Morphological innovation, diversification and invasion of a new adaptive zone

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1734, 2012, Pages 1797-1805

  Dumont, Elizabeth R ^a   Dávalos, Liliana M ^b   Goldberg, Aaron ^b   Santana, Sharlene E ^a,c   Rex, Katja ^d   Voigt, Christian C ^d  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

Author keywords

Bats; Diversification; Frugivory; Morphological innovation

Indexed keywords

ADAPTATION; BAT; BIOLOGICAL INVASION; EMPIRICAL ANALYSIS; FRUGIVORY; FUNCTIONAL MORPHOLOGY; PHENOTYPE; SKULL; SPECIATION (BIOLOGY);

CHIROPTERA; MAMMALIA; PHYLLOSTOMIDAE; STENODERMATINAE;

EID: 84858785883     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.2005     Document Type: Article

References (66)

1. Darwin, C. R. 1859 On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 1st edn. London, UK: John Murray.
2. Simpson, G. G. 1944 Tempo and mode in evolution. New York, NY: Columbia University Press.
3. Losos, J. B. 2010 Adaptive radiation, ecological opportunity, and evolutionary determinism. Am. Nat. 175, 623-639. (doi:10.1086/652433)
4. Rabosky, D. L. & Glor, R. E. 2010 Equilibrium speciation dynamics in a model adaptive radiation of island lizards. Proc. Natl Acad. Sci. USA 107, 22 178-22 183. (doi:10.1073/pnas.1007606107)
5. Bininda-Emonds, O. R. P. et al. 2007 The delayed rise of present-day mammals. Nature 446, 507-512. (doi:10. 1038/nature05634)
6. Rabosky, D. L. & Lovette, I. J. 2008 Density-dependent diversification in North American wood warblers. Proc. R. Soc. B 275, 2363-2371. (doi:10.1098/rspb.2008.0630)
7. Schluter, D. 2000 The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
8. Moore, B. R. & Donoghue, M. J. 2009 A Bayesian approach for evaluating the impact of historical events on rates of diversification. Proc. Natl Acad. Sci. USA 106, 4307-4312. (doi:10.1073/pnas.0807230106)
9. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates.
10. Heard, S. B. & Hauser, D. L. 1995 Key evolutionary innovations and their ecological mechanisms. Historical Biol. Int. J. Paleobiol. 10, 151-173.
11. Hunter, J. P. 1998 Key innovations and the ecology of macroevolution. Trends Ecol. Evol. 13, 31-36. (doi:10. 1016/S0169-5347(97)01273-1)
12. von Hagen, K. B. & Kadereit, J. W. 2003 The diversification of Halenia (Gentianaceae): ecological opportunity versus key innovation. Evolution 57, 2507-2518. (doi:10.1111/j.0014-3820.2003.tb01495.x)
13. Alfaro, M., Brock, C., Banbury, B. & Wainwright, P. 2009 Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evol. Biol. 9, 255. (doi:10.1186/1471-2148-9-255)
14. Yoder, J. B. et al. 2010 Ecological opportunity and the origin of adaptive radiations. J. Evol. Biol. 23, 1581-1596. (doi:10.1111/j.1420-9101.2010.02029.x)
15. Rundell, R. J. & Price, T. D. 2009 Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol. Evol. 24, 394-399. (doi:10.1016/j.tree.2009.02.007)
16. Mayr, E. 1963 Animal species and evolution. Cambridge, MA: Harvard University Press.
17. Van Bocxlaer, I., Loader, S. P., Roelants, K., Biju, S. D., Menegon, M. & Bossuyt, F. 2010 Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327, 679-682. (doi:10.1126/science.1181707)
18. Calsbeek, R. & Smith, T. B. 2008 Experimentally replicated disruptive selection on performance traits in a Caribbean lizard. Evolution 62, 478-484. (doi:10.1111/j.1558-5646.2007.00282.x)
19. Rex, K., Michener, R., Kunz, T. H. & Voigt, C. C. 2011 Vertical stratification of neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. J. Trop. Ecol. 27, 211-222. (doi:10.1017/S0266467411000022)
20. Giannini, N. P. & Kalko, E. K. 2004 Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105, 209-220. (doi:10.1111/j.0030-1299.2004.12690.x)
21. Freeman, P. W. 2000 Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evol. Ecol. Res. 2, 317-335.
22. Aguirre, L. F., Herrel, A., Van Damme, R. &Matthysen, E. 2003 The implications of food hardness for diet in bats. Funct. Ecol. 17, 201-212. (doi:10.1046/j.1365-2435.2003.00721.x)
23. Santana, S. E., Dumont, E. R. & Davis, J. L. 2010 Mechanics of bite force production and its relationship to diet in bats. Funct. Ecol. 24, 776-784. (doi:10.1111/j.1365-2435.2010.01703.x)
24. Dumont, E. R., Herrel, A., Medellín, R. A., Vargas-Contreras, J. A. & Santana, S. E. 2009 Built to bite: cranial design and function in the wrinkle-faced bat. J. Zool. 279, 329-337. (doi:10.1111/j.1469-7998.2009.00618.x)
25. Jones, K. E., Bininda-Emonds, O. R. P., Gittleman, J. L. & Yoder, A. 2005 Bats, clocks, and rocks: diversification patterns in Chiroptera. Evolution 59, 2243-2255. (doi:10.1554/04-635.1)
26. Freckleton, R. P., Phillimore, A. B. & Pagel, M. 2008 Relating traits to diversification: a simple test. Am. Nat. 172, 102-115. (doi:10.1086/588076)
27. Paradis, E. 2005 Statistical analysis of diversification with species traits. Evolution 59, 1-12. (doi:10.1554/04-231)
28. Santana, S. E. & Dumont, E. R. 2009 Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats. J. Evol. Biol. 22, 2131-2145. (doi:10.1111/j.1420-9101.2009.01827.x)
29. Gavrilets, S. & Losos, J. B. 2009 Adaptive radiation: contrasting theory with data. Science 323, 732-737. (doi:10. 1126/science.1157966)
30. Baker, R. J., Porter, C. A., Hoofer, S. R. & Van Den Bussche, R. A. 2003 A new higher-level classification of New World leaf-nosed bats based on nuclear and mitochondrial DNA sequences. Occasional Pap. Mus. Texas Tech. Univ. 230, 1-32.
31. Teeling, E. C., Madsen, O., Murphy, W. J., Springer, M. S. & O'Brien, S. J. 2003 Nuclear gene sequences confirm an ancient link between New Zealand's short-tailed bat and South American noctilionoid bats. Mol. Phylogenet. Evol. 28, 308-319. (doi:10.1016/S1055-7903(03) 00117-9)
32. Bininda-Emonds, O. R. P. 2005 TransAlign: using amino acids to facilitate the multiple alignment of proteincoding DNA sequences. BMC Bioinformatics 6, 156. (doi:10.1186/1471-2105-6-156)
33. Katoh, K. & Toh, H. 2008 Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9, 212. (doi:10.1186/1471-2105-9-212)
34. McGuire, J. A., Witt, C. C., Altshuler, D. L. & Remsen Jr, J. V. 2007 Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Syst. Biol. 56, 837-856. (doi:10. 1080/10635150701656360)
35. Ronquist, F. & Huelsenbeck, J. P. 2003 MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. (doi:10.1093/bioinfor matics/btg180)
36. Stamatakis, A. 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690. (doi:10.1093/bioinformatics/btl446)
37. Posada, D. & Buckley, T. R. 2004 Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53, 793-808. (doi:10.1080/10635150490522304)
38. Nylander, J. A. A. 2004 MrAIC. pl. Uppsala: Evolutionary Biology Centre Uppsala University. Program distributed by the author.
39. Drummond, A. & Rambaut, A. 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214. (doi:10.1186/1471-2148-7-214)
40. Suchard, M. A. & Rambaut, A. 2009 Many-core algorithms for statistical phylogenetics. Bioinformatics 25, 1370-1376. (doi:10.1093/bioinformatics/btp244)
41. Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'Brien, S. J. &Murphy, W. J. 2005A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307, 580-584. (doi:10.1126/science.1105113)
42. Miller-Butterworth, C. M., Murphy, W. J., O'Brien, S. J., Jacobs, D. S., Springer, M. S. & Teeling, E. C. 2007 A family matter: conclusive resolution of the taxonomic position of the long-fingered bats Miniopterus. Mol. Biol. Evol. 24, 1553-1561. (doi:10.1093/molbev/msm076)
43. Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. 2006 Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88. (doi:10.1371/journal.pbio.0040088)
44. Rambaut, A. & Drummond, A. J. 2007 Tracer, v. 1.5. See http://tree.bio.ed.ac.uk/software/tracer/.
45. Burnham, K. P. & Anderson, D. R. 2002 Model selection and multimodel inference. New York, NY: Springer.
46. R Development Core Team 2011 R: a language and environment for statistical computing, v. 2.13.2. Vienna, Austria: R Foundation for Statistical Computing.
47. Rabosky, D. L. 2006 LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol. Bioinformatics Online 2, 273-276.
48. FitzJohn, R. G., Maddison, W. P. & Otto, S. P. 2009 Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, 595-611. (doi:10.1093/sysbio/syp067)
49. Plummer, M., Best, N., Cowles, K. & Vines, K. 2006 CODA: convergence diagnosis and output analysis for MCMC. R news 6, 7-11.
50. Rex, K., Czaczkes, B. I., Michener, R., Kunz, T. H. & Voigt, C. C. 2010 Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17, 37-46. (doi:10. 2980/17-1-3294)
51. Jungers, W. L., Falsetti, A. B. & Wall, C. E. 1995 Shape, relative size, and size-adjustments in morphometrics. Am. J. Phys. Anthropol. 38, 137-161. (doi:10.1002/ajpa.1330380608)
52. Dumont, E. R. & Herrel, A. 2003 The effects of gape angle and bite point on bite force in bats. J. Exp. Biol. 206, 2117-2123. (doi:10.1242/jeb.00375)
53. Anderson, R. A., McBrayer, L. D. & Herrel, A. 2008 Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure. Biol. J. Linn. Soc. 93, 709-720. (doi:10.1111/j.1095-8312.2007.00905.x)
54. Grafen, A. 1989 The phylogenetic regression. Phil. Trans. R. Soc. Lond. B 326, 119-157. (doi:10.1098/rstb.1989.0106)
55. Paradis, E., Claude, J. & Strimmer, K. 2004 APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. (doi:10.1093/bioinfor matics/btg412)
56. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & the R Core team 2009 NLME: linear and nonlinear mixed effects models, v. 3.1-96. See http://cran.r-project.org/web/packages/nlme.
57. Pagel, M. 1997 Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331-348. (doi:10.1111/j. 1463-6409.1997.tb00423.x)
58. O'Meara, B. C., Ané, C., Sanderson, M. J., Wainwright, P. C. & Hansen, T. 2006 Testing for different rates of continuous trait evolution using likelihood. Evolution 60, 922-933. (doi:10.1554/05-130.1)
59. FitzJohn, R. G. 2010 Quantitative traits and diversification. Syst. Biol. 59, 619-633. (doi:10.1093/sysbio/syq053)
60. Kalko, E. K. V. & Handley, C. O. 2001 Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecol. 153, 319-333. (doi:10.1023/A:1017590007861)
61. Dumont, E. R. 1999 The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): an experimental study. J. Zool. 248, 219-229. (doi:10. 1111/j.1469-7998.1999.tb01198.x)
62. Popowics, T. E. 2003 Postcanine dental form in the Mustelidae and Viverridae (Carnivora: Mammalia). J. Morphol. 256, 322-341. (doi:10.1002/jmor.10091)
63. Boyer, D. 2008 Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. J. Hum. Evol. 55, 1118-1137. (doi:10.1016/j.jhevol.2008.08.002)
64. Hunter, J. P. & Jernvall, J. 1995 The hypocone as a key innovation in mammalian evolution. Proc. Natl Acad. Sci. USA 92, 10 718-10 722. (doi:10.1073/pnas.92.23. 10718)
65. Ree, R. H. & Yoder, A. 2005 Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59, 257-265. (doi:10.1554/04-369)
66. Herrel, A., De Smet, A., Aguirre, L. F. & Aerts, P. 2008 Morphological and mechanical determinants of bite force in bats: do muscles matter? J. Exp. Biol. 211, 86-91. (doi:10.1242/jeb.012211)