Causes of endemic radiation in the Caribbean: evidence from the historical biogeography and diversification of the butterfly genus Calisto (Nymphalidae: Satyrinae: Satyrini)

BMC Evolutionary Biology

Niklas Wahlberg³  Andrei Sourakov¹  Jacqueline Y Miller¹  Carlos Peña³  Rayner Núñez Águila²  Pável Matos-Maraví⁴ 

[1] McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville 32611, FL, USA;División de Colecciones Zoológicas y Sistemática, Instituto de Ecología y Sistemática, Carretera de Varona km 3.5, Capdevila, Ciudad de La Habana, Boyeros, Cuba;Laboratory of Genetics, Department of Biology, University of Turku, Turku, FI-20014, Finland;School of Biological Sciences, University of South Bohemia and Institute of Entomology, Biology Centre AS CR, Ceske Budejovice, CZ-37005, Czech Republic

关键词: Molecular phylogeny;    Lepidoptera;    Island-island vicariance;    Intra-island diversification;    Historical biogeography;    Ecological limits;    Caribbean;   

Others  :  1117946
DOI  :  10.1186/s12862-014-0199-7

 received in 2014-05-08, accepted in 2014-09-02,  发布年份 2014

【 摘 要 】

Background

Calisto is the largest butterfly genus in the West Indies but its systematics, historical biogeography and the causes of its diversification have not been previously rigorously evaluated. Several studies attempting to explain the wide-ranging diversity of Calisto gave different weights to vicariance, dispersal and adaptive radiation. We utilized molecular phylogenetic approaches and secondary calibrations points to estimate lineage ages. In addition, we used the dispersal-extinction-cladogenesis model and Caribbean paleogeographical information to reconstruct ancestral geographical distributions. We also evaluated different models of diversification to estimate the dynamics of lineage radiation within Calisto. By understanding the evolution of Calisto butterflies, we attempt to identify the main processes acting on insular insect diversity and the causes of its origin and its maintenance.

Results

The crown age of Calisto was estimated to the early Oligocene (31 ± 5 Ma), and a single shift in diversification rate following a diversity-dependent speciation process was the best explanation for the present-day diversity found within the genus. A major increase in diversification rate was recovered at 14 Ma, following geological arrangements that favoured the availability of empty niches. Inferred ancestral distributional ranges suggested that the origin of extant Calisto is in agreement with a vicariant model and the origin of the Cuban lineage was likely the result of vicariance caused by the Cuba-Hispaniola split. A long-distance dispersal was the best explanation for the colonization of Jamaica and the Bahamas.

Conclusions

The ancestral geographical distribution of Calisto is in line with the paleogeographical model of Caribbean colonization, which favours island-to-island vicariance. Because the sister lineage of Calisto remains ambiguous, its arrival to the West Indies remains to be explained, although, given its age and historical biogeography, the hypothesized GAARlandia land bridge might have been a plausible introduction route from continental America. Intra-island radiation caused by ecological innovation and the abiotic creation of niche spaces was found to be the main force shaping Calisto diversity and island endemism in Hispaniola and Cuba.

【 授权许可】

   
2014 Matos-Maraví et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 2.

Figure 3.

【 参考文献 】

• [1]Darlington PJ: The origin of the fauna of the Greater Antilles, with discussion of dispersal of animals over water and through the air. Q Rev Biol 1938, 13:274-300.
• [2]Hedges SB, Hass CA, Maxson LR: Caribbean biogeography: molecular evidence for dispersal in West Indian terrestrial vertebrates. Proc Natl Acad Sci U S A 1992, 89:1909-1913.
• [3]Hedges SB: Historical biogeography of West Indian vertebrates. Annu Rev Ecol Syst 1996, 27:163-196.
• [4]Dávalos LM: Phylogeny and biogeography of Caribbean mammals. Biol J Linn Soc 2004, 81:373-394.
• [5]Rosen DE: A vicariance model of Caribbean biogeography. Syst Zool 1975, 24:431-464.
• [6]Iturralde-Vinent MA: Meso-Cenozoic Caribbean paleogeography: implications for the historical biogeography of the region. Int Geol Rev 2006, 48:791-827.
• [7]Ricklefs RE, Cox GW: Taxon cycles in the West Indian avifauna. Am Nat 1972, 106:195-219.
• [8]Losos JB, Schluter D: Analysis of an evolutionary species-area relationship. Nature 2000, 408:847-850.
• [9]Alonso R, Crawford AJ, Bermingham E: Molecular phylogeny of an endemic radiation of Cuban toads (Bufonidae: Peltophryne) based on mitochondrial and nuclear genes. J Biogeogr 2012, 39:434-451.
• [10]Ali JR: Colonizing the Caribbean: is the GAARlandia land-bridge hypothesis gaining a foothold? J Biogeogr 2012, 39:431-433.
• [11]Van Gestel J-P, Mann P, Grindlay NR, Dolan JF: Three-phase tectonic evolution of the northern margin of Puerto Rico as inferred from an integration of seismic reflection, well, and outcrop data. Mar Geol 1999, 161:257-286.
• [12]MacPhee RDE, Iturralde-Vinent MA, Gaffney ES: Domo de Zaza, an early Miocene vertebrate locality in south-central Cuba, with notes on the tectonic evolution of Puerto Rico and the Mona Passage. Am Museum Novit 2003, 3394:1-42.
• [13]Pindell JL, Barrett SF: Geological evolution of the Caribbean Region: a plate-tectonic perspective. In Geol North Am Vol H, Caribb Reg. Edited by Dengo G, Case JE. Geological Society of America, Boulder, CO; 1990:405-432.
• [14]Hedges SB: Biogeography of the West Indies: an overview. In Biogeogr West Indies Patterns Perspect. Edited by Woods CA, Sergile FE. CRC Press, Boca Raton; 2001:15-33.
• [15]Graham A: Models and Cenozoic paleoenvironments of the Caribbean region. Syst Bot 2003, 28:378-386.
• [16]Lewis JF, Draper G: Geology and tectonic evolution of the Northern Caribbean Margin. In Geol North Am Vol H, Caribb Reg. Edited by Dengo G, Case JE. Geological Society of America, Boulder, CO; 1990:77-140.
• [17]Heubeck C, Mann P: Structural geology and cenozoic tectonic history of the Southeastern termination of the Cordillera Central, Dominican Republic. In Geol Tecton Dev North Am - Caribb plate Bound Hisp. Edited by Mann P, Draper G, Lewis JF. Geological Society of America Special Paper 262; 1991:315–336.
• [18]Maurrasse FJ-MR, Pierre-Louis F, Rigaud J-G: Cenozoic facies distribution in the Southern Peninsula of Haiti and the Barahona Peninsula, Dominican Republic. Trans 9th Caribb Geol Conf 1980, 1:161-174.
• [19]Robinson E: Jamaica. In Caribb Geol An Introd. Edited by Donovan SK, Jackson TA. University of the West Indies Publishers Association, Kingston, Jamaica; 1994:111-127.
• [20]Pindell J: Evolution of the Gulf of Mexico and the Caribbean. In Caribb Geol An Introd. Edited by Donovan SK, Jackson TA. The University of West Indies Publishers Association, Kingston, Jamaica; 1994:13-40.
• [21]Hearty PJ, Neumann AC: Rapid sea level and climate change at the close of the Last Interglaciation (MIS 5e): evidence from the Bahama Islands. Quat Sci Rev 2001, 20:1881-1895.
• [22]Michener CD: A review of the genus Calisto (Lepidoptera, Satyrinae). Am Museum Novit 1943, 1236:1-6.
• [23]Lamas G: Atlas of Neotropical Lepidoptera: Checklist: Part 4A. Hesperioidea-Papilionoidea. Association for Tropical Lepidoptera, Gainesville, Florida; 2004.
• [24]Scott JA: Biogeography of Antillean butterflies. Biotropica 1972, 4:32-45.
• [25]Fontenla JL: Biogeography of Antillean butterflies (Lepidoptera: Rhopalocera): patterns of association among areas of endemism. Trans Am Entomol Soc 2003, 129:399-410.
• [26]Smith DS, Miller LD, KcKenzie F: The butterflies of Anegada, British Virgin Islands, with descriptions of a new Calisto (Satyridae) and a new Copaeodes (Hesperiidae) endemic to the island. Bull Allyn Mus 1991, 133:1-25.
• [27]Sourakov A, Zakharov EV: “Darwin’s butterflies”? DNA barcoding and the radiation of the endemic Caribbean butterfly genus Calisto (Lepidoptera, Nymphalidae, Satyrinae). Comp Cytogenet 2011, 5:191-210.
• [28]Núñez Aguila R, Oliva Plasencia E, Matos Maravi PF, Wahlberg N: Cuban Calisto (Lepidoptera, Nymphalidae, Satyrinae), a review based on morphological and DNA data. Zookeys 2012, 165:57-105.
• [29]Núñez Aguila R, Matos-Maraví PF, Wahlberg N: New Calisto species from Cuba, with insights on the relationships of Cuban and Bahamian taxa (Lepidoptera, Nymphalidae, Satyrinae). Zootaxa 2013, 3669:503-521.
• [30]Miller LD: The higher classification, phylogeny and zoogeography of the Satyridae (Lepidoptera). Mem Am Entomol Soc 1968, 24:1-174.
• [31]Viloria AL: Historical biogeography and the origins of the satyrine butterflies of the tropical andes (Lepidoptera: Rhopalocera). In Una Perspect Latinoam la Biogeogr. Edited by Morrone JJ, Llorente J. Universidad Nacional Autónoma de México, México; 2003:247-261.
• [32]Peña C, Nylin S, Wahlberg N: The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods. Zool J Linn Soc 2011, 161:64-87.
• [33]Smith DS, Miller LD, Miller JY: The Butterflies of the West Indies and South Florida. Oxford University Press, Oxford; 1994.
• [34]Riley ND: A Field Guide to the Butterflies of the West Indies. Collins, London; 1975.
• [35]Brown FM: The origins of the West Indian butterfly fauna. In Zoogeography Caribb. Edited by Gill FB. Academy of Natural Sciences of Philadelphia, Special Publication No. 13, Pennsylvania; 1978:5-30.
• [36]Miller JY, Miller LD: The biogeography of the West Indian butterflies (Lepidoptera): an application of a vicariance/dispersalist model. In Biogeogr West Indies Patterns Perspect. 2nd edition. Edited by Woods CA, Sergile FE. CRC Press LLC, Florida; 2001:127-155.
• [37]Miller LD, Miller JY: The Biogeography of the West Indian Butterflies (Lepidoptera: Papilionidea, Hesperioidea): a Vicariance model. In Biogeogr West Indies Past, Present Futur. Edited by Woods CA. Sandhill Crane Press, Gainesville, Florida; 1989:229-262.
• [38]Rabosky DL, Glor RE: Equilibrium speciation dynamics in a model adaptive radiation of island lizards. Proc Natl Acad Sci U S A 2010, 107:22178-22183.
• [39]Sly ND, Townsend AK, Rimmer CC, Townsend JM, Latta SC, Lovette IJ: Ancient islands and modern invasions: disparate phylogeographic histories among Hispaniola’s endemic birds. Mol Ecol 2011, 20:5012-5024.
• [40]Oneal E, Otte D, Knowles LL: Testing for biogeographic mechanisms promoting divergence in Caribbean crickets (genus Amphiacusta). J Biogeogr 2010, 37:530-540.
• [41]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [42]Johnson K, Quinter EL, Matusik D: A new species of Calisto from Hispaniola with a review of the female genitalia of Hispaniolan congeners (Satyridae). J Res Lepid 1987, 25:73-82.
• [43]Schwartz A: A new species of Calisto from the Cordillera Central, Republica Dominicana. Milwaukee Public Museum, Contrib to Biol Geol 1991, 81:1-3.
• [44]Schwartz A, Gonzalez FL: A new species of Calisto (Satyridae) from Hispaniola. Bull Allyn Mus 1988, 117:1-5.
• [45]Johnson K, Hedges SB: Three new species of Calisto from Southwestern Haiti (Lepidoptera: Nymphalidae: Satyrinae). Trop Lepid 1998, 9:45-53.
• [46]Schwartz A: The Butterflies of Hispaniola. University Presses of Florida, Gainesville; 1989.
• [47]Rabosky DL: Likelihood methods for detecting temporal shifts in diversification rates. Evolution (N Y) 2006, 60:1152-1164.
• [48]Peña C, Nylin S, Freitas AVL, Wahlberg N: Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae). Zool Scr 2010, 39:243-258.
• [49]Matos-Maraví PF, Peña C, Willmott KR, Freitas AVL, Wahlberg N: Systematics and evolutionary history of butterflies in the “Taygetis clade” (Nymphalidae: Satyrinae: Euptychiina): towards a better understanding of Neotropical biogeography. Mol Phylogenet Evol 2013, 66:54-68.
• [50]Elias M, Joron M, Willmott K, Silva-Brandão KL, Kaiser V, Arias CF, Gomez Piñerez LM, Uribe S, Brower AVZ, Freitas AVL, Jiggins CD: Out of the Andes: patterns of diversification in clearwing butterflies. Mol Ecol 2009, 18:1716-1729.
• [51]Kodandaramaiah U, Wahlberg N: Phylogeny and biogeography of Coenonympha butterflies (Nymphalidae: Satyrinae) - patterns of colonization in the Holarctic. Syst Entomol 2009, 34:315-323.
• [52]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.
• [53]Condamine FL, Silva-Brandão KL, Kergoat GJ, Sperling FAH: Biogeographic and diversification patterns of Neotropical Troidini butterflies (Papilionidae) support a museum model of diversity dynamics for Amazonia. BMC Evol Biol 2012, 12:82. BioMed Central Full Text
• [54]Fox RM: Affinities and distribution of Antillean Ithomiidae. J Res Lepid 1963, 2:173-184.
• [55]Hedges SB, Johnson K: Calisto tasajera in the Hispaniolan Cordillera Central (Lepidoptera: Nymphalidae: Satyrinae). Trop Lepid 1994, 5:93-94.
• [56]Sourakov A: Notes on the genus Calisto, with descriptions of the immature stages (Part II) (Lepidoptera: Nymphalidae: Satyrinae). Trop Lepid 2000, 10:73-79.
• [57]Shelly TE, Ludwig D: Thermoregulatory behavior of the butterfly Calisto nubila (Satyridae) in a Puerto Rican forest. Oikos 1985, 44:229-233.
• [58]MacArthur RH, Wilson EO: The Theory of Island Biogeography. Princeton University Press, Princeton, NJ; 1967.
• [59]Munroe EG: The Geographical Distribution of Butterflies in the West Indies. Cornell University, Ithaca, New York, USA; 1948.
• [60]Munroe EG: The systematics of Calisto (Lepidoptera, Satyrinae), with remarks on the evolutionary and zoogeographic significance of the genus. J New York Entomol Soc 1950, 58:211-240.
• [61]Etienne RS, Haegeman B: A conceptual and statistical framework for adaptive radiations with a key role for diversity dependence. Am Nat 2012, 180:E75-E89.
• [62]Brown FM, Heineman B: Jamaica and its Butterflies. E. W. Classey, London; 1972.
• [63]Wetherbee DK: Eighth Contribution on the Larvae And/or Larval Host Plants of Hispaniolan Butterflies: The Butterfly/larva Flora with a Theory of Calisto (Satyridae) Origin and Endemicity. Selfpublished, Shelburne, Massachsetts; 1992.
• [64]Hebert PDN, Cywinska A, Ball SL, DeWaard JR: Biological identifications through DNA barcodes. Proc R Soc B Biol Sci 2003, 270:313-321.
• [65]Wahlberg N, Wheat CW: Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera. Syst Biol 2008, 57:231-242.
• [66]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
• [67]Peña C, Malm T: VoSeq: a voucher and DNA sequence web application. PLoS ONE 2012, 7:e39071.
• [68]Rota J, Wahlberg N: Exploration of data partitioning in an eight-gene dataset: phylogeny of metalmark moths (Lepidoptera, Choreutidae). Zool Scr 2012, 41:536-546.
• [69]Cummins CA, McInerney JO: A method for inferring the rate of evolution of homologous characters that can potentially improve phylogenetic inference, resolve deep divergence and correct systematic biases. Syst Biol 2011, 60:833-844.
• [70]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
• [71]Kumar S, Skjæveland Å, Orr RJS, Enger P, Ruden T, Mevik B-H, Burki F, Botnen A, Shalchian-Tabrizi K: AIR: a batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics 2009, 10:357. BioMed Central Full Text
• [72]Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP: MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012, 61:539-542.
• [73]Wahlberg N, Leneveu J, Kodandaramaiah U, Peña C, Nylin S, Freitas AVL, Brower AVZ: Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc R Soc B Biol Sci 2009, 276:4295-4302.
• [74]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
• [75]Ree RH, Smith SA: Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 2008, 57:4-14.
• [76]Smith SA: Taking into account phylogenetic and divergence-time uncertainty in a parametric biogeographical analysis of the Northern Hemisphere plant clade Caprifolieae. J Biogeogr 2009, 36:2324-2337.
• [77][http://cran.r-project.org/web/packages/BioGeoBEARS/index.html] webcite Matzke NJ: BioGeoBEARS: BioGeography with Bayesian (and Likelihood) Evolutionary Analysis in R Scripts. 2013. .
• [78]Matzke NJ: Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Front Biogeogr 2013, 5:242-248.
• [79]Rabosky DL: LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Bioinformatics 2006, 2:247-250.
• [80]Paradis E, Claude J, Strimmer K: APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
• [81][http://cran.r-project.org/web/packages/DDD/index.html] webcite Etienne RS, Haegeman B: DDD: Diversity-Dependent Diversification. 2013. .
• [82][www.r-project.org] webcite R Core Team: R: A language and environment for statistical computing. 2013. .
• [83]Matos-Maraví P, Núñez Águila R, Peña C, Miller JY, Sourakov A, Wahlberg N: DNA sequence data from the butterfly genus Calisto (Nymphalidae: Satyrinae: Satyrini). TreeBASE database. 2014.