An evaluation of the hybrid speciation hypothesis for xiphophorus clemenciae based on whole genome sequences

Evolution

Volumn 67, Issue 4, 2013, Pages 1155-1168

  Schumer, Molly ^a   Cui, Rongfeng ^b,c   Boussau, Bastien ^d,e   Walter, Ronald ^f   Rosenthal, Gil ^b,c   Andolfatto, Peter ^a  

^a PRINCETON UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Centro de Investigaciones Cientificas de Las Huastecas Aguazarca 16 de Septiembre   (Mexico)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITÉ DE LYON   (France)

^f Texas State University   (United States)

Author keywords

Hybridization; Incomplete lineage sorting; Introgression; Next generation sequencing; Sexual selection

Indexed keywords

CYPRINID; EVOLUTIONARY BIOLOGY; GENE FLOW; GENOMICS; HYBRID; HYBRIDIZATION; INTROGRESSION; PHYLOGENETICS; SEXUAL SELECTION; SPECIATION (BIOLOGY); TAXONOMY;

ANIMAL; ARTICLE; CHIMERA; CYPRINODONTIFORMES; DNA SEQUENCE; GENE FLOW; GENETICS; GENOME; PHYLOGENY; SPECIES DIFFERENTIATION;

ANIMALS; CHIMERA; CYPRINODONTIFORMES; GENE FLOW; GENETIC SPECIATION; GENOME; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

ANIMALIA; XIPHOPHORUS; XIPHOPHORUS CLEMENCIAE;

EID: 84875803782     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12009     Document Type: Article

References (75)

1. Arnold, J. 1993. Cytonuclear disequilibria in hybrid zones. Annu. Rev. Ecol. Syst. 24:521-554.
2. Arnold, M. L. 2006. Evolution through genetic exchange. Oxford Univ. Press, Oxford, U.K.
3. Avise, J. C. 2000. Cytonuclear genetic signatures of hybridization phenomena: rationale, utility, and empirical examples from fishes and other aquatic animals. Rev. Fish Biol. Fisher. 10:253-263.
4. Ballard, J. W. O., and D. M. Rand 2005. The population biology of mitochondrial DNA and its phylogenetic implications. Annu. Rev. Ecol. Syst. 36:621-642.
5. Basolo, A. L. 1990. Female preference predates the evolution of the sword in swordtail fish. Science 250:808-810.
6. Basolo, A. L. 1995. A further examination of preexisting bias favoring a sword in the genus Xiphophorus. Anim. Behav. 50:365-375.
7. Boussau, B., L. Gueguen, and M. Gouy 2009. A mixture model and a hidden markov model to simultaneously detect recombination breakpoints and reconstruct phylogenies. Evol. Bioinform. 5:67-79.
8. Brower, A. V. Z. 2011. Hybrid speciation in Heliconius butterflies? A review and critique of the evidence. Genetica 139:589-609.
9. Castric, V., J. Bechsgaard, M. H. Schierup, and X. Vekemans 2008. Repeated adaptive introgression at a gene under multiallelic balancing selection. Plos Genetics 4:1-9.
10. Christophe, N., and C. Baudoin 1998. Olfactory preferences in two strains of wild mice, Mus musculus musculus and Mus musculus domesticus, and their hybrids. Anim. Behav. 56:365-369.
11. Clark, E., L. R. Aronson, and M. Gordon 1954. Mating behavior patterns in two sympatric species of Xiphophorin fishes; their inheritance and significance in sexual isolation. Bull. Amer. Mus. Nat. Hist. 103:135-226.
12. Culumber, Z. W., H. S. Fisher, M. Tobler, M. Mateos, P. H. Barber, M. D. Sorenson, and G. G. Rosenthal 2011. Replicated hybrid zones of Xiphophorus swordtails along an elevational gradient. Mol. Ecol. 20:342-356.
13. Degnan, J. H., and N. A. Rosenberg 2009. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24:332-340.
14. Dowling, T. E., and C. L. Secor 1997. The role of hybridization and introgression in the diversification of animals. Annu. Rev. Ecol. Syst. 28:593-619.
15. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 5:1-19.
16. Fisher, H. S., B. B. M. Wong, and G. G. Rosenthal 2006. Alteration of the chemical environment disrupts communication in a freshwater fish. P. Roy. Soc. B. 273:1187-1193.
17. Funk, D. J., and K. E. Omland 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu. Rev. Ecol. Evol. Syst. 34:397-423.
18. Ganem, G., C. Litel, and T. Lenormand 2008. Variation in mate preference across a house mouse hybrid zone. Heredity 100:594-601.
19. Gompert, Z., J. A. Fordyce, M. L. Forister, A. M. Shapiro, and C. C. Nice 2006. Homoploid hybrid speciation in an extreme habitat. Science 314:1923-1925.
20. Green, R. E., J. Krause, A. W. Briggs, T. Maricic, U. Stenzel, M. Kircher, N. Patterson, H. Li, W. Zhai, M. H.-Y. Fritz, et al 2010. A draft sequence of the neandertal genome. Science 328:710-722.
21. Hanson, W. D. 1959. The breakup of initial linkage blocks under selected mating systems. Genetics 44:857-868.
22. Heliconius Genome Consortium. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487:94-98.
23. Hellenthal, G., and M. Stephens 2007. msHOT: modifying Hudson's ms simulator to incorporate crossover and gene conversion hotspots. Bioinformatics 23:520-521.
24. Hobolth, A., J. Y. Dutheil, J. Hawks, M. H. Schierup, and T. Mailund 2011. Incomplete lineage sorting patterns among human, chimpanzee, and orangutan suggest recent orangutan speciation and widespread selection. Genome Res. 21:349-356.
25. Hovick, S. M., L. G. Campbell, A. A. Snow, and K. D. Whitney 2012. Hybridization alters early life-history traits and increases plant colonization success in a novel region. Amer. Nat. 179:192-203.
26. Hudson, R. R. 1990. Gene genealogies and the coalescent process. Oxf. Surv. Evol. Biol. 7:1-44.
27. Hudson, R. R. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338.
28. Jiggins, C. D., C. Salazar, M. Linares, and J. Mavarez 2008. Hybrid trait speciation and Heliconius butterflies. Philos. T. Roy. Soc. B. 363:3047-3054.
29. Jones, J. C., J.-A. Perez-Sato, and A. Meyer 2012. A phylogeographic investigation of the hybrid origin of a species of swordtail fish from Mexico. Mol. Ecol. 21:2692-2712.
30. Kallman, K. D., and S. Kazianis 2006. The genus xiphophorus in Mexico and Central America. Zebrafish 3:271-285.
31. Kazianis, S., D. C. Morizot, B. B. McEntire, R. S. Nairn, and R. L. Borowsky 1996. Genetic mapping in Xiphophorus hybrid fish: assignment of 43 AP-PCR/RAPD and isozyme markers to multipoint linkage groups. Genome Res. 6:280-289.
32. Keck, B. P., and T. J. Near 2010. Geographic and temoporal aspects of mitochondrial replacement in nothonotus darters (Teleostei: Percidae: Etheostomatinae). Evolution 64:1410-1428.
33. Kumar, S., M. Nei, J. Dudley, and K. Tamura 2008. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 9:299-306.
34. Kunte, K., C. Shea, M. L. Aardema, J. M. Scriber, T. E. Juenger, L. E. Gilbert, and M. R. Kronforst 2011. Sex chromosome Mosaicism and Hybrid Speciation among Tiger Swallowtail Butterflies. PLoS Genetics 7:1-14.
35. Kubatko, L. S. 2009. Hybridization events in the presence of coalescence via model selection. Syst. Biol. 58:478-488.
36. Li, H., and R. Durbin 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
37. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin, and P. Genome Project Data. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079.
38. Lunter, G., and M. Goodson 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21:1-4.
39. Lynch, M. 2010. Evolution of the mutation rate. Trends Genet. 26:345-352.
40. Mallet, J. 2005. Hybridization as an invasion of the genorne. Trends. Ecol. Evolut. 20:229-237.
41. Mallet, J. 2008. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos. T. Roy. Soc. B. 363:2971-2986.
42. Martinsen, G. D., T. G. Whitham, R. J. Turek, and P. Keim 2001. Hybrid populations selectively filter gene introgression between species. Evolution 55:1325-1335.
43. Mavarez, J., C. A. Salazar, E. Bermingham, C. Salcedo, C. D. Jiggins, and M. Linares 2006. Speciation by hybridization in Heliconius butterflies. Nature 441:868-871.
44. McLennan, D. A., and M. J. Ryan 1999. Interspecific recognition and discrimination based upon olfactory cues in northern swordtails. Evolution 53:880-888.
45. Meyer, A., J. M. Morrissey, and M. Schartl 1994. Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature 368:539-542.
46. Meyer, A., W. Salzburger, and M. Schartl 2006. Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection. Mol. Ecol. 15:721-730.
47. Mullen, S. P., E. B. Dopman, and R. G. Harrison 2008. Hybrid zone origins, species boundaries, and the evolution of wing-pattern diversity in a polytypic species complex of North American admiral butterflies (Nymphalidae: Limenitis). Evolution 62:1400-1417.
48. Nolte, A. W., J. Freyhof, K. C. Stemshorn, and D. Tautz 2005. An invasive lineage of sculpins, Cottus sp (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Philos. T. Roy. Soc. B. 272:2379-2387.
49. Nolte, A. W. and D. Tautz 2010. Understanding the onset of hybrid speciation. Trends Genet. 26:54-58.
50. Pollard, D. A., V. N. Iyer, A. M. Moses, and M. B. Eisen 2006. Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. PLoS Genet. 2:1634-1647.
51. Pruefer, K., K. Munch, I. Hellmann, K. Akagi, J. R. Miller, B. Walenz, S. Koren, G. Sutton, C. Kodira, R. Winer, et al 2012. The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527-531.
52. Quail, M. A., H. Swerdlow, and D. Turner 2009. Improved protocols for the Illumina Genome Analyzer Sequencing Systerm. Curr. Protoc. Hum. Genet. 18:18.2.1-18.2.27.
53. R Development Core Team. 2008. R: A language and environment for statistical computing. Foundation for Statistical Computing. Vienna, Austria ISBN 3-900051-07-0, http://www.R-project.org.
54. Rambaut, A., and N. C. Grassly 1997. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic frees. Comput. Appl. Biosci. 13:235-238.
55. Rieseberg, L. H., O. Raymond, D. M. Rosenthal, Z. Lai, K. Livingstone, T. Nakazato, J. L. Durphy, A. E. Schwarzbach, L. A. Donovan, and C. Lexer 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211-1216.
56. Rieseberg, L. H., C. Vanfossen, and A. M. Desrochers 1995. Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375:313-316.
57. Rosenthal, G. G., and F. J. Garcia de Leon 2011. Speciation and hybridization. Pp. 109-119 in I. Schlupp, A. Pilastro, J. Evans, eds., Ecology and evolution of poeciliid fishes. Univ. of Chicago Press, Chicago
58. Salazar, C., S. W. Baxter, C. Pardo-Diaz, G. Wu, A. Surridge, M. Linares, E. Bermingham, and C. D. Jiggins 2010. Genetic evidence for hybrid trait speciation in heliconius butterflies. PLoS Genet. 6:1-12.
59. Salzburger, W., S. Baric, and C. Sturmbauer 2002. Speciation via introgressive hybridization in East African cichlids Mol. Ecol. 11:619-625.
60. Schwarz, D., B. M. Matta, N. L. Shakir-Botteri, and B. A. McPheron 2005. Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436:546-549.
61. Scribner, K. T., and J. C. Avise 1994. Cytonuclear genetics of experimental fish hybrid zones inside Biosphere-2. Proc. Natl. Acad. Sci. U.S.A. 91:5066-5069.
62. Setiamarga, D. H. E., M. Miya, Y. Yamanoue, K. Mabuchi, T. P. Satoh, J. G. Inoue, and M. Nishida 2008. Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences. Mol. Phylogenet. Evol. 49:598-605.
63. Shen, Y., J. Catchen, T. Garcia, A. Amores, I. Beldorth, J. Wagner, Z. Zhang, J. Postlethwait, W. Warren, M. Schartl et al 2012. Identification of transcriptome SNPs between Xiphophorus lines and species for assessing allele specific gene expression within F1 interspecies hybrids. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 155:102-108.
64. Shimodaira, H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51:492-508.
65. Shimodaira, H., and M. Hasegawa 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247.
66. Slatkin, M., and J. L. Pollack 2008. Subdivision in an ancestral species creates asymmetry in gene trees. Mol. Biol. Evol. 25:2241-2246.
67. Soltis, D. E., P. S. Soltis, and J. A. Tate 2004. Advances in the study of polyploidy since Plant speciation. New Phytol. 161:173-191.
68. Song, Y., S. Endepols, N. Klemann, D. Richter, F.-R. Matuschka, C.-H. Shih, M. W. Nachman, and M. H. Kohn 2011. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between old world mice. Curr. Biol. 21:1296-1301.
69. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
70. Stukenbrock, E. H., F. B. Christiansen, T. T. Hansen, J. Y. Dutheil, and M. H. Schierup 2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc. Natl. Acad. Sci. U.S.A. 109:10954-10959.
71. Velthuis, B. J., W. C. Yang, T. van Opijnen, and J. H. Werren 2005. Genetics of female mate discrimination of heterospecific males in Nasonia (Hymenoptera, Pteromalidae). Anim. Behav. 69:1107-1120.
72. Walter, R. B., J. D. Rains, J. E. Russell, T. M. Guerra, C. Daniels, D. A. Johnston, J. Kumar, A. Wheeler, K. Kelnar, V. A. Khanolkar, et al 2004. A microsatellite genetic linkage map for xiphophorus. Genetics 168:363-372.
73. Whitney, K. D., R. A. Randell, and L. H. Rieseberg 2010. Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol. 187:230-239.
74. Willis, P. M., G. G. Rosenthal, and M. J. Ryan 2012. An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni. PloS one 7:e34802.
75. Willis, P. M., M. J. Ryan, and G. G. Rosenthal 2011. Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish. Behav. Ecol. 22:1234-1240.