Breakdown in postmating isolation and the collapse of a species pair through hybridization

American Naturalist

Volumn 175, Issue 1, 2010, Pages 11-26

  Behm, Jocelyn E ^a   Ives, Anthony R ^a   Boughman, Janette W ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Ecological speciation; Endangered species; Gasterosteus aculeatus; Hybridization; Postmating isolation; Threespine stickleback

Indexed keywords

ABUNDANCE; BENTHOS; BODY SHAPE; CYTOPLASMIC INCOMPATIBILITY; ENDANGERED SPECIES; FITNESS; GROWTH RATE; HYBRID; HYBRIDIZATION; MORPHOLOGY; NATURAL SELECTION; PHYLOGENY; REPRODUCTIVE ISOLATION; SURVIVAL; SYMPATRY; TELEOST;

GASTEROSTEUS; GASTEROSTEUS ACULEATUS; PAXTON;

CARBON;

ANIMAL; ARTICLE; BODY SIZE; DIET; FEMALE; GENETICS; HISTOLOGY; HYBRIDIZATION; MALE; PHYSIOLOGY; POPULATION DYNAMICS; SEXUAL BEHAVIOR; SMEGMAMORPHA; SOCIAL ISOLATION; SPECIES DIFFERENTIATION;

ANIMALS; BODY SIZE; CARBON ISOTOPES; DIET; FEMALE; GENETIC SPECIATION; HYBRIDIZATION, GENETIC; MALE; POPULATION DYNAMICS; SEXUAL BEHAVIOR, ANIMAL; SMEGMAMORPHA; SOCIAL ISOLATION;

EID: 77449125337     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/648559     Document Type: Article

References (80)

1. Allen, J. R. M., and R. J. Wootton. 1982. Age, growth and rate of food consumption in an upland population of three-spined stickleback, Gasterosteus aculeatus L. Journal of Fish Biology 21:95-105.
2. Allendorf, F. W., R. F. Leary, P. Spruell, and J. K. Wenburg. 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution 16:613-622.
3. Bagenal, T. B. 1978. Aspects of fish fecundity: ecology of freshwater fish production. Wiley, New York.
4. Barber, M. C., and P. Jenkins. 2001. Differential effects of food and temperature lead to decoupling of short-term otolith and somatic growth rates in juvenile King George whiting. Journal of Fish Biology 58:1320-1330.
5. Baumann, H., M. A. Peck, and J. P. Herrmann. 2005. Short-term decoupling of otolith and somatic growth induced by food level changes in postlarval Baltic sprat, Sprattus sprattus. Marine and Freshwater Research 56:539-547.
6. Baumgartner, D., and K. Rothhaupt. 2003. Predictive length-dry mass regressions for freshwater invertebrates in a pre-alpine lake littoral. International Review of Hyrdobiology 88:453-463.
7. Behm, J. 2006. Loss of ecological separation coupled with postzygotic isolation breakdown in threespine stickleback species pair collapse. MS thesis, University of Wisconsin, Madison.
8. Benke, A. C., A. D. Huryn, L. A. Smock, and J. B. Wallace. 1999. Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. Journal of the North American Benthological Society 18:308-343.
9. Bentzen, P., and J. D. McPhail. 1984. Ecology and evolution of sym- patric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair. Canadian Journal of Zoology 62:2280-2286. (Pubitemid 16275056)
10. Bentzen, P., M. S. Ridgway, and J. D. McPhail. 1984. Ecology and evolution of sympatric sticklebacks (Gasterosteus): spatial segregation and seasonal habitat shifts in the Enos Lake species pair. Canadian Journal of Zoology 62:2436-439.
11. Bolnick, D. I. 2004. Can intraspecific competition drive disruptive selection? an experimental test in natural populations of sticklebacks. Evolution 58:608-18.
12. Bookstein, F. L. 1990. Introduction to methods for landmark data. Pages 215-25 in F. J. Rohlf and F. L. Bookstein, eds. Proceedings of the Michigan Morphometrics Workshop. University of Michigan Museum of Zoology, Ann Arbor.
13. -. 1997. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis 1:225-243.
14. Boughman, J. W. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944-948.
15. -. 2006. Divergence and speciation in sticklebacks: the biology of the three-spined stickleback. CRC, Boca Raton, FL.
16. Brewer, M. J. 2003. Discretisation for inference on normal mixture models. Statistics and Computing 13:209-219.
17. Campana, S. E., and J. D. Neilson. 1985. Microstucture of fish otoliths. Canadian Journal of Fisheries and Aquatic Sciences 42:1014-1032.
18. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.
19. Crawford, L., W. E. Yeomans, and C. E. Adams. 2006. The impact of introduced signal crayfish Pacifastacus leniusculus on stream invertebrate communities. Aquatic Conservation-Marine and Freshwater Ecosystems 16:611-621.
20. Day, T., J. Pritchard, and D. Schluter. 1994. A comparison of 2 sticklebacks. Evolution 48:1723-1734.
21. Dettman, J. R., C. Sirjusingh, L. M. Kohn, and J. B. Anderson. 2007. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447:585-588.
22. Dobzhansky, T. 1951. Genetics and the origin of species. Columbia University Press, New York.
23. Dowling, T., and M. Childs. 1992. Impact of hybridization on a threatened trout of the southwestern United States. Conservation Biology 6:355-364.
24. Downing, J. A., and F. H. Rigler. 1984. A manual on methods for the assessment of secondary productivity in fresh waters. Blackwell Scientific, Oxford.
25. Endler, J. A. 1986. Natural selection in the wild. Princeton University Press, Princeton, NJ.
26. Faubel, A. 1982. Determination of individual meiofauna dry weight values in relation to definite size classes. Cahiers de Biologie Marine 23:339-345.
27. Foster, S. A., J. A. Baker, and M. A. Bell. 2003. The case for conserving threespine stickleback populations: protecting an adaptive radiation. Fisheries 28:10-18.
28. Gow, J. L., C. L. Peichel, and E. B. Taylor. 2006. Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species. Molecular Ecology 15:739-752.
29. - . 2007. Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. Journal of Evolutionary Biology 20:2173-2180.
30. Gow, J. L., S. M. Rogers, M. Jackson, and D. Schluter. 2008. Ecological predictions lead to the discovery of a benthic-limnetic sympatric species pair of threespine stickleback in Little Quarry Lake, British Columbia. Canadian Journal of Zoology 86:564-571.
31. Grant, B. R., and P. R. Grant. 1993. Evolution of Darwin finches caused by a rare climatic event. Proceedings of the Royal Society B: Biological Sciences 251:111-117.
32. - . 1996. High survival of Darwin's finch hybrids: effects of beak morphology and diets. Ecology 77:500-509.
33. Hatfield, T. 2001. Status of the stickleback species pair, Gasterosteus spp., in Hadley Lake, Lasqueti Island, British Columbia. Canadian Field-Naturalist 115:579-583. (Pubitemid 35022087)
34. Hatfield, T., and D. Schluter. 1999. Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866-873.
35. Hatfield, T., J. Rosenfeld, C. Murray, C. J. Foote, D. Jesson, J. D. McPhail, J. Richardson, et al. 2003. National recovery strategy for stickleback species pairs (Gasterosteus spp.) in British Columbia. Prepared for the British Columbia Ministry of Water, Land and Air Protection, and Fisheries and Oceans Canada.
36. Hecky, R. E., and R. H. Hesslein. 1995. Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. Journal of the North American Benthological Society 14:631-653.
37. Hendry, A. P., P. R. Grant, B. R. Grant, H. A. Ford, M. J. Brewer, and J. Podos. 2006. Possible human impacts on adaptive radiation: beak size bimodality in Darwin's finches. Proceedings of the Royal Society B: Biological Sciences 273:1887-1894.
38. Hicks, G. R. F. 1985. Biomass and production estimates for an estuarine meiobenthic copepod, with an instantaneous assessment of exploitation by flatfish predators. New Zealand Journal of Ecology 8:125-127.
39. Kraak, S. B. M., B. Mundwiler, and P. J. B. Hart. 2001. Increased number of hybrids between benthic and limnetic three-spined sticklebacks in Enos Lake, Canada: the collapse of a species pair? Journal of Fish Biology 58:1458-1464.
40. Lavin, P. A., and J. D. McPhail. 1986. Adaptive divergence of trophic phenotype among fresh-water populations of the threespine stickleback (Gasterosteus aculeatus). Canadian Journal of Fisheries and Aquatic Sciences 43:2455-2463.
41. Mason, J. C. 1975. Crayish production in a small woodland stream. Freshwater Crayish 2:449-479.
42. Matsuzaki, S. S., N. Usio, N. Takamura, and I. Washitani. 2009. Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia (Berlin) 158: 673-686.
43. Mayr, E. 1942. Systematics and the origin of species. Columbia University Press, New York.
44. McPhail, J. D. 1984. Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Canadian Journal of Zoology 62:1402-1408.
45. - . 1992. Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texada Island, British Columbia. Canadian Journal of Zoology 70:361-369.
46. - . 1993. Ecology and evolution of sympatric sticklebacks (Gasterosteus): origin ofthe species pairs. Canadian Journal of Zoology 71:515-523.
47. - . 1994. Speciation and the evolution of reproductive isolation in the stickleback (Gasterosteus) of south-western British Columbia: the evolutionary biology ofthe threespine stickleback. Oxford University Press, Oxford.
48. Muller, H. J. 1942. Isolating mechanisms, evolution and temperature. Biological Symposium 6:71-125.
49. Nosil, P. 2007. Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. American Naturalist 169:151-162.
50. Nystrom, P., and J. A. Strand. 1996. Grazing by a native and an exotic crayish on aquatic macrophytes. Freshwater Biology 36:673-682.
51. Reznick, D., E. Lindbeck, and H. Bryga. 1989. Slower growth results in larger otoliths: an experimental test with guppies (Poecilia reticulata). Canadian Journal of Fisheries and Aquatic Sciences 46: 108-112.
52. Rhymer, J. M., and D. Simberloff. 1996. Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27: 83-109.
53. Robinson, B. W. 2000. Trade offs in habitat-speciic foraging eficiency and the nascent adaptive divergence ofsticklebacks in lakes. Behaviour 137:865-888.
54. Rohlf, F. J. 1999. Shape statistics: Procrustes superimpositions and tangent spaces. Journal of Classiication 16:197-223.
55. -. 2005. tpsRelw, version 1.42. Department of Ecology and Evolution, State University of New York at Stony Brook, http://life.bio.sunysb.edu/morph.
56. -. 2006. tpsDIG2, version 2.05. Department of Ecology and Evolution. State University of New York at Stony Brook, http://life.bio.sunysb.edu/morph.
57. Rundle, H. D. 2002. A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution 56:322-329.
58. Rundle, H. D., and P. Nosil. 2005. Ecological speciation. Ecology Letters 8:336-352.
59. Rundle, H. D., L. Nagel, J. W. Boughman, and D. Schluter. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306-308.
60. Rundle, H. D., S. M. Vamosi, and D. Schluter. 2003. Experimental test of predation's effect on divergent selection during character displacement in sticklebacks. Proceedings of the National Academy of Sciences of the USA 100:14943-14948.
61. Schluter, D. 1993. Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74:699-709.
62. -. 1995. Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 76:82-90.
63. -. 2001. Ecology and the origin of species. Trends in Ecology amp; Evolution 16:372-380.
64. -. 2003. Frequency dependent natural selection during character displacement in sticklebacks. Evolution 57:1142-1150.
65. Schluter, D., and J. D. McPhail. 1992. Ecological character displacement and speciation in sticklebacks. American Naturalist 140:85-108.
66. Secor, D. H., and J. M. Dean. 1989. Somatic growth effects on the otolith-fish size relationship in young pond-reared striped bass, Morone saxatalis. Canadian Journal of Fisheries and Aquatic Sciences 46:113-121.
67. Seehausen, O. 2006. Conservation: losing biodiversity by reverse speciation. Current Biology 16:R334-R337.
68. Seehausen, O., J. J. M. van Alphen, and F. Witte. 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808-1811.
69. Seehausen, O., G. Takimoto, D. Roy, and J. Jokela. 2008. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology 17:30-44.
70. Taylor, E. B. 2004. An analysis ofhomogenization and differentiation of Canadian freshwater fish faunas with an emphasis on British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 61: 68-79.
71. Taylor, E. B., J. W. Boughman, M. Groenenboom, M. Sniatynski, D. Schluter, and J. L. Gow. 2006. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology 15:343-355.
72. Vamosi, S. M., and D. Schluter. 2002. Impacts of trout predation on fitness of sympatric sticklebacks and their hybrids. Proceedings of the Royal Society B: Biological Sciences 269:923-930.
73. Vamosi, S. M., T. Hatfield, and D. Schluter. 2000. A test of ecological selection against young-of-the-year hybrids of sympatric sticklebacks. Journal of Fish Biology 57:109-121.
74. 15N and the trophic position of aquatic consumers. Ecology 80:1395-1404.
75. Vander Zanden, M. J., J. M. Casselman, and J. B. Rasmussen. 1999. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464-467.
76. Vander Zanden, M. J., S. Chandra, B. C. Allen, J. E. Reuter, and C. R. Goldman. 2003. Historical food web structure and restoration of native aquatic communities in the Lake Tahoe (California-Nevada) Basin. Ecosystems 6:274-288.
77. Weatherley, A. H., and H. S. Gill. 1987. The biology of fish growth. Academic Press, San Diego, CA.
78. Wright, P. J., N. B. Metcalfe, and J. E. Thorpe. 1990. Otolith and somatic growth rates in Atlantic salmon parr, Salmo salar L.: evidence against coupling. Journal of Fish Biology 36:241-249.
79. Yezerinac, S. M., S. C. Lougheed, and P. Handford. 1992. Measurement error and morphometric studies: statistical power and observer experience. Systematic Biology 41:471-482.
80. Zhang, Y. X., J. S. Richardson, and J. N. Negishi. 2004. Detritus processing, ecosystem engineering and benthic diversity: a test of predator-omnivore interference. Journal of Animal Ecology 73: 756-766.