Ecological and Ecomorphological Specialization Are Not Associated with Diversification Rates in Muroid Rodents (Rodentia: Muroidea)
Abstract
Multiple diversification rate shifts explain uneven clade richness in muroid rodents. Previous muroid studies have shown that extrinsic factors, notwithstanding ecological opportunity, are poor predictors of clade diversity. Here, we use a 297-muroid species chronogram that is sampled proportional to total clade diversity, along with various trait-dependent diversification approaches to investigate the association between diversification rates with intrinsic attributes—diet, habitat, body mass, and relative tail length. We found some association between both dietary specialization and body mass, as well as between habitat specialization with relative tail lengths using phylogenetic analyses of variance. However, there was no significant association between diversification rates with the evolution of these traits in muroid rodents. We also show that several of the state-dependent diversification approaches are highly susceptible to Type I error—a result that is in accordance with recent criticisms of these methods. Finally, we discuss several potential causes for the lack of association between the examined trait data with diversification rates, ranging from methodological biases (e.g. method conservativism) to biology (e.g. behavioral plasticity and ecological opportunism of muroid rodents).
Keywords
Body size Generalization Hidden-state speciation and extinction Multistate characters Quantitative traits Trait-dependent diversificationNotes
Acknowledgements
Earlier versions of the manuscript benefited from comments by Gregory Erickson, Joseph Travis, Thomas Miller, William Parker, and especially John Schenk. We also appreciate correspondence with Daniel Rabosky concerning the general issues with state-dependent diversification methods. An anonymous reviewer contributed useful comments that improved the final version of the manuscript. Financial support for this work was provided by a fellowship from Kuwait University to BHA.
Compliance with ethical standards
Conflict of interest
The authors declare that there is no conflict of interest regarding the publication of this article.
Supplementary material
References
- Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In B. N. Petrov & F. Csaki (Eds.), 2nd International symposium on information theory (pp. 267–281). Budapest: Akademiai Kiado.Google Scholar
- Akaike, H. (1974). A new look at statistical model identification. IEEE Transactions on Automatic Control, 19, 716–723.CrossRefGoogle Scholar
- Alexander, R. M., & Vernon, A. (1975). The mechanics of hopping by kangaroos (Macropodidae). Journal of Zoology, 177(2), 265–303. https://doi.org/10.1111/j.1469-7998.1975.tb05983.x.CrossRefGoogle Scholar
- Alhajeri, B. H. (2014). Adaptation, diversification, and desert ecology of the most diverse order of mammals (Mammalia, Rodentia). Tallahassee, FL: Department of Biological Science, Florida State University.Google Scholar
- Alhajeri, B. H., Schenk, J. J., & Steppan, S. J. (2016). Ecomorphological diversification following continental colonization in muroid rodents (Rodentia: Muroidea). Biological Journal of the Linnean Society, 117(3), 463–481. https://doi.org/10.1111/bij.12695.CrossRefGoogle Scholar
- Beaulieu, J. M., & O’Meara, B. C. (2016). Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Systematic Biology, 65(4), 583. https://doi.org/10.1093/sysbio/syw022.PubMedCrossRefGoogle Scholar
- Blois, J. L., & Hadly, E. A. (2009). Mammalian response to Cenozoic climatic change. Annual Review of Earth and Planetary Sciences, 37, 181–208. https://doi.org/10.1146/annurev.earth.031208.100055.CrossRefGoogle Scholar
- Blueweiss, L., Fox, H., Kudzma, V., Nakashima, D., Peters, R., & Sams, S. (1978). Relationships between body size and some life history parameters. Oecologia, 37(2), 257–272. https://doi.org/10.1007/BF00344996.PubMedCrossRefGoogle Scholar
- Bozdogan, H. (1987). Model selection and Akaike’s information criterion (AIC): The general theory and its analytical extensions. Psychometrika, 52(3), 345–370. https://doi.org/10.1007/BF02294361.CrossRefGoogle Scholar
- Büchi, L., & Vuilleumier, S. (2014). Coexistence of specialist and generalist species is shaped by dispersal and environmental factors. The American Naturalist, 183(5), 612–624. https://doi.org/10.1086/675756.PubMedCrossRefGoogle Scholar
- Burin, G., Kissling, W. D., Guimarães, P. R. Jr, Şekercioğlu, Ç. H., & Quental, T. B. (2016). Omnivory in birds is a macroevolutionary sink. Nature Communications, 7, 11250. https://doi.org/10.1038/ncomms11250.PubMedPubMedCentralCrossRefGoogle Scholar
- Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach. New York: Springer.Google Scholar
- Cantalapiedra, J. L., Fitzjohn, R. G., Kuhn, T. S., Fernández, M. H., DeMiguel, D., Azanza, B., et al. (2014). Dietary innovations spurred the diversification of ruminants during the Caenozoic. Proceedings of the Biological Sciences/The Royal Society, 281(1776), 20132746. https://doi.org/10.1098/rspb.2013.2746.CrossRefGoogle Scholar
- Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J., Bininda-Emonds, O. R. P., Sechrest, W., et al. (2005). Multiple causes of high extinction risk in large mammal species. Science, 309(5738), 1239–1241. https://doi.org/10.1126/science.1116030.PubMedCrossRefGoogle Scholar
- Carleton, M. D., & Musser, G. G. (1984). Muroid rodents. In S. Anderson & J. K. Jones Jr. (Eds.), Orders and families of recent mammals of the world (pp. 289–379). New York: Wiley.Google Scholar
- Clauset, A., & Erwin, D. H. (2008). The evolution and distribution of species body size. Science, 321(5887), 399–401. https://doi.org/10.1126/science.1157534.PubMedCrossRefGoogle Scholar
- Collar, D. C., O’Meara, B. C., Wainwright, P. C., & Near, T. J. (2009). Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution, 63(6), 1557–1573. https://doi.org/10.1111/j.1558-5646.2009.00626.x.PubMedCrossRefGoogle Scholar
- Corti, M., & Loy, A. (1987). Morphometric divergence in southern European moles (Insectívora, Talpidae). Bolletino di Zoologia, 54(2), 187–191. https://doi.org/10.1080/11250008709355580.CrossRefGoogle Scholar
- Culver, D. C., & Pipan, T. (2014). Shallow Subterranean habitats: Ecology, evolution, and conservation. Oxford: Oxford University Press.CrossRefGoogle Scholar
- Dawson, N. J., & Keber, A. W. (1979). Physiology of heat loss from an extremity: The tail of the rat. Clinical and Experimental Pharmacology and Physiology, 6(1), 69–80. https://doi.org/10.1111/j.1440-1681.1979.tb00009.x.PubMedCrossRefGoogle Scholar
- Deacon, R. M. J. (2006). Burrowing in rodents: A sensitive method for detecting behavioral dysfunction. Nature Protocols, 1(1), 118–121. https://doi.org/10.1038/nprot.2006.19.PubMedCrossRefGoogle Scholar
- Dial, K. P., & Marzluff, J. M. (1988). Are the smallest organisms the most diverse? Ecology, 69(5), 1620–1624. https://doi.org/10.2307/1941660.CrossRefGoogle Scholar
- Ebel, E. R., DaCosta, J. M., Sorenson, M. D., Hill, R. I., Briscoe, A. D., Willmott, K. R., et al. (2015). Rapid diversification associated with ecological specialization in Neotropical Adelpha butterflies. Molecular Ecology, 24(10), 2392–2405. https://doi.org/10.1111/mec.13168.PubMedCrossRefGoogle Scholar
- Etienne, R. S., de Visser, S. N., Janzen, T., Olsen, J. L., Olff, H., & Rosindell, J. (2012). Can clade age alone explain the relationship between body size and diversity? Interface Focus, 2(2), 170–179.PubMedPubMedCentralCrossRefGoogle Scholar
- Fabre, P. H., Hautier, L., Dimitrov, D., Douzery, P., & Emmanuel, J. (2012). A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evolutionary Biology, 12. https://doi.org/10.1186/1471-2148-12-88
- Farrell, B. D., Dussourd, D. E., & Mitter, C. (1991). Escalation of plant defense: Do latex and resin canals spur plant diversification?. The American Naturalist, 138(4), 881–900.CrossRefGoogle Scholar
- Feldman, A., Sabath, N., Pyron, R. A., Mayrose, I., & Meiri, S. (2016). Body sizes and diversification rates of lizards, snakes, amphisbaenians and the tuatara. Global Ecology and Biogeography, 25(2), 187–197. https://doi.org/10.1111/geb.12398.CrossRefGoogle Scholar
- FitzJohn, R. G. (2010). Quantitative traits and diversification. Systematic Biology, 59(6), 619–633. https://doi.org/10.1093/sysbio/syq053.PubMedCrossRefGoogle Scholar
- FitzJohn, R. G. (2012). Diversitree: Comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution, 3(6), 1084–1092. https://doi.org/10.1111/j.2041-210X.2012.00234.x.CrossRefGoogle Scholar
- FitzJohn, R. G., Maddison, W. P., & Otto, S. P. (2009). Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Systematic Biology, 58(6), 595–611. https://doi.org/10.1093/sysbio/syp067.PubMedCrossRefGoogle Scholar
- Fooden, J., & Albrecht, G. H. (1999). Tail-length evolution in fascicularis -group Macaques (Cercopithecidae: Macaca). International Journal of Primatology, 20, 431–440.CrossRefGoogle Scholar
- Freckleton, R. P., Phillimore, A. B., & Pagel, M. (2008). Relating traits to diversification: A simple test. The American Naturalist, 172(1), 102–115. https://doi.org/10.1086/588076.PubMedCrossRefGoogle Scholar
- Gamisch, A. (2016). Notes on the statistical power of the binary state speciation and extinction (BiSSE) model. Evolutionary Bioinformatics, 12, 165–174. https://doi.org/10.4137/EBO.S39732.CrossRefGoogle Scholar
- Gardezi, T., & da Silva, J. (1999). Diversity in relation to body size in mammals: A comparative study. The American Naturalist, 153(1), 110–123. https://doi.org/10.1086/303150.PubMedCrossRefGoogle Scholar
- Garland, T., Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42(3), 265–292. https://doi.org/10.1093/sysbio/42.3.265.CrossRefGoogle Scholar
- Gittleman, J. L., & Purvis, A. (1998). Body size and species-richness in carnivores and primates. Proceedings of the Biological sciences/The Royal Society, 265(1391), 113–119. https://doi.org/10.1098/rspb.1998.0271.CrossRefGoogle Scholar
- Goldberg, E. E., Kohn, J. R., Lande, R., Robertson, K. A., Smith, S. A., & Igić, B. (2010). Species selection maintains self-incompatibility. Science, 330(6003), 493–495. https://doi.org/10.1126/science.1194513.PubMedCrossRefGoogle Scholar
- Goldberg, E. E., Lancaster, L. T., & Ree, R. H. (2011). Phylogenetic inference of reciprocal effects between geographic range evolution and diversification. Systematic Biology, 60(4), 451–465. https://doi.org/10.1093/sysbio/syr046.PubMedCrossRefGoogle Scholar
- Harmon, L. J., Melville, J., Larson, A., & Losos, J. B. (2008). the role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). Systematic Biology, 57(4), 562–573. https://doi.org/10.1080/10635150802304779.PubMedCrossRefGoogle Scholar
- Hayssen, V. (2008). Patterns of body and tail length and body mass in Sciuridae. Journal of Mammalogy, 89(4), 852–873. https://doi.org/10.1644/07-MAMM-A-217.1.CrossRefGoogle Scholar
- Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6(2), 65–70. https://doi.org/10.2307/4615733.Google Scholar
- Hunter, J. P. (1998). Key innovations and the ecology of macroevolution. Trends in Ecology & Evolution, 13, 31-36.CrossRefGoogle Scholar
- Hutchinson, G. E., & MacArthur, R. A. (1959). A theoretical ecological model of size distributions among species of animals. American Naturalist, 93, 117–125.CrossRefGoogle Scholar
- Igea, J., Miller, E. F., Papadopulos, A. S. T., & Tanentzap, A. J. (2016). Seed size drives species diversification across angiosperms. bioRxiv. http://biorxiv.org/content/early/2016/05/12/053116.abstract.
- Isaac, N. J., Jones, K. E., Gittleman, J. L., & Purvis, A. (2005). Correlates of species richness in mammals: Body size, life history, and ecology. The American Naturalist, 165(5), 600–607.PubMedCrossRefGoogle Scholar
- Janis, C. M. (1993). Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecology and Systematics, 24, 467–500. https://doi.org/10.1146/annurev.es.24.110193.002343.CrossRefGoogle Scholar
- Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26(11), 1463–1464. https://doi.org/10.1093/bioinformatics/btq166.PubMedCrossRefGoogle Scholar
- Khanna, D. R., & Yadav, P. R. (2005). Biology of mammals. New Delhi: Discovery Publishing House.Google Scholar
- Kochmer, J. P., & Wagner, R. H. (1988). Why are there so many kinds of passerine birds? Because they are small. a reply to raikow. Systematic Biology, 37(1), 68–69. https://doi.org/10.2307/2413193.Google Scholar
- LaBarbera, M. (1989). Analyzing body size as a factor in ecology and evolution. Annual Review of Ecology and Systematics, 20(1), 97–117. https://doi.org/10.1146/annurev.es.20.110189.000525.CrossRefGoogle Scholar
- Langerhans, R. B. (2010). Predicting evolution with generalized models of divergent selection: A case study with Poeciliid Fish. Integrative and Comparative Biology, 50(6), 1167–1184. https://doi.org/10.1093/icb/icq117.PubMedCrossRefGoogle Scholar
- Lemen, C. (1980). Relationship between relative brain size and climbing ability in peromyscus. Journal of Mammalogy, 61(2), 360–364.CrossRefGoogle Scholar
- Liow, L. H. (2004). A test of Simpson’s “rule of the survival of the relatively unspecialized” using fossil crinoids. The American Naturalist, 164(4), 431–443. https://doi.org/10.1086/423673.PubMedGoogle Scholar
- Liow, L. H., Fortelius, M., Bingham, E., Lintulaakso, K., Mannila, H., Flynn, L., & Stenseth, N. C. (2008). Higher origination and extinction rates in larger mammals. Proceedings of the National Academy of Sciences of the United States of America, 105(16), 6097–6102. https://doi.org/10.1073/pnas.0709763105.PubMedPubMedCentralCrossRefGoogle Scholar
- Liow, L. H., Fortelius, M., Lintulaakso, K., Mannila, H., & Stenseth, N. C. (2009). Lower extinction risk in sleep-or-hide mammals. The American Naturalist, 173(2), 264–272. https://doi.org/10.1086/595756.PubMedCrossRefGoogle Scholar
- Little, R. A., & Stoner, H. B. (1968). The measurement of heat loss from the rat’s tail. Quarterly Journal of Experimental Physiology and Cognate Medical Sciences, 53(1), 76–83. https://doi.org/10.1113/expphysiol.1968.sp001947.PubMedCrossRefGoogle Scholar
- Lobato, F. L., Barneche, D. R., Siqueira, A. C., Liedke, A. M. R., Lindner, A., Pie, M. R., et al. (2014). Diet and diversification in the evolution of coral reef fishes. PLoS ONE, 9(7), e102094.PubMedPubMedCentralCrossRefGoogle Scholar
- Lowman, M., & Rinker, H. B. (2004). Forest canopies. Cambridge: Academic Press.Google Scholar
- Machac, A. (2014). Detecting trait-dependent diversification under diversification slowdowns. Evolutionary Biology, 41(2), 201–211. https://doi.org/10.1007/s11692-013-9258-z.CrossRefGoogle Scholar
- Maddison, W. P., Midford, P. E., & Otto, S. P. (2007). Estimating a Binary character’s effect on speciation and extinction. Systematic Biology, 56(5), 701–710. https://doi.org/10.1080/10635150701607033.PubMedCrossRefGoogle Scholar
- Mares, M. A. (2009). A desert calling: Life in a forbidding landscape. Cambridge: Harvard University Press.Google Scholar
- Martin, R. A. (1992). Generic species richness and body mass in North American mammals: Support for the inverse relationship of body size and speciation rate. Historical Biology, 6(2), 73–90. https://doi.org/10.1080/10292389209380420.CrossRefGoogle Scholar
- Martin, S. A., Alhajeri, B. H., & Steppan, S. J. (2016). Dietary adaptations in the teeth of murine rodents (Muridae): A test of biomechanical predictions. Biological Journal of the Linnean Society, 119(4), 766–784. https://doi.org/10.1111/bij.12822.CrossRefGoogle Scholar
- Matthews, L. J., Arnold, C., Machanda, Z., & Nunn, C. L. (2011). Primate extinction risk and historical patterns of speciation and extinction in relation to body mass. Proceedings of the Royal Society B: Biological Sciences, 278(1709), 1256–1263. https://doi.org/10.1098/rspb.2010.1489.PubMedCrossRefGoogle Scholar
- May, R. M. (1986). The search for patterns in the balance of nature advances and retreats. Ecology, 67, 1115–1126.CrossRefGoogle Scholar
- Mitter, C. B., Farrell, B., & Wiegmann, B. (1988). The phylogenetic study of adaptive zones: Has phytophagy promoted insect diversification? American Naturalist, 132(1), 107–128.CrossRefGoogle Scholar
- Monroe, M. J., & Bokma, F. (2009). Do speciation rates drive rates of body size evolution in mammals? The American naturalist, 174(6), 912–918. https://doi.org/10.1086/646606.PubMedCrossRefGoogle Scholar
- Moore, B. R., & Donoghue, M. J. (2007). Correlates of diversification in the plant clade dipsacales: Geographic movement and evolutionary innovations. The American Naturalist, 170, S28–S55.PubMedCrossRefGoogle Scholar
- Musser, G. G., & Carleton, M. D. (2005). Superfamily Muroidea. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world (3rd ed., pp. 894–1531). Baltimore: The Johns Hopkins University Press.Google Scholar
- Nevo, E. (1985). Speciation in action and adaptation in subterranean mole rats: Patterns and theory. Bolletino di Zoologia, 52(1–2), 65–95. https://doi.org/10.1080/11250008509440344.CrossRefGoogle Scholar
- Ng, J., & Smith, S. D. (2014). How traits shape trees: New approaches for detecting character state-dependent lineage diversification. Journal of Evolutionary Biology, 27(10), 2035–2045. https://doi.org/10.1111/jeb.12460.PubMedCrossRefGoogle Scholar
- Nowak, R. M. (1999). Walker’s mammals of the world. Volume 1 and 2 (6th ed.). Baltimore: John Hopkins University Press.Google Scholar
- Pabinger, S., Rödiger, S., Kriegner, A., Vierlinger, K., & Weinhäusel, A. (2014). A survey of tools for the analysis of quantitative PCR (qPCR) data. Biomolecular Detection and Quantification, 1(1), 23–33. https://doi.org/10.1016/j.bdq.2014.08.002.PubMedPubMedCentralCrossRefGoogle Scholar
- Parada, A., D’Elía, G., & Palma, R. E. (2015). The influence of ecological and geographical context in the radiation of Neotropical sigmodontine rodents. BMC Evolutionary Biology, 15(1), 172. https://doi.org/10.1186/s12862-015-0440-z.PubMedPubMedCentralCrossRefGoogle Scholar
- Paradis, E. (2005). Statistical analysis of diversification with species traits. Evolution, 59(1), 1–12. https://doi.org/10.1111/j.0014-3820.2005.tb00889.x.PubMedCrossRefGoogle Scholar
- Parent, C. E., & Crespi, B. J. (2009). Ecological opportunity in adaptive radiation of Galápagos endemic land snails. The American Naturalist, 174, 898–905.PubMedCrossRefGoogle Scholar
- Peters, R. H. (1983). The ecological implications of body size. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
- Pineda-Munoz, S., & Alroy, J. (2014). Dietary characterization of terrestrial mammals. Proceedings of the Royal Society B: Biological Sciences, 281(1789), 20141173PubMedPubMedCentralCrossRefGoogle Scholar
- Pineda-Munoz, S., Evans, A. R., & Alroy, J. (2016). The relationship between diet and body mass in terrestrial mammals. Paleobiology, 42(4), 659–669.CrossRefGoogle Scholar
- Pinto, G., Mahler, D. L., Harmon, L. J., & Losos, J. B. (2008). Testing the island effect in adaptive radiation: Rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards. Proceedings of the Royal Society B: Biological Sciences, 275(1652), 2749–2757. https://doi.org/10.1098/rspb.2008.0686.PubMedPubMedCentralCrossRefGoogle Scholar
- Plummer, M., Best, N., Cowles, K., & Vines, K. (2010). Coda: Output analysis and diagnostics for MCMC. R package version 0.14-2Google Scholar
- Price, S. A., Hopkins, S. S. B., Smith, K. K., & Roth, V. L. (2012). Tempo of trophic evolution and its impact on mammalian diversification. Proceedings of the National Academy of Sciences, 109(18), 7008–7012. https://doi.org/10.1073/pnas.1117133109.CrossRefGoogle Scholar
- Price, S. L., Powell, S., Kronauer, D. J. C., Tran, L. A. P., Pierce, N. E., & Wayne, R. K. (2014a). Renewed diversification is associated with new ecological opportunity in the Neotropical turtle ants. Journal of Evolutionary Biology, 27(2), 242–258. https://doi.org/10.1111/jeb.12300.PubMedCrossRefGoogle Scholar
- Price, T. D., Hooper, D. M., Buchanan, C. D., Johansson, U. S., Tietze, D. T., Alstrom, P., et al. (2014b). Niche filling slows the diversification of Himalayan songbirds. Nature, 509(7499), 222–225. https://doi.org/10.1038/nature13272.PubMedCrossRefGoogle Scholar
- Promislow, D. E. L., & Harvey, P. H. (1990). Living fast and dying young: A comparative analysis of life-history variation among mammals. Journal of Zoology, 220(3), 417–437. https://doi.org/10.1111/j.1469-7998.1990.tb04316.x.CrossRefGoogle Scholar
- Pyron, R. A., & Burbrink, F. T. (2014). Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecology Letters, 17(1), 13–21. https://doi.org/10.1111/ele.12168.PubMedCrossRefGoogle Scholar
- Rabosky, D. L. (2014). Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE, 9(2), e89543. https://doi.org/10.1371/journal.pone.0089543.PubMedPubMedCentralCrossRefGoogle Scholar
- Rabosky, D. L., & Goldberg, E. E. (2015). Model inadequacy and mistaken inferences of trait-dependent speciation. Systematic Biology, 64(2), 340–355. https://doi.org/10.1093/sysbio/syu131.PubMedCrossRefGoogle Scholar
- Rabosky, D. L., Grundler, M., Anderson, C., Title, P., Shi, J. J., Brown, J. W., et al. (2014). BAMMtools: An R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods in Ecology and Evolution. https://doi.org/10.1111/2041-210X.12199.Google Scholar
- Rabosky, D. L., & Huang, H. (2016). A robust semi-parametric test for detecting trait-dependent diversification. Systematic Biology, 65(2), 181. https://doi.org/10.1093/sysbio/syv066.PubMedCrossRefGoogle Scholar
- Rabosky, D. L., & Matute, D. R. (2013). Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1305529110.Google Scholar
- Rabosky, D. L., & McCune, A. R. (2010). Reinventing species selection with molecular phylogenies. Trends in Ecology & Evolution, 25(2), 68–74. https://doi.org/10.1016/j.tree.2009.07.002.CrossRefGoogle Scholar
- Rabosky, D. L., Santini, F., Eastman, J., Smith, S. A., Sidlauskas, B., Chang, J., & Alfaro, M. E. (2013). Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications, 4, 1958. https://doi.org/10.1038/ncomms2958.PubMedCrossRefGoogle Scholar
- Read, A. F., & Harvey, P. H. (1989). Life history differences among the eutherian radiations. Journal of Zoology, 219(2), 329–353. https://doi.org/10.1111/j.1469-7998.1989.tb02584.x.CrossRefGoogle Scholar
- Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x.CrossRefGoogle Scholar
- Ricklefs, R. E. (2006). Global variation in the diversification rate of passerine birds. Ecology, 87(10), 2468–2478.PubMedCrossRefGoogle Scholar
- Rojas, D., Vale, Á, Ferrero, V., & Navarro, L. (2012). The role of frugivory in the diversification of bats in the Neotropics. Journal of Biogeography, 39(11), 1948–1960. https://doi.org/10.1111/j.1365-2699.2012.02709.x.CrossRefGoogle Scholar
- Rolland, J., Condamine, F. L., Jiguet, F., & Morlon, H. (2014). Faster speciation and reduced extinction in the tropics contribute to the Mammalian latitudinal diversity gradient. PLoS Biology, 12(1), e1001775. https://doi.org/10.1371/journal.pbio.1001775.PubMedPubMedCentralCrossRefGoogle Scholar
- Sacks, B. N., Bannasch, D. L., Chomel, B. B., & Ernest, H. B. (2008). coyotes demonstrate how habitat specialization by individuals of a generalist species can diversify populations in a heterogeneous ecoregion. Molecular Biology and Evolution, 25(7), 1384–1394. https://doi.org/10.1093/molbev/msn082.PubMedCrossRefGoogle Scholar
- Samuels, J. X. (2009). Cranial morphology and dietary habits of rodents. Zoological Journal of the Linnean Society, 156(4), 864–888. https://doi.org/10.1111/j.1096-3642.2009.00502.x.CrossRefGoogle Scholar
- Santana, S. E., & Cheung, E. (2016). Go big or go fish: Morphological specializations in carnivorous bats. Proceedings of the Royal Society B: Biological Sciences, 283(1830), 20160615.PubMedPubMedCentralCrossRefGoogle Scholar
- Schenk, J. J., Rowe, K. C., & Steppan, S. J. (2013). Ecological opportunity and incumbency in the diversification of repeated continental colonizations by muroid rodents. Systematic Biology, 62(6), 837–864. https://doi.org/10.1093/sysbio/syt050.PubMedCrossRefGoogle Scholar
- Schluter, D. (2000). The ecology of adaptive radiation. Oxford: Oxford University Press.Google Scholar
- Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution, 16(7), 372–380.CrossRefGoogle Scholar
- Shimer, H. W. (1903). Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals. III. Fossorial adaptations. The American Naturalist, 37(444), 819–825.CrossRefGoogle Scholar
- Sibly, R. M., & Brown, J. H. (2007). Effects of body size and lifestyle on evolution of mammal life histories. Proceedings of the National Academy of Sciences of the United States of America, 104(45), 17707–17712. https://doi.org/10.1073/pnas.0707725104.PubMedPubMedCentralCrossRefGoogle Scholar
- Simpson, G. G. (1944). The tempo and mode in evolution. New York: Columbia University Press.Google Scholar
- Smits, P. D. (2015). Expected time-invariant effects of biological traits on mammal species duration. Proceedings of the National Academy of Sciences, 112(42), 13015–13020. https://doi.org/10.1073/pnas.1510482112.CrossRefGoogle Scholar
- Steppan, S., Adkins, R., & Anderson, J. (2004). Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology, 53(4), 533–553. https://doi.org/10.1080/10635150490468701.PubMedCrossRefGoogle Scholar
- Stuart, O., & Landry, J. (1970). The Rodentia as omnivores. The Quarterly Review of Biology, 45(4), 351–372. https://doi.org/10.1086/406647.CrossRefGoogle Scholar
- Swihart, R. K. (1984). Body size, breeding season length, and life history tactics of Lagomorphs. Oikos, 43(3), 282–290. https://doi.org/10.2307/3544145.CrossRefGoogle Scholar
- Team, R. D. C. (2016). R: A language and environment for statistical computing. Vienna: R Core TeamGoogle Scholar
- Tomiya, S. (2013). Body size and extinction risk in terrestrial mammals above the species level. The American Naturalist, 182(6), E196–E214. https://doi.org/10.1086/673489.PubMedCrossRefGoogle Scholar
- Tran, L. A. P. (2014). The role of ecological opportunity in shaping disparate diversification trajectories in a bicontinental primate radiation. Proceedings of the Royal Society of London B: Biological Sciences, 281(1781), 20131979.CrossRefGoogle Scholar
- Tran, L. A. P. (2016). Interaction between digestive strategy and niche specialization predicts speciation rates across herbivorous mammals. The American Naturalist, 187(4), 468–480. https://doi.org/10.1086/685094.PubMedCrossRefGoogle Scholar
- Vamosi, J. C., Armbruster, W. S., & Renner, S. S. (2014). Evolutionary ecology of specialization: Insights from phylogenetic analysis. Proceedings of the Royal Society of London B: Biological Sciences, 281(1795), 20142004. https://doi.org/10.1098/rspb.2014.2004.CrossRefGoogle Scholar
- Verde Arregoitia, L. D., Fisher, D. O., & Schweizer, M. (2017). Morphology captures diet and locomotor types in rodents. Royal Society Open Science, 4(1), 160957. https://doi.org/10.1098/rsos.160957.PubMedPubMedCentralCrossRefGoogle Scholar
- von Hagen, K. B., & Kadereit, J. W. (2003). The diversification of Halenia (Gentianaceae): Ecological opportunity versus key innovation. Evolution, 57(11), 2507–2518. https://doi.org/10.1111/j.0014-3820.2003.tb01495.x.CrossRefGoogle Scholar
- Wagenmakers, E.-J., & Farrell, S. (2004). AIC model selection using Akaike weights. Psychonomic Bulletin & Review, 11(1), 192–196. https://doi.org/10.3758/BF03206482.CrossRefGoogle Scholar
- Walker, D. M., Castlebury, L. A., Rossman, A. Y., & Struwe, L. (2014). Host conservatism or host specialization? Patterns of fungal diversification are influenced by host plant specificity in Ophiognomonia (Gnomoniaceae: Diaporthales). Biological Journal of the Linnean Society, 111(1), 1–16. https://doi.org/10.1111/bij.12189.CrossRefGoogle Scholar
- Whittow, G. C. (2013). Comparative physiology of thermoregulation: Mammals. Waltham: Academic Press.Google Scholar
- Williams, S., & Kay, R. (2001). A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution, 8(3), 207–229. https://doi.org/10.1023/A:1012231829141.CrossRefGoogle Scholar
- Wilson, D. S., & Yoshimura, J. (1994). On the coexistence of specialists and generalists. The American Naturalist, 144(4), 692–707. https://doi.org/10.1086/285702.CrossRefGoogle Scholar
- Withers, P. C., Cooper, C. E., Cruz-Neto, A. P., & Bozinovic, F. (2016). Ecological and environmental physiology of mammals. Oxford: Oxford University Press.CrossRefGoogle Scholar
- Wollenberg, K. C., Vieites, D. R., Glaw, F., & Vences, M. (2011). Speciation in little: The role of range and body size in the diversification of Malagasy mantellid frogs. BMC Evolutionary Biology, 11(1), 217. https://doi.org/10.1186/1471-2148-11-217.PubMedPubMedCentralCrossRefGoogle Scholar