Small body size increases the regional differentiation of populations of tropical mantellid frogs (Anura: Mantellidae)

Journal of Evolutionary Biology

Volumn 25, Issue 11, 2012, Pages 2310-2324

  Pabijan, M ^a,b   Wollenberg, K C ^c,d   Vences, M ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF TRIER   (Germany)

Author keywords

Allopatric speciation; Gene flow; Microendemic phenotype; Vicariance

Indexed keywords

MITOCHONDRIAL DNA; RNA 16S;

ALLOPATRY; BODY SIZE; DISPERSAL; DIVERGENCE; FROG; GENE FLOW; GENETIC VARIATION; GENOTYPE; GEOGRAPHICAL VARIATION; INTERPOPULATION VARIATION; MICROHABITAT; MITOCHONDRIAL DNA; PHENOTYPE; RAINFOREST; RANGE SIZE; REPRODUCTIVE SUCCESS; SKIN; SPECIATION (BIOLOGY); VICARIANCE;

ANIMAL; ANURA; ARTICLE; BODY SIZE; CLASSIFICATION; ECOSYSTEM; GENE FLOW; GENETIC POLYMORPHISM; GENETICS; HAPLOTYPE; MADAGASCAR; MALE; METABOLISM; METHODOLOGY; PHYLOGENY; PHYSIOLOGY; POPULATION DYNAMICS; POPULATION GENETICS; REPRODUCTION; SKIN; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ANIMALS; ANURA; BODY SIZE; DNA, MITOCHONDRIAL; ECOSYSTEM; GENE FLOW; GENETIC SPECIATION; GENETICS, POPULATION; HAPLOTYPES; MADAGASCAR; MALE; PHYLOGENY; POLYMORPHISM, GENETIC; POPULATION DYNAMICS; REPRODUCTION; RNA, RIBOSOMAL, 16S; SKIN; SPECIES SPECIFICITY;

AMPHIBIA; ANURA; MANTELLINAE;

EID: 84868192282     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02613.x     Document Type: Article

References (100)

1. Agnarsson, I. & Kuntner, M. 2012. The generation of a biodiversity hotspot: biogeography and phylogeography of the Western Indian Ocean islands. In: Current Topics in Phylogenetics and Phylogeography of Terrestrial and Aquatic Systems (K. Anamthawat-Jonsson, ed.), pp. 33-82. In Tech Publishers, Rijeka.
2. Amos, W. & Harwood, J. 1998. Factors affecting levels of genetic diversity in natural populations. Philos. Trans. Roy. Soc. B 353: 177-186.
3. Anderson, D.R. & Burnham, K.R. 2002. Avoiding pitfalls when using information-theoretic methods. J. Wildl. Manage. 66: 912-918.
4. Andreone, F., Vences, M., Guarino, F.M., Glaw, F. & Randrianirina, J.E. 2002. Natural history and larval morphology of Boophis occidentalis (Anura: Mantellidae: Boophinae) provide new insights into the phylogeny and adaptive radiation of endemic Malagasy frogs. J. Zool. 257: 425-438.
5. Andreone, F., Giacoma, C., Guarino, F.M., Mercurio, V. & Tessa, G. 2011. Age profile in nine Mantella poison frogs from Madagascar, as revealed by skeletochronological analyses. Alytes 27: 73-84.
6. Avise, J.C. 1995. Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conserv. Biol. 9: 686-690.
7. Avise, J.C. 2004. Molecular Markers, Natural History, and Evolution, 2nd edn. Sinauer Associates, Sunderland, MA.
8. Barraclough, T.G., Vogler, A.P. & Harvey, P.H. 1998. Revealing the factors that promote speciation. Philos. Trans. Roy. Soc. B 353: 241-249.
9. Bazin, E., Glémin, S. & Galtier, N. 2006. Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570-572.
10. Becker, C.G., Fonseca, C.R., Haddad, C.F.B., Batista, R.F. & Prado, P.I. 2007. Habitat split and the global decline of amphibians. Science 318: 1775-1777.
11. Birky, C.W. Jr, Fuerst, P. & Maruyama, T. 1989. Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121: 613-627.
12. Blackburn, D.C. 2008. Biogeography and evolution of body size and life history of African frogs: phylogeny of squeakers (Arthroleptis) and long-fingered frogs (Cardioglossa) estimated from mitochondrial data. Mol. Phylogenet. Evol. 49: 806-826.
13. Blomberg, S.P., Garland, T. Jr & Ives, A.R. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717-745.
14. Burnham, K.P. & Anderson, D.R. 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York, NY.
15. Cardillo, M., Huxtable, J.S. & Bromham, L. 2003. Geographic range size, life history and rates of diversification in Australian mammals. J. Evol. Biol. 16: 282-288.
16. Chan, L.M. & Zamudio, K.R. 2009. Population differentiation of temperate amphibians in unpredictable environments. Mol. Ecol. 18: 3185-3200.
17. Chelgren, N.D., Rosenberg, D.K., Heppell, S.S. & Gitelman, A.I. 2006. Carryover aquatic effects on survival of metamorphic frogs during pond emigration. Ecol. Appl. 16: 250-261.
18. Claramunt, S., Derryberry, E.P., Remsen, J.V. Jr & Brumfield, R.T. 2012. High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proc. R. Soc. B, 279: 1567-1574.
19. Coyne, J.A. & Orr, H.A. 2004. Speciation. Sinauer Associates, Sunderland, MA.
20. Crottini, A., Madsen, O., Poux, C., Strauβ, A., Vieites, D.R. & Vences, M. 2012. Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K-T boundary in Madagascar. Proc. Natl Acad. Sci. USA 109: 5358-5363.
21. Dewar, R.E. & Richard, A.F. 2012. Madagascar: a history of arrivals and what happened, and what will happen next. Annu. Rev. Anthropol. 41: doi: 10.1146/annurev-anthro-092611-145758.
22. Dubois, A. 2005. Developmental pathway, speciation and supraspecific taxonomy in amphibians, 1: why are there so many frog species in Sri Lanka? Alytes 22: 19-37.
23. Duminil, J., Fineschi, S., Hampe, A., Jordano, P., Salvini, D., Vendramin, G.G. et al. 2007. Can population genetic structure be predicted from life history traits? Am. Nat. 169: 662-672.
24. Espeland, M. & Johanson, K.A. 2010. The diversity and radiation of the largest monophyletic animal group on New Caledonia (Trichoptera: Ecnomidae: Agmina). J. Evol. Biol. 23: 2112-2122.
25. Etienne, R.S. & Olff, H. 2004. How dispersal limitation shapes species-body size distributions in local communities. Am. Nat 163: 69-83.
26. Excoffier, L., Foll, M. & Petit, R.J. 2009. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40: 481-501.
27. Fitzpatrick, B.M., Fordyce, J.A. & Gavrilets, S. 2009. Pattern, process and geographic modes of speciation. J. Evol. Biol. 22: 2342-2347.
28. García-París, M., Good, D.A., Parra-Olea, G. & Wake, D.B. 2000. Biodiversity of Costa Rican salamanders: Implications of high levels of genetic differentiation and phylogeographic structure for species formation. Proc. Natl Acad. Sci. USA 97: 1640-1647.
29. Glaw, F. & Vences, M. 2007. A Field Guide to the Amphibians and Reptiles of Madagascar, 3rd edn. Vences & Glaw, Köln.
30. Gomez-Uchida, D., Knight, T.W. & Ruzzante, D.E. 2009. Interaction of landscape and life history attributes on genetic diversity, neutral divergence and gene flow in a pristine community of salmonids. Mol. Ecol. 18: 4854-4869.
31. Gonzalez-Voyer, A., Padial, J.M., Castroviejo-Fisher, S., De La Riva, I. & Vila, C. 2011. Correlates of species richness in the largest Neotropical amphibian radiation. J. Evol. Biol. 24: 931-942.
32. Guarino, F.M., Andreone, F. & Angelini, F. 1998. Growth and longevity by skeletochronological analysis in Mantidactylus microtympanum, a rain-forest anuran of southern Madagascar. Copeia 1998: 194-198.
33. Guarino, F.M., Tessa, G., Mercurio, V. & Andreone, F. 2010. Rapid sexual maturity and short life span in the blue-legged frog and the rainbow frog from the arid Isalo Massif, southern-central Madagascar. Zoology 113: 378-384.
34. Hamrick, J.L. & Godt, M.J.W. 1996. Effects of life history traits on genetic diversity in plant species. Philos. Trans. Roy. Soc. B 351: 1291-1298.
35. e/N ratio. Evolution 59: 1596-1599.
36. Hoelzer, G.A., Drewes, R., Meier, J. & Doursat, R. 2008. Isolation-by-distance and outbreeding depression are sufficient to drive parapatric speciation in the absence of environmental influences. PLoS Comput. Biol. 4: e1000126.
37. Hudson, R.R., Slatkin, M. & Maddison, W.P. 1992. Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
38. Hughes, J.M., Schmidt, D.J. & Finn, D.S. 2009. Genes in streams: using DNA to understand the movement of fresh-water fauna and their riverine habitat. Bioscience 59: 573-583.
39. Inger, R.F., Voris, H.K. & Voris, H.H. 1974. Genetic variation and population ecology of some Southeast Asian frogs of the genera Bufo and Rana. Biochem. Genet. 12: 121-145.
40. Isaac, N.J.B., Jones, K.E., Gittleman, J.L. & Purvis, A. 2005. Correlates of species richness in mammals: body size, life history, and ecology. Am. Nat. 165: 600-607.
41. Jovanovic, O. & Vences, M. 2010. Skeletochronological analysis of age structure in populations of four species of Malagasy poisonous frogs, genus Mantella. Amphib-Reptil 31: 553-557.
42. 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: 1463-1464.
43. Kisel, Y. & Barraclough, T.G. 2010. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175: 316-334.
44. Knouft, J.H. & Page, L.M. 2003. The evolution of body size in extant groups of North American freshwater fishes: speciation, size distributions, and Cope's rule. Am. Nat. 161: 413-421.
45. Knowles, L.L. & Richards, C.L. 2005. Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation. Mol. Ecol. 14: 4023-4032.
46. Kohne, D.E. 1970. Evolution of higher-organism DNA. Q. Rev. Biophys. 33: 327-375.
47. Librado, P. & Rozas, J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
48. Martin, A.P. & Palumbi, S.R. 1993. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl Acad. Sci. USA 90: 4087-4091.
49. Marzloff, J.M. & Dial, K.P. 1991. Life history correlates of taxonomic diversity. Ecology 72: 428-439.
50. Mazerolle, M.J. 2006. Improving data analysis in herpetology: using Akaike's information criterion (AIC) to assess the strength of biological hypotheses. Amphib-Reptil 27: 169-180.
51. Mazerolle, M.J. 2011. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package, version 1.15. URL http://CRAN.R-project.org/package=AICcmodavg.
52. Moen, D.S. & Wiens, J.J. 2009. Phylogenetic evidence for competitively driven divergence: body-size evolution in Caribbean treefrogs (Hylidae: Osteopilus). Evolution 63: 195-214.
53. Morjan, C.L. & Rieseberg, L.H. 2004. How species evolve collectively: implication of gene flow and selection for the spread of advantageous alleles. Mol. Ecol. 13: 1341-1356.
54. Moyle, L.C. 2006. Correlates of genetic differentiation and isolation by distance in 17 congeneric Silene species. Mol. Ecol. 15: 1067-1081.
55. Mullen, L.B., Woods, H.A., Schwartz, M.K., Sepulveda, A.J. & Lowe, W.H. 2010. Scale-dependent genetic structure of the Idaho giant salamander (Dicamptodon aterrimus) in stream networks. Mol. Ecol. 19: 898-909.
56. Nabholz, B., Glémin, S. & Galtier, N. 2008a. Strong variations of mitochondrial mutation rate across mammals - the longevity hypothesis. Mol. Biol. Evol. 25: 120-130.
57. Nabholz, B., Mauffrey, J.F., Bazin, E., Galtier, N. & Glémin, S. 2008b. Determination of mitochondrial genetic diversity in mammals. Genetics 178: 351-361.
58. Nabholz, B., Glémin, S. & Galtier, N. 2009. The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals. BMC Evol. Biol. 9: 54.
59. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, NY.
60. Orme, C.D.L., Isaac, N.J.B. & Purvis, A. 2002a. Are most species small? Not within species-level phylogenies Proc. R. Soc. B 269: 1279-1287.
61. Orme, C.D.L., Quicke, D.L.J., Cook, J.M. & Purvis, A. 2002b. Body size does not predict species richness among the metazoan phyla. J. Evol. Biol. 15: 235-247.
62. Owens, I.P.F., Bennett, P.M. & Harvey, P.H. 1999. Species richness among birds: body size, life history, sexual selection or ecology? Proc. R. Soc. B 266: 933-939.
63. Palo, J.U., Lesbarrères, D., Schmeller, D.S., Primmer, C.R. & Merilä, J. 2004. Microsatellite marker data suggest sex-biased dispersal in the common frog Rana temporaria. Mol. Ecol. 13: 2865-2869.
64. Palumbi, S.R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Annu. Rev. Ecol. Syst. 25: 547-572.
65. Papadopoulou, A., Anastasiou, I., Keskin, B. & Vogler, A.P. 2009. Comparative phylogeography of tenebrionid beetles in the Aegean archipelago: the effect of dispersal ability and habitat preference. Mol. Ecol. 18: 2503-2517.
66. Papadopoulou, A., Anastasiou, I., Spagopoulou, F., Stalimerou, M., Terzopoulou, S., Legakis, A. et al. 2011. Testing the species-genetic diversity correlation in the aegean archipelago: toward a haplotype-based macroecology? Am. Nat. 178: 241-255.
67. Phillimore, A.B., Freckleton, R.P., Orme, C.D.L. & Owens, I.P.F. 2006. Ecology predicts large-scale patterns of phylogenetic diversification in birds. Am. Nat. 168: 220-229.
68. Phillips, B.L., Brown, G.P. & Shine, R. 2010. Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. J. Evol. Biol. 23: 2595-2601.
69. Pilliod, D.S., Peterson, C.R. & Ritson, P.I. 2002. Seasonal migration of Columbia spotted frogs (Rana luteiventris) among complementary resources in a high mountain basin. Can. J. Zool. 80: 1849-1862.
70. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & the R Development Core Team. 2011. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-101.
71. R Development Core Team. 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
72. Ray, C. 1958. Vital limits and rates of desiccation in salamanders. Ecology 39: 75-83.
73. Revell, L.J. 2010. Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1: 319-329.
74. Rosenzweig, M.L. 1995. Species Diversity in Space and Time. Cambridge University Press, Cambridge, UK.
75. Samonds, K.E., Godfrey, L.R., Ali, J.R., Goodman, S.M., Vences, M., Sutherland, M.R. et al. 2012. Spatial and temporal arrival patterns of Madagascar's vertebrate fauna explained by distance, ocean currents, and ancestor type. Proc. Natl Acad. Sci. USA 109: 5352-5357.
76. Santos, J.C. 2012. Fast molecular evolution associated with high active metabolic rates in poison frogs. Mol. Biol. Evol. 29: 2001-2018.
77. Sasa, M.M., Chippindale, P.T. & Johnson, N.A. 1998. Patterns of postzygotic isolation in frogs. Evolution 52: 1811-1820.
78. Schatz, G.E. 2000. Endemism in the Malagasy tree flora. In: Diversity and Endemism in Madagascar: 1-9 (W.R. Lourenco & S.E. Goodman, ed.), pp. 1-8. Mémoires de la Société de Biogéographie, Paris.
79. Shine, R., Brown, G.P. & Phillips, B.L. 2011. An evolutionary process that assembles phenotypes through space rather than through time. Proc. Natl Acad. Sci. USA 108: 5708-5711.
80. Stephens, P.A., Buskirk, S.W., Hayward, G.D. & Del Rio, C.M. 2005. Information theory and hypothesis testing: a call for pluralism. J. Appl. Ecol. 42: 4-12.
81. Strauß, A., Reeve, E., Randrianiaina, R.D., Vences, M. & Glos, J. 2010. The world's richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar's stream-dwelling amphibian larvae. BMC Ecol. 10: 12.
82. Tolley, K.A., De Villiers, A.L., Cherry, M.I. & Measey, G.J. 2010. Isolation and high genetic diversity in dwarf mountain toads (Capensibufo) from South Africa. Biol. J. Linn. Soc. 100: 822-834.
83. Tracy, C.R., Christian, K.A. & Tracy, C.R. 2010. Not just small, wet, and cold: effects of body size and skin resistance on thermoregulation and arboreality of frogs. Ecology 91: 1477-1484.
84. 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.
85. Vellend, M. 2005. Species diversity and genetic diversity: parallel processes and correlated patterns. Am. Nat. 166: 199-215.
86. Vellend, M. & Geber, M.A. 2005. Connections between species diversity and genetic diversity. Ecol. Lett. 8: 767-781.
87. Vences, M. & Wake, D.B. 2007. Speciation, species boundaries and phylogeography of amphibians. In: Amphibian Biology, Vol. 6, Systematics (H.H. Heatwole & M. Tyler, eds), pp. 2613-2669. Surrey Beatty & Sons, Chipping Norton, Australia.
88. Vences, M., Andreone, F., Glaw, F., Kosuch, J., Meyer, A., Schaefer, C. et al. 2002. Exploring the potential of life-history key innovation: brook breeding in the radiation of the Malagasy treefrog genus Boophis. Mol. Ecol. 11: 1453-1463.
89. Vences, M., Thomas, M., Van der Meijden, A., Chiari, Y. & Vieites, D.R. 2005. Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Front. Zool. 2: 5.
90. Vences, M., Köhler, J., Crottini, A. & Glaw, F. 2010. High mitochondrial sequence divergence meets morphological and bioacoustic conservatism: Boophis quasiboehmei sp. n., a new cryptic treefrog species from south-eastern Madagascar. Bonn Zool. Bull. 57: 241-255.
91. Vieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. 2009. Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proc. Natl Acad. Sci. USA 106: 8267-8272.
92. Ward, R.D., Skibinski, D.O. & Woodwark, M. 1992. Protein heterozygosity, protein structure, and taxonomic differentiation. Evol. Biol. 26: 73-159.
93. Weathers, W.W. & Snyder, G.K. 1977. Relation of oxygen consumption to temperature and time of day in tropical anuran amphibians. Aust. J. Zool. 25: 19-24.
94. Wells, K.D. 2007. The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago, IL.
95. Whiteley, A.R., Spruell, P. & Allendorf, F.W. 2004. Ecological and life history characteristics predict population genetic divergence of two salmonids in the same landscape. Mol. Ecol. 13: 3675-3688.
96. Whitlock, M.C. & McCauley, D.E. 1999. Indirect measures of gene flow and migration: FST ≠1/(4Nm +1). Heredity 82: 117-125.
97. Wiens, J.J., Pyron, R.A. & Moen, D.S. 2011. Phylogenetic origins of local-scale diversity patterns and the causes of Amazonian megadiversity. Ecol. Lett. 14: 643-652.
98. Wilmé, L., Goodman, S.M. & Ganzhorn, J.U. 2006. Biogeographic evolution of Madagascar's microendemic biota. Science 312: 1063-1065.
99. 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 Evol. Biol. 11: 217.
100. Xiang, Q.-Y., Soltis, D.E., Soltis, P.S., Manchester, S.R. & Crawford, D.J. 2000. Timing the eastern Asian and eastern North American floristic disjunction: molecular clocks confirm paleontological estimates. Mol. Phylogenet. Evol. 17: 1446-1455.