Genomic tests of the species-pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands

Evolution

Volumn 69, Issue 6, 2015, Pages 1501-1517

  Papadopoulou, Anna ^a   Knowles, L Lacey ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Biogeography; Pleistocene Aggregate Island Complex; Rad seq; Sea level change

Indexed keywords

COLONIZATION; CONNECTIVITY; GENETIC DIFFERENTIATION; GENOME; GRASSHOPPER; HABITAT FRAGMENTATION; ISLAND; PERSISTENCE; POPULATION GENETICS; SPECIATION (BIOLOGY);

LEEWARD ISLANDS [LESSER ANTILLES]; VIRGIN ISLANDS;

GRYLLIDAE; NEMOBIINAE;

ANIMAL; ANIMAL DISPERSAL; CARIBBEAN ISLANDS; CLASSIFICATION; GENETIC DRIFT; GENETIC VARIATION; GENETICS; GRYLLIDAE; INSECT GENOME; ISLAND (GEOLOGICAL); PHYLOGENY; PHYLOGEOGRAPHY; POPULATION GENETICS; SPECIES DIFFERENTIATION;

ANIMAL DISTRIBUTION; ANIMALS; GENETIC DRIFT; GENETIC SPECIATION; GENETIC VARIATION; GENETICS, POPULATION; GENOME, INSECT; GRYLLIDAE; ISLANDS; PHYLOGENY; PHYLOGEOGRAPHY; WEST INDIES;

EID: 84931570257     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12667     Document Type: Article

References (100)

1. Acevedo-Rodriguez, P. 1996. Flora of St. John, U.S. Virgin Islands. The New York Botanical Garden Press, Bronx, New York.
2. Allmon, W. D. 1992. A causal analysis of stages in allopatric speciation. Oxford Surv. Evol. Biol. 8:219-219.
3. Arnold, B., R. Corbett-Detig, D. Hartl, and K. Bomblies. 2013. RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling. Mol. Ecol. 22:3179-3190.
4. Brown, R., and A. Diesmos. 2009. Philippines, biology. Encyclopedia of Islands. California Univ. Press, Berkeley, pp. 723-732.
5. Brown, R. M., C. D. Siler, C. H. Oliveros, J. A. Esselstyn, A. C. Diesmos, P. A. Hosner, C. W. Linkem, A. J. Barley, J. R. Oaks, M. B. Sanguila et al. 2013. Evolutionary processes of diversification in a Model Island Archipelago. Annu. Rev. Ecol. Syst. 44:411-435.
6. Camoin, G., L. Montaggioni, and C. Braithwaite. 2004. Late glacial to post glacial sea levels in the Western Indian Ocean. Mar. Geol. 206:119-146.
7. Catchen, J., P. A. Hohenlohe, S. Bassham, A. Amores, and W. A. Cresko. 2013. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22:3124-3140.
8. Catchen, J. M., A. Amores, P. Hohenlohe, W. Cresko, and J. H. Postlethwait. 2011. Stacks: building and genotyping loci de novo from short-read sequences. G3 1:171-182.
9. Chifman, J., and L. Kubatko. 2014. Quartet inference from SNP data under the coalescent model. Bioinformatics 30:3317-3324.
10. Crispo, E., P. Bentzen, D. N. Reznick, M. T. Kinnison, and A. P. Hendry. 2006. The relative influence of natural selection and geography on gene flow in guppies. Mol. Ecol. 15:49-62.
11. Davalos, L. M., and A. L. Russell. 2012. Deglaciation explains bat extinction in the Caribbean. Ecol. Evol. 2:3045-3051.
12. Dynesius, M., and R. Jansson. 2014. Persistence of within-species lineages: a neglected control of speciation rates. Evolution 68:923-934.
13. Earl, D. A. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4:359-361.
14. Edelaar, P., D. Alonso, S. Lagerveld, J. Senar, and M. Björklund. 2012. Population differentiation and restricted gene flow in Spanish crossbills: not isolation-by-distance but isolation-by-ecology. J. Evol. Biol. 25:417-430.
15. Emerson, K. J., C. R. Merz, J. M. Catchen, P. A. Hohenlohe, W. A. Cresko, W. E. Bradshaw, and C. M. Holzapfel. 2010. Resolving postglacial phylogeography using high-throughput sequencing. Proc. Nat. Acad. Sci. USA 107:16196-16200.
16. Esselstyn, J. A., and R. M. Brown. 2009. The role of repeated sea-level fluctuations in the generation of shrew (Soricidae: Crocidura) diversity in the Philippine Archipelago. Mol. Phylogenet. Evol. 53:171-181.
17. Esselstyn, J. A., S. P. Maher, and R. M. Brown. 2011. Species interactions during diversification and community assembly in an island radiation of shrews. PLoS One 6:e21885.
18. Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14:2611-2620.
19. Excoffier, L., I. Dupanloup, E. Huerta-Sánchez, V. C. Sousa, and M. Foll. 2013. Robust demographic inference from genomic and SNP data. PLoS Genet. 9:e1003905.
20. Excoffier, L., and M. Foll. 2011. Fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex evolutionary scenarios. Bioinformatics 27:1332-1334.
21. Falk, B. G., and S. L. Perkins. 2013. Host specificity shapes population structure of pinworm parasites in Caribbean reptiles. Mol. Ecol. 22:4576-4590.
22. Futuyma, D. J. 1987. On the role of species in anagenesis. Am. Nat. 130:465-473.
23. Glor, R. E., M. E. Gifford, A. Larson, J. B. Losos, L. R. Schettino, A. R. Chamizo Lara, and T. R. Jackman. 2004. Partial island submergence and speciation in an adaptive radiation: a multilocus analysis of the Cuban green anoles. Proc. R. Soc. Lond. B Biol. Sci. 271:2257-2265.
24. Glor, R. E., J. B. Losos, and A. Larson. 2005. Out of Cuba: overwater dispersal and speciation among lizards in the Anolis carolinensis subgroup. Mol. Ecol. 14:2419-2432.
25. Gore, S. 2013. Anegada: an emergent Pleistocene Reef Island. Pp. 47-60 in C. R. C. Sheppard, ed. Coral reefs of the world. Springer, Netherlands.
26. Gorog, A. J., M. H. Sinaga, and M. D. Engstrom. 2004. Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biol. J. Linn. Soc. 81:91-109.
27. Grothe, P., L. Taylor, B. Eakins, K. Carignan, R. Caldwell, E. Lim, and D. Friday. 2012. Digital elevation models of the US Virgin Islands: procedures, data sources and analysis, NOAA technical memorandum NESDIS NGDC-55. U.S. Dept. of Commerce, Boulder, CO.
28. Guillot, G., F. Rousset, and L. Harmon. 2013. Dismantling the Mantel tests. Methods Ecol. Evol. 4:336-344.
29. Harter, A. V., K. A. Gardner, D. Falush, D. L. Lentz, R. A. Bye, and L. H. Rieseberg. 2004. Origin of extant domesticated sunflowers in eastern North America. Nature 430:201-205.
30. He, Q., D. L. Edwards, and L. L. Knowles. 2013. Integrative testing of how environments from the past to the present shape genetic structure across landscapes. Evolution 67:3386-3402.
31. Heaney, L. 1985. Zoogeographic evidence for middle and late Pleistocene land bridges to the Philippine Islands. Modern Quat. Res. Southeast Asia 9:127-144.
32. Heaney, L. R. 1986. Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biol. J. Linn. Soc. 28:127-165.
33. Heaney, L. R., J. S. Walsh, and A. T. Peterson. 2005. The roles of geological history and colonization abilities in genetic differentiation between mammalian populations in the Philippine archipelago. J. Biogeogr. 32:229-247.
34. Heatwole, H., R. Levins, and M. Byers. 1981. Biogeography of the Puerto Rican Bank: geography, geology, vegetation, and general ecology. Atoll Res. Bull. 251:1-62.
35. Heatwole, H., and F. MacKenzie. 1967. Herpetogeography of Puerto Rico. IV. Paleogeography, faunal similarity and endemism. Evolution 21:429-438.
36. Hedges, S. B. 1996. Historical biogeography of West Indian vertebrates. Annu. Rev. Ecol. Syst. 27:163-196.
37. Hedges S. B. 2006. Paleogeography of the Antilles and origin of West Indian terrestrial vertebrates. Annal. Missouri Bot. Garden 93:231-244.
38. Hedges, S. B., and M. P. Heinicke. 2007. Molecular phylogeny and biogeography of West Indian frogs of the genus Leptodactylus (Anura, Leptodactylidae). Mol. Phylogenet. Evol. 44:308-314.
39. Heinen, J. L., M. W. Coco, M. S. Marcuard, D. N. White, M. N. Peterson, R. A. Martin, and R. B. Langerhans. 2013. Environmental drivers of demographics, habitat use, and behavior during a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi). Evol. Ecol. 27:971-991.
40. Henderson, R. W., and R. Powell. 1999. West Indian herpetoecology. In Caribbean amphibians and reptiles. Academic Press, San Diego, California, pp. 223-268.
41. Hohenlohe, P. A., S. Bassham, P. D. Etter, N. Stiffler, E. A. Johnson, and W. A. Cresko. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6:e1000862.
42. Huang, H., and L. L. Knowles. 2014. Unforeseen consequences of excluding missing data from next-generation sequences: simulation study of RAD sequences. Syst. Biol.
43. Hubbard, D. K., R. B. Burke, I. P. Gill, W. R. Ramirez, and C. Sherman. 2008. Coral-reef geology: Puerto Rico and the US Virgin islands. Pp. 263-302 in B.M. Riegl and R.E. Dodge eds. Coral Reefs of the USA. Springer, USA.
44. Iturralde-Vinent, M., and R. D. MacPhee. 1999. Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bull. AMNH 238:1-95
45. Jakobsson, M., and N. A. Rosenberg. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-1806.
46. Jordan, S., C. Simon, D. Foote, and R. A. Englund. 2005. Phylogeographic patterns of Hawaiian Megalagrion damselflies (Odonata: Coenagrionidae) correlate with Pleistocene island boundaries. Mol. Ecol. 14:3457-3470.
47. Keightley, P. D., U. Trivedi, M. Thomson, F. Oliver, S. Kumar, and M. Blaxter. 2009. Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res. 19:1195-1201.
48. Kierepka, E. M., and E. K. Latch. 2014. Performance of partial statistics in individual-based landscape genetics. Mol. Ecol. Res. 15:512-525. doi: 10.1111/1755-0998.12332.
49. Kisel, Y., and T. G. Barraclough. 2010. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175:316-334.
50. Langerhans, R. B., M. E. Gifford, and E. O. Joseph. 2007. Ecological speciation in Gambusia fishes. Evolution 61:2056-2074.
51. Lee, C. R., and T. Mitchell-Olds. 2011. Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Mol. Ecol. 20:4631-4642.
52. Legendre, P., and M. J. Anderson. 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69:1-24.
53. Legendre, P., and M. J. Fortin. 2010. Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol. Ecol. Res. 10:831-844.
54. Losos, J. B., T. R. Jackman, A. Larson, K. D. Queiroz, and L. Rodriguez-Schettino. 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115-2118.
55. Losos, J. B., and R. E. Ricklefs. 2009. Adaptation and diversification on islands. Nature 457:830-836.
56. Losos, J. B., and D. Schluter. 2000. Analysis of an evolutionary species-area relationship. Nature 408:847-850.
57. Martin, C. H., and L. C. Feinstein. 2014. Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes. Mol. Ecol. 23:1846-1862.
58. Massatti, R., and L. L. Knowles. 2014. Microhabitat differences impact phylogeographic concordance of codistributed species: genomic evidence in montane sedges (Carex L.) from the Rocky Mountains. Evolution 68:2833-2846.
59. Meirmans, P. G., and P. H. Van Tienderen. 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4:792-794.
60. Oaks, J. R., J. Sukumaran, J. A. Esselstyn, C. W. Linkem, C. D. Siler, M. T. Holder, and R. M. Brown. 2013. Evidence for climate-driven diversification? A caution for interpreting ABC inferences of simultaneous historical events. Evolution 67:991-1010.
61. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, B. O'Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, and H. Wagner. 2013. Vegan: community ecology package. R Package Version 2.0-9.
62. Oneal, E., and L. L. Knowles. 2013. Ecological selection as the cause and sexual differentiation as the consequence of species divergence? Proc. R. Soc. Lond. B Biol. Sci. 280:20122236.
63. Oneal, E., D. Otte, and L. L. Knowles. 2010. Testing for biogeographic mechanisms promoting divergence in Caribbean crickets (genus: Amphiacusta). J. Biogeogr. 37:530-540.
64. Otte, D., and D. Perez-Gelabert 2009. Crickets of the Caribbean. Publications on orthopteran diversity, The Orthopterists Society, Ann Arbor, MI, 792 p.
65. Parchman, T. L., Z. Gompert, J. Mudge, F. D. Schilkey, C. W. Benkman, and C. Buerkle. 2012. Genome-wide association genetics of an adaptive trait in lodgepole pine. Mol. Ecol. 21:2991-3005.
66. Parent, C. E., and B. J. Crespi. 2006. Sequential colonization and diversification of Galapagos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora). Evolution 60:2311-2328.
67. Parks, D. H., M. Porter, S. Churcher, S. Wang, C. Blouin, J. Whalley, S. Brooks, and R. G. Beiko. 2009. GenGIS: a geospatial information system for genomic data. Genome Res. 19:1896-1904.
68. Peterson, B. K., J. N. Weber, E. H. Kay, H. S. Fisher, and H. E. Hoekstra. 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PloS One 7:e37135.
69. Pregill, G. K., and S. L. Olson. 1981. Zoogeography of West Indian vertebrates in relation to Pleistocene climatic cycles. Annu. Rev. Ecol. Syst.:75-98.
70. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
71. Purcell, S., B. Neale, K. Todd-Brown, L. Thomas, M. Ferreira, D. Bender, J. Maller, P. Sklar, P. de Bakker, M. Daly et al. 2007. PLINK: a toolset for whole-genome association and population-based linkage analysis. Am. J. Hum. Genet. 81:559-575.
72. Reitzel, A., S. Herrera, M. Layden, M. Martindale, and T. Shank. 2013. Going where traditional markers have not gone before: utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Mol. Ecol. 22:2953-2970.
73. Reynolds, R. G., M. L. Niemiller, S. B. Hedges, A. Dornburg, A. R. Puente-Rolon, and L. J. Revell. 2013. Molecular phylogeny and historical biogeography of West Indian boid snakes (Chilabothrus). Mol. Phylogenet. Evol. 68:461-470.
74. Rhymer, J. M., and D. Simberloff. 1996. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst.27:83-109.
75. Ricklefs, R. E., and E. Bermingham. 2004. History and the species-area relationship in Lesser Antillean birds. Am. Nat. 163:227-239.
76. Ricklefs, R. E., and E. Bermingham. 2007. The causes of evolutionary radiations in archipelagoes: passerine birds in the Lesser Antilles. Am. Nat. 169:285-297.
77. Rijsdijk, K. F., T. Hengl, S. J. Norder, R. Otto, B. C. Emerson, S. P. Ávila, H. López, E. E. van Loon, E. Tjørve, J. M. Fernández-Palacios et al. 2014. Quantifying surface-area changes of volcanic islands driven by Pleistocene sea-level cycles: biogeographical implications for the Macaronesian archipelagos. J. Biogeogr. 41:1242-1254.
78. Roberts, T. E. 2006. Multiple levels of allopatric divergence in the endemic Philippine fruit bat Haplonycteris fischeri (Pteropodidae). Biol. J. Linn. Soc. 88:329-349.
79. Rosenberg, N. A. 2004. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 4:137-138.
80. Ryan, P. G., P. Bloomer, C. L. Moloney, T. J. Grant, and W. Delport. 2007. Ecological speciation in South Atlantic island finches. Science 315:1420-1423.
81. Salvi, D., P. J. Schembri, A. Sciberras, and D. J. Harris. 2014. Evolutionary history of the Maltese wall lizard Podarcis filfolensis: insights on the 'Expansion-Contraction' model of Pleistocene biogeography. Mol. Ecol. 23:1167-1187.
82. Schluter, D., and G. L. Conte. 2009. Genetics and ecological speciation. Proc. Natl. Acad. Sci. USA 106(Suppl 1):9955-9962.
83. Seehausen, O. 2006. Conservation: losing biodiversity by reverse speciation. Curr. Biol. 16:R334-R337.
84. Siler, C. D., J. R. Oaks, J. A. Esselstyn, A. C. Diesmos, and R. M. Brown. 2010. Phylogeny and biogeography of Philippine bent-toed geckos (Gekkonidae: Cyrtodactylus) contradict a prevailing model of Pleistocene diversification. Mol. Phylogenet. Evol. 55:699-710.
85. Slatkin, M. 1977. Gene flow and genetic drift in a species subject to frequent local extinctions. Theor. Popul. Biol. 12:253-262.
86. Slatkin, M. 1985. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16:393-430.
87. Sly, N. D., A. K. Townsend, C. C. Rimmer, J. M. Townsend, S. C. Latta, and I. J. Lovette. 2011. Ancient islands and modern invasions: disparate phylogeographic histories among Hispaniola's endemic birds. Mol. Ecol. 20:5012-5024.
88. Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313.
89. Taylor, E., J. Boughman, M. Groenenboom, M. Sniatynski, D. Schluter, and J. Gow. 2006. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol. Ecol. 15:343-355.
90. Team, R. C. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
91. Thorpe, R. S., Y. Surget-Groba, and H. Johansson. 2008. The relative importance of ecology and geographic isolation for speciation in anoles. Philos. Trans. R. Soc. B-Biol. Sci. 363:3071-3081.
92. Thorpe, R. S., Y. Surget-Groba, and H. Johansson. 2010. Genetic tests for ecological and allopatric speciation in anoles on an island archipelago. PLoS Genet 6:e1000929.
93. Thorpe, R. S., Y. Surget-Groba, and H. Johansson. 2012. Quantitative traits and mode of speciation in Martinique anoles. Mol. Ecol. 21:5299-5308.
94. Wagner, C. E., I. Keller, S. Wittwer, O. M. Selz, S. Mwaiko, L. Greuter, A. Sivasundar, and O. Seehausen. 2013. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol. Ecol. 22:787-798.
95. Wang, C., Z. A. Szpiech, J. H. Degnan, M. Jakobsson, T. J. Pemberton, J. A. Hardy, A. B. Singleton, and N. A. Rosenberg. 2010. Comparing spatial maps of human population-genetic variation using Procrustes analysis. Stat. Appl. Genet. Mol. Biol. 9.
96. Wang, C., S. Zöllner, and N. A. Rosenberg. 2012. A quantitative comparison of the similarity between genes and geography in worldwide human populations. PLoS Genet. 8:e1002886.
97. Wang, I. J., R. E. Glor, and J. B. Losos. 2013. Quantifying the roles of ecology and geography in spatial genetic divergence. Ecol. Lett. 16:175-182.
98. Whetten, J. T. 1966. Geology of St. Croix, US Virgin Islands. Geol. Soc. Am. Memoirs 98:177-240.
99. Williams, E. E. 1983. Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis. Pp. 326-370 in R. B. Huey, E. R. Pianka, and T. W. Schoener, eds. Lizard ecology: studies of a model organism. Harvard Univ. Press, Cambridge, MA.
100. Zheng, X., D. Levine, J. Shen, S. M. Gogarten, C. Laurie, and B. S. Weir. 2012. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326-3328.