901637106
- Stiller, M., Knapp, M., Stenzel, U., Hofreiter, M., & Meyer, M. (2009). Direct multiplex sequencing (DMPS)—A novel method for targeted high-throughput sequencing of ancient and highly degraded DNA. Genome Research, 19, 1843–1848. https://doi.org/10.1101/gr.095760.109
- Stockwell, D. (1999). The GARP modelling system: Problems and solutions to automated spatial prediction. International Journal of Geographical Information Science, 13, 143–158. https://doi.org/10.1080/136588199241391
- Stuart-Smith, R. D., Edgar, G. J., & Bates, A. E. (2017). Thermal limits to the geographic distributions of shallow-water marine species. Nature Ecology and Evolution, 1, 1846–1852. https://doi.org/10.1038/s41559-017-0353-x
- Suárez-Atilano, M., Rojas-Soto, O., Parra, J. L., & Vázquez-Domínguez, E. (2017). The role of the environment on the genetic divergence between two Boa imperator lineages. Journal of Biogeography, 44, 2045–2056.
- Swanson, H. K., Lysy, M., Power, M., Stasko, A. D., Johnson, J. D., & Reist, J. D. (2015). A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap. Ecology, 96, 318–324.
- Varela, S., Lima-Ribeiro, M. S., & Terribile, L. C. (2015). A short guide to the climatic variables of the last glacial maximum for biogeographers. PlosOne, 10(6), e0129037. https://doi.org/10.1371/journal.pone.0129037
- Varela, S., Lobo, J. M., & Hortal, J. (2011). Using species distribution models in paleobiogeography: A matter of data, predictors and concepts. Palaeogeography Palaeoclimatology, Palaeoecology, 310, 451–463. https://doi.org/10.1016/j.palaeo.2011.07.021
- Vieites, D. R., Nieto-Román, S., & Wake, D. B. (2009). Reconstruction of the climate envelopes of salamanders and their evolution through time. Proceedings of the National Academy of Sciences, 106, 19715–19722. https://doi.org/10.1073/pnas.0902956106
- Wang, I. J. (2013). Examining the full effects of landscape heterogeneity on spatial genetic variation: A multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution, 67, 3403–3411. https://doi.org/10.1111/evo.12134
- Wang, I. J., Glor, R. E., & Losos, J. B. (2013). Quantifying the roles of ecology and geography in spatial genetic divergence. Ecology Letters, 16, 175–182. https://doi.org/10.1111/ele.12025
- Webb, C. O., Ackerly, D. D., McPeek, M. A., & Donoghue, M. J. (2002). Phylogenies and community ecology. Annual Review of Eecology and Systematics, 33, 475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
10.1146/annurev.ecolsys.33.010802.150448 Google Scholar
- Wiens, J. J., & Graham, C. H. (2005). Niche conservatism: Integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519–539. https://doi.org/10.1146/annurev.ecolsys.36.102803.095431
- Wooten, J. A., & Gibbs, H. L. (2012). Niche divergence and lineage diversification among closely related Sistrurus rattlesnakes. Journal of Evolutionary Biology, 25, 317–328. https://doi.org/10.1111/j.1420-9101.2011.02426.x
- Wu, J., Kohno, N., Mano, S., Fukumoto, Y., Tanabe, H., Hasegawa, M., & Yonezawa, T. (2015). Phylogeographic and demographic analysis of the Asian Black Bear (Ursus thibetanus) based on mitochondrial DNA. PlosOne, 10(9), e0136398. https://doi.org/10.1371/journal.pone.0136398
- Yannic, G., Ortego, J., Pellissier, L., Lecomte, N., Bernatchez, L., & Côté, S. D. (2017). Linking genetic and ecological differentiation in an ungulate with a circumpolar distribution. Ecography, 41, 922–937. https://doi.org/10.1111/ecog.02995
- Yoder, J. B., Clancey, E., Des roches, S., Eastman, J. M., Gentry, L., Godsoe, W., … Harmon, L. J. (2010). Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology, 23, 1581–1596. https://doi.org/10.1111/j.1420-9101.2010.02029.x
