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The Evolution of Climatic Niches and its Role in Shaping Diversity Patterns in Diprotodontid Marsupials

  • Vicente García-Navas
  • Marta Rodríguez-Rey
Original Paper

Abstract

The interplay between niche conservatism and niche evolution has been suggested to play a key role in shaping the biogeographical history of a given clade. Here, we integrate climatic data associated with the distribution range of 86 diprotodontid species and their phylogenetic relationships in order to examine the evolutionary dynamics of ecological niches of Diprotodontia and explore the link between diversification, niche evolution, and trends in biodiversity over space in this iconic group. Both mean annual temperature (MAT) and annual precipitation (AP) best-fitted punctuated modes of evolution indicate that climatic niche evolution in diprotodonts is speciational. Among-clade variation in rates of climatic niche evolution was correlated with variation in rates of lineage diversification, which reinforces the view that rapid shifts in climatic niches promote speciation. We found that both climatic attributes, AP and MAT, exhibited a pattern according to which species richness progressively declined along a gradient from ancestral to derived climatic conditions and, in turn, it was negatively correlated to niche breadth. However, correlation between niche breadth and niche position was not similar for both climatic traits, as these differ with respect to the relative position of the zone colonized by the most recent common ancestor within its corresponding axis. Diprotodontia diversity decreased while phylogenetic clustering increased, suggesting that niche conservatism associated with ancestral climate probably drives most of variation in species richness in this region. Our study shows that the diversification of diprotodontid marsupials appears to have occurred against a background of moderate phylogenetic niche consevatism, which largely determines the current distribution of this group.

Keywords

Australia Diversification Evolutionary radiation Macroevolution Niche conservatism 

Notes

Acknowledgements

Dr. Kieren J. Mitchell and Prof. Alan Cooper kindly provided the phylogenetic tree. Ben Whittaker checked the English. Dr. John R. Wible, Dr. Andrés Posso-Terranova, and anonymous reviewer provided valuable comments that improved the original manuscript. VGN was supported by a “Juan de la Cierva” postdoctoral fellowship from Spanish Ministry of Economy and Competitiveness (FPDI-2013-16828). MRR was supported by a PhD fellowship funded by Aquainvad-ED, a Marie Skłodowska-Curie Innovative Training Network H2020-MSCA-ITN-2014-ETN-642197.

Supplementary material

10914_2018_9435_MOESM1_ESM.docx (29 kb)
ESM 1 (DOCX 28 kb)

References

  1. Ackerly D (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc Natl Acad Sci USA 106: 19699–19706Google Scholar
  2. Algar AC, Mahler DL (2016) Area, climate heterogeneity, and the response of climate niches to ecological opportunity in island radiations of Anolis lizards. Global Ecol Biogeogr 25: 781–791CrossRefGoogle Scholar
  3. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15: 365–377CrossRefPubMedPubMedCentralGoogle Scholar
  4. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745CrossRefPubMedGoogle Scholar
  5. Bonetti MF, Wiens JJ (2014) Evolution of climatic niche specialization: a phylogenetic analysis in amphibians. Proc R Soc B 281: 20133229CrossRefPubMedPubMedCentralGoogle Scholar
  6. Boucher FC, Thuiller W, Davies TJ, Lavergne S (2014) Neutral biogeography and the evolution of climatic niches. Am Nat 183: 573–584CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brown JH (2014) Why are there so many species in the tropics? J Biogeogr 41: 8–22CrossRefPubMedGoogle Scholar
  8. Butler MA, King AA (2004) Phylogenetic comparative analysis: a modelling approach for adaptive evolution. Am Nat 164: 683–695CrossRefPubMedGoogle Scholar
  9. Buckley LB, Davies TJ, Ackerly DD, Kraft NJB, Harrison SP, Anacker BL, Cornell HV, Damschen EI, Grytnes JA, Hawkins BA, McCain CM, Stephens PR, Wiens JJ (2010) Phylogeny, niche conservatism and the latitudinal diversity gradient in mammals. Proc R Soc B 277: 2131–2138CrossRefPubMedPubMedCentralGoogle Scholar
  10. Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll K-H (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol Ecol 17: 4398–4417Google Scholar
  11. Cardillo M (2011) Phylogenetic structure of mammal assemblages at large geographical scales: linking phylogenetic community ecology with macroecology. Phil Trans R Soc Lond B 366: 2545–2553Google Scholar
  12. Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12: 693–715CrossRefPubMedGoogle Scholar
  13. Clavel J, Escarguel G, Merceron G (2015) mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Met Ecol Evol 6: 1311–1319CrossRefGoogle Scholar
  14. Chejanovski Z, Wiens JJ (2014) Climatic niche breadth and species richness in temperate treefrogs. J Biogeogr 41: 1936–1946CrossRefGoogle Scholar
  15. Cook LG, Hardy NB, Crisp MD (2015) Three explanations for biodiversity hotspots: small range size, geographical overlap and time for species accumulation. An Australian case study. New Phytol 207: 390–400CrossRefPubMedGoogle Scholar
  16. Cooney CR, Seddon N, Tobias JA, Phillimore A (2016) Widespread correlations between climatic niche evolution and species diversification in birds. J Anim Ecol 85: 869–878Google Scholar
  17. Cooper N, Jetz W, Freckleton RP (2010) Phylogenetic comparative approaches for studying niche conservatism. J Evol Biol 23: 2529–2539CrossRefPubMedGoogle Scholar
  18. Crisp MD, Cook LG (2012) Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes? New Phytol 196: 681–694CrossRefPubMedGoogle Scholar
  19. Dawson TJ (1995) Kangaroos: Biology of the Largest Marsupials. UNSW Press, Sydney.Google Scholar
  20. Dormann CF, Gruber B, Winter M, Herrmann D (2010) Evolution of climate niches in European mammals? Biol Lett 6: 229–232CrossRefPubMedGoogle Scholar
  21. Duran A, Meyer AL, Pie MR (2013) Climatic niche evolution in New World monkeys (Platyrrhini). PLoS One 8: e83684CrossRefPubMedPubMedCentralGoogle Scholar
  22. Duran A, Pie MR (2015) Tempo and mode of climatic niche evolution in primates. Evolution 69: 2496–2506CrossRefPubMedGoogle Scholar
  23. Eldredge N, Gould SJ (1972) Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf TJM (ed) Models in Paleobiology. Freeman, San Francisco, pp 82–115Google Scholar
  24. Evans ME, Smith SA, Flynn RS, Donoghue MJ (2009) Climate, niche evolution, and diversification of the “bird-cage” evening primroses (Oenothera, sections Anogra and Kleinia). Am Nat 173: 225–240CrossRefPubMedGoogle Scholar
  25. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125: 1–15Google Scholar
  26. Flannery T (1995) Mammals of New Guinea. Revised and updated edition. Reed Books, Chatswood, New South WalesGoogle Scholar
  27. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19: 207–233CrossRefGoogle Scholar
  28. García-Navas V, Rodríguez-Rey M, Westerman M (2018) Bursts of morphological and lineage diversification in modern dasyurids, a “classic” adaptive radiation. Biol J Linn SocGoogle Scholar
  29. Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42: 1–16Google Scholar
  30. Gillman LN, Wright SD (2014) Species richness and evolutionary speed: the influence of temperature, water and area. J Biogeogr 41: 39–51CrossRefGoogle Scholar
  31. Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evolution 51: 1341–1351CrossRefPubMedGoogle Scholar
  32. Harmon LJ, Schulte JA, Larson A, Losos JB (2003) Tempo and mode of evolutionary radiation in iguanian lizards. Science 301: 961–964CrossRefPubMedGoogle Scholar
  33. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24: 129–131CrossRefPubMedGoogle Scholar
  34. Hawkins BA, Diniz-Filho JAF, Soeller SA (2005) Water links the historical and contemporary components of the Australian bird diversity gradient. J Biogeogr 32: 1035–1042CrossRefGoogle Scholar
  35. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) The WorldClim interpolated global terrestrial climate surfaces. Version 1.3. Available at: http://biogeo.berkeley.edu/. Last accessed 1 May 2017
  36. Hutter CR, Guayasamin JM, Wiens JJ (2013) Explaining Andean megadiversity: the evolutionary and ecological causes of glassfrog elevational richness patterns. Ecol Lett 16: 1135–1144CrossRefPubMedGoogle Scholar
  37. IUCN (2017) The IUCN Red List of Threatened Species 2016. http://www.iucnredlist.org. Retrieved on 20th July 2017
  38. Jara-Arancio P, Arroyo MT, Guerrero PC, Hinojosa LF, Arancio G, Méndez MA (2013) Phylogenetic perspectives on biome shifts in Leucocoryne (Alliaceae) in relation to climatic niche evolution in western South America. J Biogeogr 41: 328–338CrossRefGoogle Scholar
  39. Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12: 949–960CrossRefPubMedGoogle Scholar
  40. Kembel S, Cowan P, Helmus M, Cornwell W, Morlon H, Ackerly D, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinform 26:1463–1464Google Scholar
  41. Kozak KH, Wiens JJ (2006) Does niche conservatism drive speciation? A case study in North American salamanders. Evolution 60: 2604–2621CrossRefPubMedGoogle Scholar
  42. Kozak KH, Wiens JJ (2010a) Accelerated rates of climatic-niche evolution underlie rapid species diversification. Ecol Lett 13: 1378–1389CrossRefPubMedGoogle Scholar
  43. Kozak KH, Wiens JJ (2010b) Niche conservatism drives elevational diversity patterns in Appalachian salamanders. Am Nat 176: 40–54CrossRefPubMedGoogle Scholar
  44. Labra A, Pienaar J, Hansen TF (2009) Evolution of thermal physiology in Liolaemus lizards: adaptation, phylogenetic inertia, and niche tracking. Am Nat 174: 204–220CrossRefPubMedGoogle Scholar
  45. Lanier HC, Edwards DL, Knowles LL (2013) Phylogenetic structure of vertebrate communities across the Australian arid zone. J Biogeogr 40: 1059–1070CrossRefGoogle Scholar
  46. Lin L, Wiens JJ (2017) Comparing macroecological patterns across continents: evolution of climatic niche breadth in varanid lizards. Ecography 40: 960–970CrossRefGoogle Scholar
  47. Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11: 995–1003.CrossRefPubMedGoogle Scholar
  48. Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457: 830–836CrossRefPubMedGoogle Scholar
  49. Lv X, Xia L, Ge D, Wu Y, Yang Q (2016) Climatic niche conservatism and ecological opportunity in the explosive radiation of arvicoline rodents (Arvicolinae, Cricetidae). Evolution 47: 1094–1104CrossRefGoogle Scholar
  50. Meredith RW, Westerman M, Springer MS (2008) A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: Marsupialia) based on nuclear DNA sequences. Aust J Zool 56: 395–410CrossRefGoogle Scholar
  51. Miller ET, Zanne AE, Ricklefs RE (2013) Niche conservatism constrains Australian honeyeater assemblages in stressful environments. Ecol Lett 16: 1186–1194CrossRefPubMedGoogle Scholar
  52. Mitchell KJ, Pratt RC, Watson LN, Gibb GC, Llamas B, Kasper M, Edson J, Hopwood B, Male D, Armstrong KN, Meyer M, Hofreiter M, Austin J, Donnellan SC, Lee MS, Phillips MJ, Cooper A (2014) Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Mol Biol Evol 31: 2322–2330CrossRefPubMedGoogle Scholar
  53. Morinière J, Van Dam MH, Hawlitschek O, Bergsten J, Michat MC, Hendrich L, Ribera I, Toussaint EFA, Balke M (2016) Phylogenetic niche conservatism explains an inverse latitudinal diversity gradient in freshwater arthropods. Sci Rep 6: 26340Google Scholar
  54. Münkemüller T, Boucher F, Thuiller W, Lavergne S (2015) Phylogenetic niche conservatism - common pitfalls and ways forward. Funct Ecol 29: 627–639Google Scholar
  55. Münkemüller T, Lavergne S, Bzeznik B, Dray S, Jombart T, Schiffers K, Thuiller W (2012) How to measure and test phylogenetic signal. Met Ecol Evol 3: 743–756CrossRefGoogle Scholar
  56. Olalla-Tárraga MÁ, González-Suárez M, Bernardo-Madrid R, Revilla E, Villalobos F (2017) Contrasting evidence of phylogenetic trophic niche conservatism in mammals worldwide. J Biogeogr 44: 99–110CrossRefGoogle Scholar
  57. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2012) caper: comparative analyses of phylogenetics and evolution in R. Version 0.5Google Scholar
  58. Peterson AT, Soberón J, Pearson RG, Anderson RP, Martínez-Meyer E, Nakamura M, Araújo, MB (2011) Ecological Niches and Geographic Distributions. Princeton University Press, PrincetonGoogle Scholar
  59. Pie MR, Campos LF, Meyer ALS, Duran A (2017) The evolution of climatic niches in squamate reptiles. Proc R Soc B 284: 20170268CrossRefPubMedGoogle Scholar
  60. Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6: 7–11Google Scholar
  61. Powney GD, Grenyer R, Orme CDL, Owens IPF, Meiri S (2010) Hot, dry and different: Australian lizard richness is unlike that of mammals, amphibians and birds. Global Ecol Biogeogr 19: 386–396CrossRefGoogle Scholar
  62. Pyron RA, Burbrink FT (2012) Trait-dependent diversification and the impact of palaeontological data on evolutionary hypothesis testing in New World ratsnakes (tribe Lampropeltini). J Evol Biol 25: 497–508CrossRefPubMedGoogle Scholar
  63. Pyron AR, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev 90: 1248–1262CrossRefPubMedGoogle Scholar
  64. Pyron RA, Wiens JJ (2013) Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proc R Soc B 280: 20131622Google Scholar
  65. Rabosky DL, Donnellan SC, Grundler M, Lovette IJ (2014) Analysis and visualization of complex macroevolutionary dynamics: an example from Australian scincid lizards. Syst Biol 63: 610–627CrossRefPubMedGoogle Scholar
  66. Rabosky DL, Donnellan SC, Talaba AL, Lovette IJ (2007) Exceptional among-lineage variation in diversification rates during the radiation of Australia’s most diverse vertebrate clade. Proc R Soc B 274: 2915–2923CrossRefPubMedPubMedCentralGoogle Scholar
  67. Rabosky DL, Grundler M, Anderson C, Title P, Shi JJ, Huang H, Brown JW, Larson J (2017) BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Meth Ecol Evol 5: 701–707CrossRefGoogle Scholar
  68. Rabosky DL, Huang H (2015) A robust semi-parameteric test for trait-dependent diversification. Syst Biol 65: 181–193CrossRefPubMedGoogle Scholar
  69. Rabosky DL, Santini F, Eastman JT, Smith SA, Sidlauskas BL, Chang J, Alfaro ME (2013) Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat Commun 4: 1958CrossRefPubMedGoogle Scholar
  70. Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Met Ecol Evol 3: 217–223CrossRefGoogle Scholar
  71. Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57: 591–601CrossRefPubMedGoogle Scholar
  72. Ritchie EG, Martin JK, Johnson CN, Fox BJ (2009) Separating the influences of environment and species interactions on patterns of distribution and abundance: competition between large herbivores. J Anim Ecol 78: 724–731CrossRefPubMedGoogle Scholar
  73. Rix MG, Edwards DL, Byrne M, Harvey MS, Joseph L, Roberts JD (2015) Biogeography and speciation of terrestrial fauna in the south-western Australian biodiversity hotspot. Biol Rev 90: 762–793CrossRefPubMedGoogle Scholar
  74. Rohde K (1992) Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65: 514–527CrossRefGoogle Scholar
  75. Rolland J, Condamine FL, Jiguet F, Morlon H (2014) Faster speciation and reduced extinction in the tropics contribute to the mammalian latitudinal diversity gradient. PLoS Biol 12: e1001775CrossRefPubMedPubMedCentralGoogle Scholar
  76. Salariato DL, Zuloaga FO (2016) Climatic niche evolution in the Andean genus Menonvillea (Cremolobeae: Brassicaceae). Org Div Evol 17: 11–28CrossRefGoogle Scholar
  77. Schnitzler J, Graham CH, Dormann CF, Schiffers K, Linder PH (2012) Climatic niche evolution and species diversification in the Cape flora, South Africa. J Biogeogr 39: 2201–2211CrossRefGoogle Scholar
  78. Seeholzer GF, Claramunt S, Brumfield RT (2017) Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae). Evolution 71: 702–715Google Scholar
  79. Smith BT, Bryson RW, Houston D, Klicka J (2012) An asymmetry in niche conservatism contributes to the latitudinal species diversity gradient in New World vertebrates. Ecol Lett 15: 1318–1325CrossRefPubMedGoogle Scholar
  80. Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10: 1115–1123Google Scholar
  81. Stevens RD (2011) Relative effects of time for speciation and tropical niche conservatism on the latitudinal diversity gradient of phyllostomid bats. Proc R Soc B 278: 2528–2536CrossRefPubMedPubMedCentralGoogle Scholar
  82. Stroud JT, Losos, JB (2016) Ecological opportunity and adaptive radiation. Annu Rev Ecol Evol Syst 47: 507–532CrossRefGoogle Scholar
  83. Title PO, Burns KJ (2015) Rates of climatic niche evolution are correlated with species richness in a large and ecologically diverse radiation of songbirds. Ecol Lett 18: 433–440Google Scholar
  84. Van Dyck S, Gynther I, Baker A (2013) Field Companion to the Mammals of Australia. New Holland Publishers, SydneyGoogle Scholar
  85. Velasco J, Martínez-Meyer E, Flores-Villela O, García A, Algar AC, Köhler G, Daza JM (2015) Climatic niche attributes and diversification in Anolis lizards. J Biogeogr 43: 134–144CrossRefGoogle Scholar
  86. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Evol Syst 33: 475–505Google Scholar
  87. Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58: 193–197CrossRefPubMedGoogle Scholar
  88. Wiens JJ (2011) The causes of species richness patterns across space, time, and clades and the role of “ecological limits.” Rev Biol 86: 75–96Google Scholar
  89. Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Davies TJ, Grytnes JA, Harrison SP, Hawkins BA, Holt RD, McCain CM, Stephens PR (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13: 1310–1324CrossRefPubMedGoogle Scholar
  90. Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology, and species richness. Trends Ecol Evol 19: 639–644Google Scholar
  91. Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36: 519–539CrossRefGoogle Scholar
  92. Wiens JJ, Kozak KH, Silva N (2013) Diversity and niche evolution along aridity gradients in North American lizards (Phrynosomatidae). Evolution 67: 1715–1728CrossRefPubMedGoogle Scholar
  93. Wiens JJ, Parra-Olea G, García-París M, Wake DB (2007) Phylogenetic history underlies elevational biodiversity patterns in tropical salamanders. Proc R Soc B 274: 919–928CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Integrative Ecology, Estación Biológica de Doñana (EBD-CSIC)SevilleSpain
  2. 2.Department of BiosciencesSwansea UniversitySwanseaUK

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