BMC Evolutionary Biology | |
Biogeographic and diversification patterns of Neotropical Troidini butterflies (Papilionidae) support a museum model of diversity dynamics for Amazonia | |
Felix AH Sperling2  Gael J Kergoat3  Karina L Silva-Brandão4  Fabien L Condamine1  | |
[1] CNRS, UMR 7641 Centre de Mathématiques Appliquées (École Polytechnique), Route de Saclay, 91128, Palaiseau, France;Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada, T6G 2E9;INRA, UMR Centre de Biologie pour la Gestion des Populations, CBGP, (INRA/IRD/CIRAD/Montpellier SupAgro), Campus International de Baillarguet, CS30016, 34988, Montferrier-sur-Lez, France;Departamento de Entomologia e Acarologia, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Av. Padua Dias 11, Piracicaba, SP, Brazil, 13418-900 | |
关键词: Swallowtail butterflies; GAARlandia connection; Diversification; Biogeography; Andean uplift; Amazon rainforest; | |
Others : 1141100 DOI : 10.1186/1471-2148-12-82 |
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received in 2012-02-29, accepted in 2012-06-04, 发布年份 2012 | |
【 摘 要 】
Background
The temporal and geographical diversification of Neotropical insects remains poorly understood because of the complex changes in geological and climatic conditions that occurred during the Cenozoic. To better understand extant patterns in Neotropical biodiversity, we investigated the evolutionary history of three Neotropical swallowtail Troidini genera (Papilionidae). First, DNA-based species delimitation analyses were conducted to assess species boundaries within Neotropical Troidini using an enlarged fragment of the standard barcode gene. Molecularly delineated species were then used to infer a time-calibrated species-level phylogeny based on a three-gene dataset and Bayesian dating analyses. The corresponding chronogram was used to explore their temporal and geographical diversification through distinct likelihood-based methods.
Results
The phylogeny for Neotropical Troidini was well resolved and strongly supported. Molecular dating and biogeographic analyses indicate that the extant lineages of Neotropical Troidini have a late Eocene (33–42 Ma) origin in North America. Two independent lineages (Battus and Euryades + Parides) reached South America via the GAARlandia temporary connection, and later became extinct in North America. They only began substantive diversification during the early Miocene in Amazonia. Macroevolutionary analysis supports the “museum model” of diversification, rather than Pleistocene refugia, as the best explanation for the diversification of these lineages.
Conclusions
This study demonstrates that: (i) current Neotropical biodiversity may have originated ex situ; (ii) the GAARlandia bridge was important in facilitating invasions of South America; (iii) colonization of Amazonia initiated the crown diversification of these swallowtails; and (iv) Amazonia is not only a species-rich region but also acted as a sanctuary for the dynamics of this diversity. In particular, Amazonia probably allowed the persistence of old lineages and contributed to the steady accumulation of diversity over time with constant net diversification rates, a result that contrasts with previous studies on other South American butterflies.
【 授权许可】
2012 Condamine et al.; licensee BioMed Central Ltd.
【 预 览 】
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20150325221507586.pdf | 3160KB | download | |
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Figure 1. | 107KB | Image | download |
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【 参考文献 】
- [1]Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J: Biodiversity hotspots for conservation priorities. Nature 2000, 403:853-858.
- [2]Raven PH, Axelrod DI: Angiosperm biogeography and past continental movements. Ann Missouri Bot Gard 1974, 61:539-673.
- [3]Simpson G, Haffer J: Speciation patterns in the Amazonian forest biota. Annu Rev Ecol Evol Syst 1978, 9:497-518.
- [4]Gentry AH: Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Ann Mo Bot Gard 1982, 69:557-593.
- [5]Hughes C, Eastwood SV: Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 2006, 103:10334-10339.
- [6]Antonelli A, Nylander JAA, Persson C, Sanmartín I: Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc Natl Acad Sci USA 2009, 106:9749-9754.
- [7]Erkens RHJ, Maas JW, Couvreur TLP: From Africa via Europe to South America: migrational route of a species-rich genus of Neotropical lowland rain forest trees (Guatteria, Annonaceae). J Biogeogr 2009, 36:2338-2352.
- [8]Couvreur TLP, Forest F, Baker W: Origin and global diversification patterns of tropical rain forests: inferences from a complete genus-level phylogeny of palms. BMC Biol 2011, 9:44. BioMed Central Full Text
- [9]Pennington RT, Dick CW: The role of immigrants in the assemblage of the South American rainforest tree flora. Philos Trans R Soc B 2004, 359:1611-1622.
- [10]Wallace AR: Tropical Nature, and Other Essays. Macmillan: London; 1978.
- [11]Fischer AG: Latitudinal variation in organic diversity. Evolution 1960, 14:64-81.
- [12]Haffer J: Speciation in Amazonian forest birds. Science 1969, 165:131-137.
- [13]McKenna DD, Farrell BD: Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proc Natl Acad Sci USA 2006, 103:10947-10951.
- [14]Antonelli A, Sanmartín I: Why are there so many plant species in the Neotropics? Taxon 2011, 60:403-414.
- [15]Hoorn CM, Wesselingh FP: Amazonia, Landscape and Species Evolution: A Look into the Past. 1st edition. Wiley-Blackwell: London; 2010.
- [16]Antonelli A, Sanmartín I: Mass Extinction, gradual cooling, or rapid radiation? Reconstructing the spatiotemporal evolution of the ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empirical and simulated approaches. Syst Biol 2011, 60:596-615.
- [17]Wiens JJ, Pyron RA, Moen DC: Phylogenetic origins of local-scale diversity patterns and causes of Amazonian megadiversity. Ecol Lett 2011, 14:643-652.
- [18]Moritz C, Patton JL, Schneider CJ, Smith TB: Diversification of rainforest faunas: An integrated molecular approach. Annu Rev Ecol Evol Syst 2000, 31:533-563.
- [19]Currie DJ, Mittelbach GG, Cornell HV, Field R, Guégan J-F, Hawkins BA, Kaufman DM, Kerr JT, Oberdorff T, O’Brien E, Turner JRG: Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecol Lett 2004, 7:1121-1134.
- [20]Erwin DH: Climate as a driver of evolutionary change. Curr Biol 2009, 19:575-583.
- [21]Kozak KH, Wiens JJ: Accelerated rates of climatic-niche evolution underlie rapid species diversification. Ecol Lett 2010, 13:1378-1389.
- [22]Wiens JJ, Donoghue MJ: Historical biogeography, ecology and species richness. Trends Ecol Evol 2004, 19:639-644.
- [23]Wiens JJ, Sukumaran J, Pyron RA, Brown RM: Evolutionary and biogeographic origins of high tropical diversity in old world frogs (Ranidae). Evolution 2009, 63:1217-1231.
- [24]Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA, McCain CM, McCune AR, McDade LA, McPeek MA, Near TJ, Price TD, Ricklefs RE, Roy K, Sax DF, Schluter D, Sobel JM, Turelli M: Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 2007, 10:315-331.
- [25]Becerra JX, Venable DL: Macroevolution of insect-plant associations: the relevance of host biogeography to host affiliation. Proc Natl Acad Sci USA 1999, 96:12625-12631.
- [26]Winkler IS, Mitter C, Scheffer SJ: Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies. Proc Natl Acad Sci USA 2009, 106:18103-18108.
- [27]Tyler HA, Brown KS, Wilson K: Swallowtail Butterflies of the Americas: a Study in Biological Dynamics, Ecological Diversity, Biosystematics, and Conservation. Scientific Publishers: Gainesville; 1994.
- [28]Silva-Brandão KL, Freitas AVL, Brower AVZ, Solferini VN: Phylogenetic relationships of the New World Troidini swallowtails (Lepidoptera: Papilionidae) based on COI, COII, and EF-1α genes. Mol Phylogenet Evol 2005, 36:468-483.
- [29]Racheli T: The Genus Parides: An Unended Quest. In Butterflies of the World. Edited by Bauer F, Frankenbach T. Keltern, Deutschland: Goecke and Evers; 2006:116.
- [30]Braby MF, Trueman JWH, Eastwood R: When and where did troidine butterflies (Lepidoptera: Papilionidae) evolve? Phylogenetic and biogeographic evidence suggests an origin in remnant Gondwana in the Late Cretaceous. Invert Syst 2005, 19:113-143.
- [31]Simonsen TJ, Zakharov EV, Djernaes M, Cotton AM, Vane-Wright RI, Sperling FAH: Phylogeny, host plant associations and divergence time of Papilioninae (Lepidoptera: Papilionidae) inferred from morphology and seven genes with special focus on the enigmatic genera Teinopalpus and Meandrusa. Cladistics 2011, 27:113-137.
- [32]Ehrlich PR, Raven PH: Butterflies and plants: a study in coevolution. Evolution 1964, 18:586-608.
- [33]Weintraub JD: Host plant association patterns and phylogeny in the tribe Troidini (Lepidoptera: Papilionidae). In Swallowtail Butterflies: their Ecology and Evolutionary Biology. Edited by Scriber JM, Tsubaki Y, Lederhouse RC. Gainesville: Scientific Publishers; 1995:307-316.
- [34]Silva-Brandão KL, Solferini VN: Use of host plants by Troidini butterflies (Papilionidae, Papilioninae): constraints on host shift. Biol J Linn Soc 2007, 90:247-261.
- [35]Fordyce JA: Host shifts and evolutionary radiations of butterflies. Proc R Soc B 2010, 277:3735-3743.
- [36]Condamine FL, Sperling FAH, Wahlberg N, Rasplus J-Y, Kergoat GJ: What causes latitudinal gradients in species diversity? Evolutionary processes and ecological constraints on swallowtail biodiversity. Ecol Lett 2012, 15:264-277.
- [37]Ho SYW, Phillips MJ: Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 2009, 58:367-380.
- [38]Caterino MS, Reed RD, Kuo MM, Sperling FAH: A partitioned likelihood analysis of swallowtail butterfly Phylogeny (Lepidoptera: Papilionidae). Syst Biol 2001, 50:106-127.
- [39]Silva-Brandão KL, Azeredo AML, Freitas AVL: New evidence on the systematic and phylogenetic position of Parides burchellanus (Lepidoptera: Papilionidae). Mol Ecol Resources 2008, 8:502-511.
- [40]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinfo 2007, 23:2947-2948.
- [41]Pons J, Barraclough TG, Gómez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP: Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 2006, 55:595-609.
- [42]Rabosky DL: Likelihood methods for detecting temporal shifts in diversification rates. Evolution 2006, 60:1152-1164.
- [43]Paradis E, Claude J, Strimmer K: APE: analyses of phylogenetics and evolution in R language. Bioinfo 2004, 20:289-290.
- [44]Hebert PDN, Cywinska A, Ball SL, DeWaard JR: Biological identifications through DNA barcodes. Proc R Soc B 2003, 270:313-321.
- [45]Britton T, Anderson CL, Jacquet D, Lundqvist S, Bremer K: Estimating divergence times in large phylogenetic trees. Syst Biol 2007, 56:541-752.
- [46]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
- [47]Brown JM, Lemmon AR: The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics. Syst Biol 2007, 56:643-655.
- [48]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
- [49]Felsenstein J: Inferring Phylogenies. Massachusetts, Sinauer: Sunderland; 2004.
- [50]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinfo 2003, 19:1572-1574.
- [51]Kass RE, Raftery AE: Bayes factors. J Am Stat Assoc 1995, 90:773-795.
- [52]Shimodaira H, Hasegawa M: Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 1999, 16:1114-1116.
- [53]Drummond AJ, Ho SYW, Phillips MJ, Rambaut A: Relaxed phylogenetics and dating with confidence. PLoS Biol 2006, 4:e88.
- [54]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
- [55]Ree RH, Smith SA: Maximum-likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 2008, 57:4-14.
- [56]Scotese CR: Atlas of Earth History. Volume 1. Paleogeography. Arlington, Texas: PALEOMAP Project; 2001.
- [57]Hines HM: Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Syst Biol 2008, 57:58-75.
- [58]Iturralde-Vinent MA: Meso-Cenozoic Caribbean paleogeography: Implications for the historical biogeography of the region. Int Geol Rev 2006, 48:791-827.
- [59]Elias M, Joron M, Willmott K, Silva-Brandão KL, Kaiser V, Arias CF, Pinerez GLM, Uribe S, Brower AVZ, Freitas AVL, Jiggins CD: Out of the Andes: patterns of diversification in clearwing butterflies. Mol Ecol 2009, 18:1716-1729.
- [60]Johnson KP, Weckstein JD: The Central American land bridge as an engine of diversification in New World doves. J Biogeogr 2011, 38:1069-1076.
- [61]Harmon LJ, Weir J, Brock C, Glor RE, Challenger W: GEIGER: Investigating evolutionary radiations. Bioinfo 2008, 24:129-131.
- [62]Rabosky DL: LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol Bioinfo Online 2006, 2:257-260.
- [63]Magallón S, Sanderson MJ: Absolute diversification rates in angiosperm clades. Evolution 2001, 55:1762-1780.
- [64]Pybus OG, Harvey PH: Testing macro-evolutionary models using incomplete molecular phylogenies. Proc R Soc B 2000, 267:2267-2272.
- [65]Rabosky DL, Lovette IJ: Density-dependent diversification in North American wood warblers. Proc R Soc B 2008, 275:2363-2371.
- [66]Ali JR: Colonizing the Caribbean: is the GAARlandia land-bridge hypothesis gaining a foothold? J Biogeogr 2012, 39:431-433.
- [67]Wahlberg N, Freitas AVL: Colonization of and radiation in South America by butterflies in the subtribe Phyciodina (Lepidoptera: Nymphalidae). Mol Phylogenet Evol 2007, 44:1257-1272.
- [68]Peña C, Nylin S, Freitas AVL, Wahlberg N: Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae). Zoolog Scripta 2010, 39:243-258.
- [69]Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sánchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A: Amazonia through time: Andean uplift, climate change, landscape evolution and biodiversity. Science 2010, 330:927-931.
- [70]Mullen SP, Savage WK, Wahlberg N, Willmot KR: Rapid diversification and not clade age explains high diversity in Neotropical Adelpha butterflies. Proc R Soc B 2011, 278:1777-1785.
- [71]Strutzenberger P, Fielder K: Temporal patterns of diversification in Andean Eois, a species-rich clade of moth (Lepidoptera, Geometridae). J Evol Biol 2011, 24:919-925.
- [72]Janz N, Nylin S, Wahlberg N: Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BMC Evol Biol 2006, 6:4. BioMed Central Full Text
- [73]Dayrat B: Towards integrative taxonomy. Biol J Linn Soc 2005, 85:407-415.
- [74]Rabosky DL: Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. Ecol Lett 2009, 12:735-743.
- [75]Cusimano N, Renner SS: Slowdowns in diversification rates from real phylogenies may not be real. Syst Biol 2010, 59:458-464.