Speciation in ninespine stickleback: Reproductive isolation and phenotypic divergence among cryptic species of Japanese ninespine stickleback

Journal of Evolutionary Biology

Volumn 26, Issue 7, 2013, Pages 1417-1430

  Ishikawa, A ^a   Takeuchi, N ^a   Kusakabe, M ^b   Kume, M ^c   Mori, S ^c   Takahashi, H ^d   Kitano, J ^a,e  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c GIFU KEIZAI UNIVERSITY   (Japan)

^d NATIONAL FISHERIES UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Convergence; Cryptic species; Parallel evolution; Pungitius sinensis Pungitius pungitius species complex; Speciation

Indexed keywords

ADAPTATION; BRACKISH WATER; DIVERGENCE; FRESHWATER ENVIRONMENT; GENETIC ANALYSIS; PHENOTYPE; PHYLOGENETICS; POPULATION STRUCTURE; REPRODUCTIVE ISOLATION; SALINITY TOLERANCE; TELEOST;

ANIMAL; ARTICLE; BINOCULAR CONVERGENCE; CRYPTIC SPECIES; ECOSYSTEM; GENETICS; HISTOLOGY; JAPAN; PARALLEL EVOLUTION; PHENOTYPE; PHYSIOLOGY; PUNGITIUS SINENSIS-PUNGITIUS PUNGITIUS SPECIES COMPLEX; REPRODUCTIVE ISOLATION; SMEGMAMORPHA; SPECIES DIFFERENTIATION; STOMACH;

CONVERGENCE; CRYPTIC SPECIES; PARALLEL EVOLUTION; PUNGITIUS SINENSIS-PUNGITIUS PUNGITIUS SPECIES COMPLEX; SPECIATION;

ANIMALS; ECOSYSTEM; GENETIC SPECIATION; JAPAN; PHENOTYPE; REPRODUCTIVE ISOLATION; SMEGMAMORPHA; STOMACH;

HOKKAIDO; JAPAN;

GASTEROSTEUS; GASTEROSTEUS ACULEATUS; PUNGITIUS; PUNGITIUS PUNGITIUS; PUNGITIUS SINENSIS; PUNGITIUS TYMENSIS;

EID: 84880701600     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12146     Document Type: Article

References (98)

1. Abramoff, M.D., Magelhaes, P.J. & Ram, S.J. 2004. Image processing with Image. J. Biophot. Int. 11: 36-42.
2. Adachi, T., Ishikawa, A., Mori, S., Makino, W., Kume, M., Kawata, M. et al. 2012. Shifts in morphology and diet of non-native sticklebacks introduced into Japanese crater lakes. Ecol. Evol. 2: 1083-1098.
3. Aldenhoven, J.T., Miller, M.A., Corneli, P.S. & Shapiro, M.D. 2010. Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits. Mol. Ecol. 19: 4061-4076.
4. Arendt, J. & Reznick, D. 2007. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23: 26-32.
5. Ballard, L., Adams, P., Bao, Y., Bartley, D., Bintzler, D., Kasch, L. et al. 2002. Strategies for genotyping: Effectiveness of tailing primers to increase accuracy in short tandem repeat determinations. J. Biomol. Tech. 13: 20-29.
6. Barrett, R.D., Rogers, S.M. & Schluter, D. 2009. Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback. Evolution 63: 2831-2837.
7. Behm, J.E., Ives, A.R. & Boughman, J.W. 2010. Breakdown in postmating isolation and the collapse of a species pair through hybridization. Am. Nat. 175: 11-26.
8. Bell, M.A. & Foster, S.A. 1994. The Evolutionary Biology of the Threespine Stickleback. Oxford University Press, Oxford.
9. Bell, M.A., Aguirre, W. & Buck, N. 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58: 814-824.
10. Bergstrom, C. 2002. Fast-start swimming performance and lateral plate reduction in threespine stickleback. Can. J. Zool. 80: 207-213.
11. Bernatchez, L., Vuorinen, J.A., Bodaly, R.A. & Dodson, J.J. 1996. Genetic evidence for reproductive isolation and multiple origins of sympatric trophic ecotypes of whitefish (Coregonus). Evolution 50: 624-635.
12. Berner, D., Roesti, M., Hendry, A.P. & Salzburger, W. 2010. Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents. Mol. Ecol. 19: 4963-4978.
13. Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K. et al. 2007. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22: 148-155.
14. Cano, J.M., Matsuba, C., Mäkinen, H. & Merilä, J. 2006. The utility of QTL-linked markers to detect selective sweeps in natural populations - a case study of the EDA gene and a linked marker in threespine stickleback. Mol. Ecol. 15: 4613-4621.
15. Chan, Y.F., Marks, M.E., Jones, F.C., Villarreal, G., Shapiro, M.D., Brady, S.D. et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
16. Chiba, S. 2004. Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands. J. Evol. Biol. 17: 131-143.
17. Colosimo, P.F., Peichel, C.L., Nereng, K., Blackman, B.K., Shapiro, M.D., Schluter, D. et al. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2: E109.
18. Colosimo, P.F., Hosemann, K.E., Balabhadra, S., Villarreal, G. Jr, Dickson, M., Grimwood, J. et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307: 1928-1933.
19. Conte, G., Arnegard, M.A., Schluter, D. & Peichel, C.L. 2012. The probability of genetic parallelism and convergence in natural populations. Proc. Roy. Soc. B Biol. Sci. 279: 5039-5047.
20. Crawford, N.G. 2010. SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Resour. 10: 556-557.
21. Cresko, W.A., McGuigan, K.L., Phillips, P.C. & Postlethwait, J.H. 2006. Studies of threespine stickleback developmental evolution: progress and promise. Genetica 129: 105-126.
22. Evanno, G., Regnaut, S. & Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-2620.
23. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. 1: 47-50.
24. Foote, C.J., Wood, C.C., Clarke, W.C. & Blackburn, J. 1992. Circannual cycle of seawater adaptability in Oncorhynchus nerka: genetic differences between sympatric sockeye salmon and kokanee. Can. J. Fish. Aquat. Sci. 49: 99-109.
25. Foster, S.A., Baker, J.A. & Bell, M.A. 2003. The case for conserving threespine stickleback populations: Protecting an adaptive radiation. Fisheries 28: 10-18.
26. Fuller, R.C., McGhee, K.E. & Schrader, M. 2007. Speciation in killifish and the role of salt tolerance. J. Evol. Biol. 20: 1962-1975.
27. Giles, N. 1983. The possible role of environmental calcium levels during the evolution of phenotypic diversity in the outer Hebridean populations of the three-spined stickleback, Gasterosteus aculeatus. J. Zool. 199: 535-544.
28. Gompel, N. & Prud'homme, B. 2009. The causes of repeated genetic evolution. Dev. Biol. 332: 36-47.
29. Goudet, J. 1995. Fstat version 1.2: a computer program to calculate Fstatistics. J. Hered. 86: 485-486.
30. Greenwood, A.K., Jones, F.C., Chan, Y.F., Brady, S.D., Absher, D.M., Grimwood, J. et al. 2011. The genetic basis of divergent pigment patterns in juvenile threespine sticklebacks. Heredity 107: 155-166.
31. Hagen, D.W. 1967. Isolating mechanisms in threespine sticklebacks (Gasterosteus). J. Fish. Res. Bd. Canada 24: 1637-1692.
32. Hagen, D.W. & Gilbertson, L.G. 1972. Geographic variation and environmental selection in Gasterosteus aculeatus L. in the Pacific Northwest. America. Evol. 26: 32-51.
33. Hoekstra, H.E. & Coyne, J.A. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
34. Hohenlohe, P.A., Bassham, S., Etter, P.D., Stiffler, N., Johnson, E.A. & Cresko, W.A. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6: e1000862.
35. Huntingford, F.A., Wright, P.J. & Tierney, J.F. 1994. Adaptive variation in antipredator behaviour in threespine stickleback. In: The Evolutionary Biology of the Threespine Stickleback, (M.A. Bell & S.A. Foster, eds), pp. 277-296. Oxford University Press, Oxford.
36. Jin, L. & Chakraborty, R. 1993. Estimation of genetic distance and coefficient of gene diversity from single-probe multilocus DNA fingerprinting data. Mol. Biol. Evol. 11: 120-127.
37. Jones, F.C., Chan, Y.F., Schmutz, J., Grimwood, J., Brady, S.D., Southwick, A.M. et al. 2012a. A Genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr. Biol. 22: 83-90.
38. Jones, F.C., Grabherr, M.G., Chan, Y.F., Russell, P., Mauceli, E., Johnson, J. et al. 2012b. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55-61.
39. ST and its relatives do not measure differentiation. Mol. Ecol. 18: 2088-2091.
40. Kaeuffer, R., Peichel, C.L., Bolnick, D.I. & Hendry, A.P. 2012. Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66: 402-418.
41. Kingsley, D.M. & Peichel, C.L. 2007 The molecular genetics of evolutionary changes in sticklebacks. In: Biology of Three-Spined Stickleback (S. Östlund-Nilsson, I. Mayer, F.A. Huntingford, eds), pp. 41-81. CRC Press, Boca Raton.
42. Kitano, J., Mori, S. & Peichel, C.L. 2007. Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks. Biol. J. Linn. Soc. 91: 671-685.
43. Kitano, J., Bolnick, D.I., Beauchamp, D.A., Mazur, M.M., Mori, S., Nakano, T. et al. 2008. Reverse evolution of armor plates in the threespine stickleback. Curr. Biol. 18: 769-774.
44. Kitano, J., Ross, J.A., Mori, S., Kume, M., Jones, F.C., Chan, Y.F. et al. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature 461: 1079-1083.
45. Kitano, J., Lema, S.C., Luckenbach, J.A., Mori, S., Kawagishi, Y., Kusakabe, M. et al. 2010. Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation. Curr. Biol. 20: 2124-2130.
46. Kitano, J., Kawagishi, Y., Mori, S., Peichel, C.L., Makino, T., Kawata, M. et al. 2011. Divergence in sex steroid hormone signaling between sympatric species of Japanese threespine stickleback. PLoS ONE 6: e29253.
47. Kume, M., & Mori, S. 2009. Sea-run migratory behaviour in the Japan Sea form of three-spined stickleback Gasterosteus aculeatus in the tidal pool of eastern Hokkaido Island, Japan. J. Fish. Biol. 75: 2845-2850.
48. Kume, M., Kitano, J., Mori, S. & Shibuya, T. 2010. Ecological divergence and habitat isolation between two migratory forms of Japanese threespine stickleback (Gasterosteus aculeatus). J. Evol. Biol. 23: 1436-1446.
49. Landry, L. & Bernatchez, L. 2010. Role of epibenthic resource opportunities in the parallel evolution of lake whitefish species pairs (Coregonus sp.). J. Evol. Biol. 23: 2602-2613.
50. Le Rouzic, A., Østbye, A.K., Klepaker, T.O., Hansen, T.F., Bernatchez, L., Schluter, D. et al. 2011. Strong and consistent natural selection associated with armour reduction in sticklebacks. Mol. Ecol. 20: 2483-2493.
51. Losos, J.B. 2009. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. University of California Press, Berkley and Los Angeles.
52. McCairns, R.J. & Bernatchez, L. 2008. Landscape genetic analyses reveal cryptic population structure and putative selection gradients in a large-scale estuarine environment. Mol. Ecol. 17: 3901-3916.
53. McKinnon, J.S. & Rundle, H.D. 2002. Speciation in nature: the threespine stickleback model systems. Trends Ecol. Evol. 117: 480-488.
54. McPeek, M.A. & Wellborn, G.A. 1998. Genetic variation and reproductive isolation among phenotypically divergent amphipod populations. Limnol. Oceanog. 43: 1162-1169.
55. McPhail, J.D. 1994. Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. In: The Evolutionary Biology of the Threespine Stickleback (M.A. Bell & S.A. Foster, eds.), pp. 399-437. Oxford University Press, Oxford.
56. Miller, C.T., Beleza, S., Pollen, A.A., Schluter, D., Kittles, R.A., Shriver, M.D. et al. 2007. cis-Regulatory changes in kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131: 1179-1189.
57. Mori, S. 1997. Streams With Sticklebacks: Conservation of Freshwater Ecosystems. Chuko, Tokyo.
58. Mori, S. 2003. Distribution of threespine stickleback in Japan: conserving stickleback populations. In: The Natural History of Sticklebacks (A. Goto & S. Mori, eds), pp. 201-212. Hokkaido University Press, Sapporo.
59. Nadeau, N.J. & Jiggins, C.D. 2010. A golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends Genet. 26: 4840492.
60. Nei, M. & Kumar, S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, Oxford.
61. Nosil, P. 2012. Ecological Speciation. Oxford University Press, New York.
62. Nosil, P., Crespi, B.J. & Sandoval, C.P. 2002. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417: 440-443.
63. Nosil, P., Vines, T.H. & Funk, D.J. 2005. Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59: 705-719.
64. van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4: 535-538.
65. Patankar, R., Von Hippel, F.A. & Bell, M.A. 2006. Extinction of a weakly armoured threespine stickleback (Gasterosteus aculeatus) population in Prator Lake. Alaska. Ecol. Freshwater Fish. 15: 482-487.
66. Peichel, C.L., Nereng, K.S., Ohgi, K.A., Cole, B.L., Colosimo, P.F., Buerkle, C.A. et al. 2001. The genetic architecture of divergence between threespine stickleback species. Nature 414: 901-905.
67. Pinkas, A., Oliphant, M.S. & Iverson, I.K. 1971. Food habits of albacore, bluefin tuna and bonito in California waters. Fish. Bull. 152: 1-105.
68. Price, T., Lovette, I.J., Bermingham, E., Gibbs, H.L. & Richman, A.D. 2000. The imprint of history on communities of North American and Asian warblers. Am. Nat. 156: 354-367.
69. Pritchard, J.K., Stephens, M. & Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
70. R Development Core Team 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
71. ST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Mol. Ecol. 16: 891-905.
72. Raymond, M. & Rousset, F. 1995a. An exact test for population differentiation. Evolution 49: 1280-1283.
73. Raymond, M. & Rousset, F. 1995b. GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
74. Reimchen, T.E. 1994. Predators and morphological evolution in threespine stickleback. In: The Evolutionary Biology of the Threespine Stickleback (M.A. Bell & S.A. Foster, eds), pp. 241-276. Oxford University Press, Oxford.
75. Reimchen, T.E. 2000. Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: implications for stasis and distribution of the ancestral plate condition. Behaviour 137: 1081-1096.
76. Romero, A. 2011. The evolution of cave life. Am. Sci. 99: 144-151.
77. Rosenblum, E.B. & Harmon, L.J. 2011. "Same same but different": replicated ecological speciation at White Sands. Evolution 65: 946-960.
78. Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press, New York.
79. Schluter, D. & Conte, G.L. 2009. Genetics and ecological speciation. Proc. Natl. Acad. Sci. USA 106: 9955-9962.
80. Schluter, D., Clifford, E.A., Nemethy, M. & McKinnon, J.S. 2004. Parallel evolution and inheritance of quantitative traits. Am. Nat. 163: 809-822.
81. Seehausen, O., Takimoto, G., Roy, D. & Jokela, J. 2008. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol. Ecol. 17: 30-44.
82. Shapiro, M.D., Marks, M.E., Peichel, C.L., Blackman, B.K., Nereng, K.S., Jonsson, B. et al. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428: 717-723.
83. Shapiro, M.D., Summers, B.R., Balabhadra, S., Aldenhoven, J.T., Miller, A.L., Cunningham, C.B. et al. 2009. The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Curr. Biol. 19: 1140-1145.
84. Stern, D.L. & Orgogozo, V. 2009. Is genetic evolution predictable? Science 323: 746-751.
85. Stoks, R., Nystrom, J.L., May, M.L. & McPeek, M.A. 2005. Parallel evolution in ecological and reproductive traits to produce cryptic damselfly species across the holarctic. Evolution 59: 1976-1988.
86. Takahashi, H. & Goto, A. 2003. The evolutionary history of ninespine stickleback (genus Pungitius) in the Far East inferred from mtDNA phylogeography. In: The Natural History of Sticklebacks (A. Goto & S. Mori, eds), pp. 74-89. Hokkaido University Press, Sapporo.
87. Takahashi, H., Takata, K. & Goto, A. 2001. Phylogeography of lateral plate dimorphism in the freshwater type of ninespine sticklebacks, genus Pungitius. Ichthyol. Res. 48: 143-154.
88. Takahashi, H., Nagai, T. & Goto, A. 2005. Hybrid male sterility between the fresh- and brackish-water types of ninespine stickleback Pungitius pungitius (Pisces, Gasterosteidae). Zoolog. Sci. 22: 35-40.
89. Takata, K., Goto, A. & Yamazaki, F. 1987. Biochemical identification of a brackish water type of Pungitius pungitius, and its morphological and ecological features in Hokkaido. Japan. Jpn. J. Ichthyol. 34: 176-183.
90. Taylor, E.B. 1999. Species pairs of north temperate freshwater fishes: evolution, taxonomy, and conservation. Rev. Fish Biol. Fisher. 9: 299-334.
91. Taylor, E.B. & McPhail, J.D. 1986. Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus. Can. J. Zool. 64: 416-420.
92. Taylor, E.B., Boughman, J.W., Groenenboom, M., Sniatynski, M., Schluter, D. & Gow, J.L. 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.
93. Tsuruta, T., Machida, Y. & Goto, A. 2008. Nesting habitat use and partitioning of three sympatric ninespine sticklebacks (genus Pungitius): implications for reproductive isolation. Environ. Biol. Fish. 82: 143-150.
94. Vonlanthen, P., Bittner, D., Hudson, A.G., Young, K.A., Müller, R., Lundsgaard-Hansen, B. et al. 2012. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482: 357-362.
95. Wake, D.B., Wake, M.H. & Specht, C.D. 2011. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331: 1032-1035.
96. Wark, A.R. & Peichel, C.L. 2010. Lateral line diversity among ecologically divergent threespine stickleback populations. J. Exp. Biol. 213: 108-117.
97. Whitehead, A., Roach, J.L., Zhang, S. & Galvez, F. 2011. Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc. Natl. Acad. Sci. USA 108: 6193-6198.
98. Wootton, R.J. 1976. The Biology of the Sticklebacks. Academic Press, London.