The genomic trajectory of hybrid swarms: Outcomes of repeated crosses between populations of tigriopus californicus

Evolution

Volumn 67, Issue 3, 2013, Pages 774-791

  Pritchard, Victoria L ^a   Edmands, Suzanne ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Copepod; Cytonuclear coadaptation; Genomic clines; Hybrid zone; Introgression; Segregation distortion

Indexed keywords

CLINE; CRUSTACEAN; DIVERGENCE; FITNESS; GENOMICS; HYBRID; HYBRID ZONE; HYBRIDIZATION; INTROGRESSION; REPRODUCTIVE SUCCESS; SWARMING; TAXONOMY;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; COPEPOD; FEMALE; GENETICS; HYBRIDIZATION; MALE; POPULATION DENSITY;

ANIMALS; COMPUTER SIMULATION; COPEPODA; FEMALE; HYBRIDIZATION, GENETIC; MALE; MODELS, GENETIC; POPULATION DENSITY;

COPEPODA; TIGRIOPUS CALIFORNICUS;

EID: 84874750127     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01814.x     Document Type: Article

References (69)

1. Allendorf, F. W., R. F. Leary, P. Spruell, and J. K. Wenburg 2001. The problems with hybrids: setting conservation guidelines. Trends Ecol. Evol. 16:613-622.
2. Barreto, F. S., G. W. Wenburg, and R. S. Burton 2011. Interpopulation patterns of divergence and selection across the transcriptome of the copepod Tigriopus californicus. Mol. Ecol. 20:560-572.
3. Benjamini, Y., and Y. Hochberg 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57:289-300.
4. Brown, A. F. 1991. Outbreeding depression as a cost of dispersal in the harpacticoid copepod, Tigriopus californicus. Biol. Bull. 181:123-126.
5. Burton, R. S. 1985. Mating system of the intertidal copepod Tigriopus californicus. Mar. Biol. 86:247-252.
6. Burton, R. S. 1986. Evolutionary consequences of restricted gene flow among natural populations of the copepod, Tigriopus californicus. Bull. Mar. Sci. 39:526-535.
7. Burton, R. S. 1987. Differentiation and integration of the genome in populations of the marine copepod Tigriopus californicus. Evolution 41:504-513.
8. Burton, R. S. 1990. Hybrid breakdown in developmental time in the copepod Tigriopus californicus. Evolution 44:1814-1822.
9. Burton, R. S., R. J. Byrne, and P. D. Rawson 2007. Three divergent mitochondrial genomes from California populations of the copepod Tigriopus californicus. Gene 403:53-59.
10. Dybdahl, M. F. 1994. Extinction, recolonization, and the genetic structure of tidepool copepod populations. Evol. Ecol. 8:113-124.
11. Edmands, S. 1999. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53:1757-1768.
12. Edmands, S. 2001. Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Mol. Ecol. 10:1743-1750.
13. Edmands, S., and R. S. Burton 1999. Cytochrome C oxidase activity in interpopulation hybrids of a marine copepod: a test for nuclear-nuclear or nuclear-cytoplasmic coadaptation. Evolution 53:1972-1978.
14. Edmands, S., H. V. Feaman, J. S. Harrison, and C. C. Timmerman 2005. Genetic consequences of many generations of hybridization between divergent copepod populations. J. Hered. 96:114-123.
15. Edmands, S., S. L. Northrup, and A. S. Hwang 2009. Maladapted gene complexes within populations of the intertidal copepod Tigriopus californicus Evolution 63:2184-2192.
16. Ellison, C. K., and R. S. Burton 2008a. Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62:631-638.
17. Ellison, C. K., and R. S. Burton 2008b. Genotype-dependent variation of mitochondrial transcriptional profiles in interpopulation hybrids. Proc. Natl. Acad. Sci. USA 105:15831-15836.
18. Fang, S., R. Yukilevich, Y. Chen, D. A. Turissini, K. Zeng, I. A. Boussy, and C.-I. Wu 2012. Incompatibility and competitive exclusion of genomic segments between sibling Drosophila species. PLoS Genetics 8:e1002795.
19. Fitzpatrick, B. M., J. R. Johnson, D. K. Kump, H. B. Shaffer, J. J. Smith, and S. R. Voss 2009. Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders. BMC Evol. Biol. 9:176.
20. Fitzpatrick, B. M., J. R. Johnson, D. K. Kump, J. J. Smith, S. R. Voss, and H. B. Shaffer 2010. Rapid spread of invasive genes into a threatened native species. Proc. Natl. Acad. Sci. USA 107:3606-3610.
21. Foley, B., C. Rose, D. Rundle, W. Leong, G. Moy, R. Burton, and S. Edmands 2011. A gene-based SNP resource and linkage map for the copepod Tigriopus californicus. BMC Genomics 12:568.
22. Gagnaire, P.-A., Y. Minegishi, S. Zenboudji, P. Valade, J. Aoyama, and P. Berrebi 2011. Within-population structure highlighted by differential introgression across semipermeable barriers to gene flow in Anguilla marmorata. Evolution 65:3413-3427.
23. Ganz, H. H., and R. S. Burton 1995. Genetic differentiation and reproductive incompatibility among Baja California populations of the copepod Tigriopus californicus. Mar. Biol. 123:821-827.
24. Gompert, Z., and C. A. Buerkle 2010. Introgress: a software package for mapping components of isolation in hybrids. Mol. Ecol. Resour. 10:378-384.
25. Gompert, Z., L. Lucas, C. Nice, J. A. Fordyce, M. L. Forister, and C. A. Buerkle 2012a. Genomic regions with a history of divergent selection affect fitness of hybrids between two butterfly species. Evolution 66:2167-2181.
26. Gompert, Z., T. L. Parchman, and C. A. Buerkle 2012b. Genomics of isolation in hybrids. Philos. Trans. R. Soc. Lond. B 367:439-450.
27. Gusmao, L. F. M., and A. D. McKinnon 2009. Sex ratios, intersexuality and sex change in copepods. J. Plankton Res. 31:1101-1117.
28. Harrison, J. S., and S. Edmands 2006. Chromosomal basis of viability differences in Tigriopus californicus interpopulation hybrids. J. Evol. Biol. 19:2040-2051.
29. Hermansen, J. S., S. A. Saether, T. O. Elgvin, T. Borge, E. Hjelle, and G.-P. Saetre 2011. Hybrid speciation in sparrows I: phenotypic intermediacy, genetic admixture and barriers to gene flow. Mol. Ecol. 20:3812-3822.
30. Hwang, A. S., S. L. Northrup, J. K. Alexander, K. T. Vo, and S. Edmands 2011. Long-term experimental hybrid swarms between moderately incompatible Tigriopus californicus populations: hybrid inferiority in early generations yields to hybrid superiority in later generations. Conserv. Genet. 12:895-909.
31. Janoušek, V., L. Wang, K. Luzynski, P. Dufková, M. M. Vyskočilová, M. W. Nachman, P. Munclinger, M. Macholán, J. Piálek, and P. K. Tucker 2012. Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Mus musculus musculus and M. m. domesticus. Mol. Ecol. 21:3032-3047.
32. Karrenberg, S., C. Lexer, and L. H. Rieseberg 2007. Reconstructing the history of selection during homoploid hybrid speciation. Am. Nat. 169:725-737.
33. Keller, S. R., and D. R. Taylor 2010. Genomic admixture increases fitness during a biological invasion. J. Evol. Biol. 23:1720-1731.
34. Kelly, L. S. 1998. Chemical communication during mating of the harpacticoid Tigriopus japonicus. Philos. Trans. R. Soc. Lond. B 353:737-744.
35. Kelly, M. W., E. Sanford, and R. K. Grosberg 2012. Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proc. R. Soc. Lond. B 279:349-356.
36. Lamaze, F. C., C. Sauvage, A. Marie, D. Garant, and L. Bernatchez 2012. Dynamics of introgressive hybridization assessed by SNP population genomics of coding genes in stocked brook charr (Salvelinus fontinalis). Mol. Ecol. 21:2877-2895.
37. Lazzaretto, I., F. Franco, and B. Battaglia 1994. Reproductive behaviour in the harpacticoid copepod Tigriopus fulvus. Hydrobiologia 292-293:229-234.
38. Lexer, C., J. A. Joseph, M. van Loo, T. Barbará, B. Heinze, D. Bartha, S. Castiglione, M. F. Fay, and C. A. Buerkle 2010. Genomic admixture analysis in European Populus spp. reveals unexpected patterns of reproductive isolation and mating. Genetics 186:699-712.
39. Lucek, K., D. Roy, E. Bezault, A. Sivasundar, and O. Seehausen 2010. Hybridization between distant lineages increases adaptive variation during a biological invasion: stickleback in Switzerland. Mol. Ecol. 19:3995-4011.
40. Luttikhuizen, P. C., J. Drent, K. T. C. A. Peijnenburg, H. W. Van Der Veer, and K. Johannesson 2012. Genetic architecture in a marine hybrid zone: comparing outlier detection and genomic clines analysis in the bivalve Macoma balthica. Mol. Ecol. 21:3048-3061.
41. Manly, K. F., R. H. Cudmore, and J. M. Meer 2001. Map Manager QTX, cross-platform software for genetic mapping. Mamm. Genome 12:930-932.
42. Martin, N. H., and J. H. Willis 2010. Geographic variation in postzygotic isolation and its genetic basis within and between two Mimulus species. Philos. Trans. R. Soc. Lond. B 365:2469-2478.
43. Miller, J. M., J. Poissant, J. T. Hogg, and D. W. Coltman 2012. Genomic consequences of genetic rescue in an insular population of bighorn sheep (Ovis canadensis). Mol. Ecol. 21:1583-1596.
44. Nolte, A. W., Z. Gompert, and C. A. Buerkle 2009. Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Mol. Ecol. 18:2615-2627.
45. Ovenden, J. R., D. Peel, R. Street, A. J. Courtney, S. D. Hoyle, S. L. Peel, and H. Podlich 2007. The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol. Ecol. 16:127-138.
46. Palmer, C. A., and S. Edmands 2000. Mate choice in the face of both inbreeding and outbreeding depression in the intertidal copepod Tigriopus californicus. Mar. Biol. 136:693-698.
47. Payseur, B. 2010. Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol. Ecol. Resour. 10:806-820.
48. Peng, B., and M. Kimmel 2005. SimuPOP: a forward-time population genetics simulation environment. Bioinformatics 21:3686-3687.
49. Pritchard, V. L., L. Dimond, J. S. Harrison, C. C. S Velázquez, J. T. Zieba, R. S. Burton, and S. Edmands 2011. Interpopulation hybridization results in widespread viability selection across the genome in Tigriopus californicus. BMC Genet. 12:54.
50. R Development Core Team. 2009. Pp. 1-2896. R: a language and environment for statistical computing. Vol. 1. R Foundation for Statistical Computing, Vienna Austria
51. Raymond, M., and F. Rousset 1995. GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248-249.
52. Rieseberg, L. H., B. Sinervo, C. R. Linder, M. C. Ungerer, and D. M. Arias 1996. Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. Science 272:741-745.
53. Stelkens, R. B., C. Schmid, O. Selz, and O. Seehausen 2009. Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish. BMC Evol. Biol. 9:283.
54. Stemshorn, K. C., and F. A. Reed 2011. Rapid formation of distinct hybrid lineages after secondary contact of two fish species (Cottus sp.). Mol. Ecol. 20:1475-1491.
55. Tallmon, D. A., G. Luikart, and R. S. Waples 2004. The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19:489-496.
56. Teeter, K. C., L. M. Thibodeau, Z. Gompert, C. A. Buerkle, M. W. Nachman, and P. K. Tucker 2010. The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64:472-485.
57. Ting, J. H., and T. W. Snell 2003. Purification and sequencing of a mate-recognition protein from the copepod Tigriopus japonicus. Mar. Biol. 143:1-8.
58. Toews, D. P. L., and A. Brelsford 2012. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21:3907-3930.
59. Turgeon, J., A. Tayeh, B. Tayeh, E. Lombaert, P. De Clercq, N. Berkvens, J. G. Lundgren, and A. Estoup 2011. Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion. J. Evol. Biol. 24:1044-1052.
60. Verhoeven, K. J. F., M. Macel, L. M. Wolfe, and A. Biere 2011. Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc. R. Soc. Lond. B 278:2-8.
61. Vittor, B. A. 1971. Effects of the environment on fitness- related life history characters in Tigriopus californicus. Ph.D. dissertation, University of Oregon. Available at http://scholarsbank.uoregon.edu. Accessed September 1, 2012.
62. Voordouw, M. J., and B. R. Anholt 2002a. Heritability of sex tendency in a harpacticoid copepod, Tigriopus californicus. Evolution 56:1754-1763.
63. Voordouw, M. J., and B. R. Anholt 2002b. Environmental sex determination in a splash pool copepod. Biol. J. Linn. Soc. 76:511-520.
64. Voordouw, M. J., H. E. Robinson, and B. R. Anholt 2005. Paternal inheritance of the primary sex ratio in a copepod. J. Evol. Biol. 18:1304-1314.
65. Waples, R. S. 1989. A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379-391.
66. Willett, C. S. 2007. Significant variation for fitness impacts of ETS loci in hybrids between populations of Tigriopus californicus. J. Hered. 99:56-65.
67. Willett, C. S. 2010. Potential fitness trade-offs for thermal tolerance in the intertidal copepod Tigriopus californicus. Evolution 64:2521-2534.
68. Willett, C. S. 2011. Complex deleterious interactions associated with malic enzyme may contribute to reproductive isolation in the copepod Tigriopus californicus. PLoS One 6:12.
69. Willett, C. S., and J. N. Berkowitz 2007. Viability effects and not meiotic drive cause dramatic departures from Mendelian inheritance for malic enzyme in hybrids of Tigriopus californicus populations. J. Evol. Biol. 20:1196-1205.