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International Journal of Ecology
Volume 2012 (2012), Article ID 902438, 14 pages
doi:10.1155/2012/902438
Divergent Selection and Then What Not: The Conundrum of Missing Reproductive Isolation in Misty Lake and Stream Stickleback
1Redpath Museum and Department of Biology, McGill University, 859 Sherbrooke Street. W, Montreal, QC, H3A 2K6, Canada
2Department of Aquatic Ecology, Eawag and ETH-Zurich, Institute of Integrative Biology, Ueberlandstraβe 133, 8600 Duebendorf, Switzerland
3Department of Biology and Centre for Advanced Research in Environmental Genomics, University of Ottawa, Ottawa, ON, K1N 6N5, Canada
Received 1 July 2011; Accepted 28 October 2011
Academic Editor: Rui Faria
Copyright © 2012 Katja Räsänen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- D. Schluter, The Ecology of Adaptive Radiation, Oxford University Press, Oxford, UK, 2000.
- H. D. Rundle and P. Nosil, “Ecological speciation,” Ecology Letters, vol. 8, no. 3, pp. 336–352, 2005. View at Publisher · View at Google Scholar · View at Scopus
- D. J. Funk, P. Nosil, and W. J. Etges, “Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 9, pp. 3209–3213, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. J. Funk, “Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles,” Evolution, vol. 52, no. 6, pp. 1744–1759, 1998. View at Scopus
- H. D. Rundle, L. Nagel, J. W. Boughman, and D. Schluter, “Natural selection and parallel speciation in sympatric sticklebacks,” Science, vol. 287, no. 5451, pp. 306–308, 2000. View at Publisher · View at Google Scholar · View at Scopus
- P. Nosil, B. J. Crespi, and C. P. Sandoval, “Host-plant adaptation drives the parallel evolution of reproductive isolation,” Nature, vol. 417, no. 6887, pp. 440–443, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. S. McKinnon, S. Mori, B. K. Blackman et al., “Evidence for ecology's role in speciation,” Nature, vol. 429, no. 6989, pp. 294–298, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. W. Boughman, H. D. Rundle, and D. Schluter, “Parallel evolution of sexual isolation in sticklebacks,” Evolution, vol. 59, no. 2, pp. 361–373, 2005. View at Scopus
- T. H. Vines and D. Schluter, “Strong assortative mating between allopatric sticklebacks as a by-product of adaptation to different environments,” Proceedings of the Royal Society B, vol. 273, no. 1589, pp. 911–916, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- R. B. Langerhans, M. E. Gifford, and E. O. Joseph, “Ecological speciation in Gambusia fishes,” Evolution, vol. 61, no. 9, pp. 2056–2074, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. Ellers and C. L. Boggs, “The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies,” Evolution, vol. 57, no. 5, pp. 1100–1106, 2003. View at Scopus
- H. D. Rundle, “Divergent environments and population bottlenecks fail to generate premating isolation in Drosophila pseudoobscura,” Evolution, vol. 57, no. 11, pp. 2557–2565, 2003. View at Scopus
- A. Brelsford and D. E. Irwin, “Incipient speciation despite little assortative mating: the yellow-rumped warbler hybrid zone,” Evolution, vol. 63, no. 12, pp. 3050–3060, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- L. Kwan and H. D. Rundle, “Adaptation to desiccation fails to generate pre- and postmating isolation in replicate Drosophila melanogaster laboratory populations,” Evolution, vol. 64, no. 3, pp. 710–723, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- A. K. Schwartz, D. J. Weese, P. Bentzen, M. T. Kinnison, and A. P. Hendry, “Both geography and ecology contribute to mating isolation in guppies,” PLoS ONE, vol. 5, no. 12, Article ID e15659, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- A. P. Hendry, “Ecological speciation! Or the lack thereof?” Canadian Journal of Fisheries and Aquatic Sciences, vol. 66, no. 8, pp. 1383–1398, 2009. View at Publisher · View at Google Scholar · View at Scopus
- P. Nosil, L. J. Harmon, and O. Seehausen, “Ecological explanations for (incomplete) speciation,” Trends in Ecology and Evolution, vol. 24, no. 3, pp. 145–156, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- P. Nosil, “Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks,” American Naturalist, vol. 169, no. 2, pp. 151–162, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- E. B. Rosenblum and L. J. Harmon, ““Same same but different”: replicated ecological speciation at white sands,” Evolution, vol. 65, no. 4, pp. 946–960, 2011. View at Publisher · View at Google Scholar · View at PubMed
- M. A. Bell and S. A. Foster, The Evolutionary Biology of the Threespine Stickleback, Oxford University Press, New York, NY, USA, 1994.
- J. S. McKinnon and H. D. Rundle, “Speciation in nature: the threespine stickleback model systems,” Trends in Ecology and Evolution, vol. 17, no. 10, pp. 480–488, 2002. View at Publisher · View at Google Scholar · View at Scopus
- A. P. Hendry, D. I. Bolnick, D. Berner, and C. L. Peichel, “Along the speciation continuum in sticklebacks,” Journal of Fish Biology, vol. 75, no. 8, pp. 2000–2036, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- M. S. Ridgway and J. D. McPhail, “Ecology and evolution of sympatric sticklebacks (Gasterosteus): mate choice and reproductive isolation in the Enos Lake species pair,” Canadian Journal of Zoology, vol. 62, no. 9, pp. 1813–1818, 1984. View at Scopus
- L. Nagel and D. Schluter, “Body size, natural selection, and speciation in sticklebacks,” Evolution, vol. 52, no. 1, pp. 209–218, 1998. View at Scopus
- G. M. Kozak, M. Reisland, and J. W. Boughmann, “Sex differences in mate recognition and conspecific preference in species with mutual mate choice,” Evolution, vol. 63, no. 2, pp. 353–365, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. E. Hay and J. D. McPhail, “Mate selection in threespine sticklebacks,” Canadian Journal of Zoology, vol. 53, pp. 441–450, 1975.
- G. Á. Ólafsdóttir, M. G. Ritchie, and S. S. Snorrason, “Positive assortative mating between recently described sympatric morphs of Icelandic sticklebacks,” Biology Letters, vol. 2, no. 2, pp. 250–252, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- F. C. Jones, C. Brown, and V. A. Braithwaite, “Lack of assortative mating between incipient species of stickleback from a hybrid zone,” Behaviour, vol. 145, no. 4-5, pp. 463–484, 2008. View at Scopus
- J. A. M. Raeymaekers, M. Boisjoly, L. Delaire, D. Berner, K. Räsänen, and A. P. Hendry, “Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback,” Journal of Evolutionary Biology, vol. 23, no. 12, pp. 2694–2708, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- C. E. Thompson, E. B. Taylor, and J. D. Mcphail, “Parallel evolution of lake-stream pairs of threespine sticklebacks (Gasterosteus) inferred from mitochondrial DNA variation,” Evolution, vol. 51, no. 6, pp. 1955–1965, 1997. View at Scopus
- A. P. Hendry and E. B. Taylor, “How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs,” Evolution, vol. 58, no. 10, pp. 2319–2331, 2004. View at Scopus
- D. Berner, A. C. Grandchamp, and A. P. Hendry, “Variable progress toward ecological speciation in parapatry: stickleback across eight lake-stream transitions,” Evolution, vol. 63, no. 7, pp. 1740–1753, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. Berner, M. Roesti, A. P. Hendry, and W. Salzburger, “Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents,” Molecular Ecology, vol. 19, no. 22, pp. 4963–4978, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- G. E. E. Moodie, “Morphology, life history and ecology of an unusual stickleback (Gasterosteus aculeatus) in the Queen Charlotte Islands, Canada,” Canadian Journal of Zoology, vol. 50, pp. 721–732, 1972.
- G. E. E. Moodie, “Predation, natural selection and adaptation in an unusual threespine stickleback,” Heredity, vol. 28, pp. 155–167, 1972.
- T. E. Reimchen, E. M. Stinson, and J. S. Nelson, “Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands,” Canadian Journal of Zoology, vol. 63, pp. 2944–2951, 1985.
- P. A. Lavin and J. D. McPhail, “Parapatric lake and stream sticklebacks on northern Vancouver Island: disjunct distribution or parallel evolution?” Canadian Journal of Zoology, vol. 71, no. 1, pp. 11–17, 1993. View at Scopus
- A. P. Hendry, E. B. Taylor, and J. D. McPhail, “Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the Misty system,” Evolution, vol. 56, no. 6, pp. 1199–1216, 2002. View at Scopus
- D. Berner, D. C. Adams, A. C. Grandchamp, and A. P. Hendry, “Natural selection drives patterns of lake-stream divergence in stickleback foraging morphology,” Journal of Evolutionary Biology, vol. 21, no. 6, pp. 1653–1665, 2008. View at Publisher · View at Google Scholar · View at PubMed
- A. P. Hendry, K. Hudson, J. A. Walker, K. Räsänen, and L. J. Chapman, “Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback,” Journal of Evolutionary Biology, vol. 24, no. 1, pp. 23–35, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. S. Moore, J. L. Gow, E. B. Taylor, and A. P. Hendry, “Quantifying the constraining influence of gene flow on adaptive divergence in the lake-stream threespine stickleback system,” Evolution, vol. 61, no. 8, pp. 2015–2026, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- K. Räsänen and A. P. Hendry, “Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification,” Ecology Letters, vol. 11, no. 6, pp. 624–636, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- S. Gavrilets and A. Vose, “Dynamic patterns of adaptive radiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 50, pp. 18040–18045, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- X. Thibert-Plante and A. P. Hendry, “Five questions on ecological speciation addressed with individual-based simulations,” Journal of Evolutionary Biology, vol. 22, no. 1, pp. 109–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
- X. Thibert-Plante and A. P. Hendry, “When can ecological speciation be detected with neutral loci?” Molecular Ecology, vol. 19, no. 11, pp. 2301–2314, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. M. T. Sharpe, K. Räsänen, D. Berner, and A. P. Hendry, “Genetic and environmental contributions to the morphology of lake and stream stickleback: implications for gene flow and reproductive isolation,” Evolutionary Ecology Research, vol. 10, no. 6, pp. 849–866, 2008. View at Scopus
- J. S. Moore and A. P. Hendry, “Both selection and gene flow are necessary to explain adaptive divergence: evidence from clinal variation in stream stickleback,” Evolutionary Ecology Research, vol. 7, no. 6, pp. 871–886, 2005. View at Scopus
- G. M. Kozak, M. L. Head, and J. W. Boughman, “Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks,” Proceedings of the Royal Society B, vol. 278, no. 1718, pp. 2604–2610, 2011. View at Publisher · View at Google Scholar · View at PubMed
- G. M. Kozak and J. W. Boughman, “Learned conspecific mate preference in a species pair of sticklebacks,” Behavioral Ecology, vol. 20, no. 6, pp. 1282–1288, 2009. View at Publisher · View at Google Scholar · View at Scopus
- J. H. Jennings and W. J. Etges, “Species hybrids in the laboratory but not in nature: a reanalysis of premating isolation between Drosophila arizonae and D. mojavensis,” Evolution, vol. 64, no. 2, pp. 587–598, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- M. Delcourt, K. Räsänen, and A. P. Hendry, “Genetic and plastic components of divergent male intersexual behavior in Misty lake/stream stickleback,” Behavioral Ecology, vol. 19, no. 6, pp. 1217–1224, 2008. View at Publisher · View at Google Scholar · View at Scopus
- T. Hatfield and D. Schluter, “A test for sexual selection on hybrids of two sympatric sticklebacks,” Evolution, vol. 50, no. 6, pp. 2429–2434, 1996. View at Scopus
- J. A. M. Raeymaekers, L. Delaire, and A. P. Hendry, “Genetically based differences in nest characteristics between lake, inlet, and hybrid threespine stickleback from the misty system, British Columbia, Canada,” Evolutionary Ecology Research, vol. 11, no. 6, pp. 905–919, 2009. View at Scopus
- H. D. Rundle and D. Schluter, “Reinforcement of stickleback mate preferences: sympatry breeds contempt,” Evolution, vol. 52, no. 1, pp. 200–208, 1998. View at Scopus
- J. D. McPhail and D. E. Hay, “Differences in male courtship in freshwater and marine sticklebacks,” Canadian Journal of Zoology, vol. 61, pp. 292–297, 1983.
- S. A. Foster, “Understanding the evolution of behavior in threespine stickleback: the value of geographic variation,” Behaviour, vol. 132, no. 15-16, pp. 1107–1129, 1995. View at Scopus
- M. Ishikawa and S. Mori, “Mating success and male courtship behaviors in three populations of the threespine stickleback,” Behaviour, vol. 137, no. 7-8, pp. 1065–1080, 2000. View at Scopus
- SAS Institute, SAS/STAT® 9.2 User’s Guide, SAS Institute, Cary, NC, USA, 2008.
- K. P. Burnham and D. R. Andersson, Model Selection and Multimodel Inference: A Practical Information-Theoretical Approach, Springer, New York, NY, USA, 2nd edition, 2002.
- E. Lewandowski and J. Boughman, “Effects of genetics and light environment on colour expression in threespine sticklebacks,” Biological Journal of the Linnean Society, vol. 94, no. 4, pp. 663–673, 2008. View at Publisher · View at Google Scholar · View at Scopus
- M. J. West-Eberhardt, Developmental Plasticity and Evolution, Oxford University Press, New York, NY, USA, 2003.
- E. Crispo, “Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow,” Journal of Evolutionary Biology, vol. 21, no. 6, pp. 1460–1469, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- R. Svanbäck, M. Pineda-Krch, and M. Doebeli, “Fluctuating population dynamics promotes the evolution of phenotypic plasticity,” American Naturalist, vol. 174, no. 2, pp. 176–189, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. W. Pfennig, M. A. Wund, E. C. Snell-Rood, T. Cruickshank, C. D. Schlichting, and A. P. Moczek, “Phenotypic plasticity's impacts on diversification and speciation,” Trends in Ecology and Evolution, vol. 25, no. 8, pp. 459–467, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- X. Thibert-Plante and A. P. Hendry, “The consequences of phenotypic plasticity for ecological speciation,” Journal of Evolutionary Biology, vol. 24, no. 2, pp. 326–342, 2011. View at Publisher · View at Google Scholar · View at PubMed
- D. Schluter, “Ecology and the origin of species,” Trends in Ecology and Evolution, vol. 16, no. 7, pp. 372–380, 2001. View at Publisher · View at Google Scholar · View at Scopus
- A. S. Kondrashov and F. A. Kondrashov, “Interactions among quantitative traits in the course of sympatric speciation,” Nature, vol. 400, no. 6742, pp. 351–354, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. D. Fry, “Multilocus models of sympatric speciation: bush versus rice versus felsenstein,” Evolution, vol. 57, no. 8, pp. 1735–1746, 2003. View at Scopus
- S. Gavrilets, Fitness Landscapes and the Origin of Species, Princeton University Press, Princeton, NJ, USA, 2004.
- M. R. Servedio, G. S. V. Doorn, M. Kopp, A. M. Frame, and P. Nosil, “Magic traits in speciation: “magic” but not rare?” Trends in Ecology and Evolution, vol. 26, no. 8, pp. 389–397, 2011. View at Publisher · View at Google Scholar · View at PubMed
- A. Y. K. Albert and D. Schluter, “Reproductive character displacement of male stickleback mate preference: reinforcement or direct selection?” Evolution, vol. 58, no. 5, pp. 1099–1107, 2004. View at Scopus
- S. B. M. Kraak and T. C. M. Bakker, “Mutual mate choice in sticklebacks: attractive males choose big females, which lay big eggs,” Animal Behaviour, vol. 56, no. 4, pp. 859–866, 1998. View at Publisher · View at Google Scholar · View at Scopus
- U. Candolin and H. R. Voigt, “Correlation between male size and territory quality: consequence of male competition or predation susceptibility?” Oikos, vol. 95, no. 2, pp. 225–230, 2001. View at Scopus
- G. E. E. Moodie, “Why asymmetric mating preferences may not show the direction of evolution,” Evolution, vol. 36, pp. 1096–1097, 1982.
- W. J. Rowland, “Mate choice and the supernormality effect in female sticklebacks (Gasterosteus aculeatus),” Behavioral Ecology and Sociobiology, vol. 24, no. 6, pp. 433–438, 1989. View at Publisher · View at Google Scholar
- J. Felsenstein, “Skepticism towards Santa Rosalia, or why are there so few kinds of animals?” Evolution, vol. 35, pp. 124–138, 1981.
- M. R. Servedio, “Beyond reinforcement: the evolution of premating isolation by direct selection on preferences and postmating, prezygotic incompatibilities,” Evolution, vol. 55, no. 10, pp. 1909–1920, 2001. View at Scopus
- M. R. Servedio and M. A. F. Noor, “The role of reinforcement in speciation: theory and data,” Annual Review of Ecology, Evolution, and Systematics, vol. 34, pp. 339–364, 2003. View at Scopus
- P. Nosil, T. H. Vines, and D. J. Funk, “Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats,” Evolution, vol. 59, no. 4, pp. 705–719, 2005. View at Scopus
- D. B. Lowry, J. L. Modliszewski, K. M. Wright, C. A. Wu, and J. H. Willis, “Review. The strength and genetic basis of reproductive isolating barriers in flowering plants,” Philosophical Transactions of the Royal Society B, vol. 363, no. 1506, pp. 3009–3021, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. L. Feder, S. B. Opp, B. Wlazlo, K. Reynolds, W. Go, and S. Spisak, “Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 17, pp. 7990–7994, 1994. View at Publisher · View at Google Scholar · View at Scopus
- D. J. Bolnick, L. Snowberg, C. Patenia, O. L. Lau, W. E. Stutz, and T. Ingram, “Habitat choice contributes to adaptive divergence between lake and stream populations of three-spine stickleback,” Evolution, vol. 63, pp. 2004–2016, 2009.
- R. D. Alexander and R. S. Bigelow, “Allochronic speciation in field crickets, and a new species, Acheta veletis,” Evolution, vol. 14, pp. 334–346, 1960.
- V. L. Friesen, A. L. Smith, E. Gómez-Díaz et al., “Sympatric speciation by allochrony in a seabird,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 47, pp. 18589–18594, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- S. Via, A. C. Bouck, and S. Skillman, “Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments,” Evolution, vol. 54, no. 5, pp. 1626–1637, 2000. View at Scopus
- D. C. Presgraves, L. Balagopalan, S. M. Abmayr, and H. A. Orr, “Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila,” Nature, vol. 423, no. 6941, pp. 715–719, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. Ramsey, H. D. Bradshaw, and D. W. Schemske, “Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae),” Evolution, vol. 57, no. 7, pp. 1520–1534, 2003. View at Scopus
- R. K. Butlin, J. Galindo, and J. W. Grahame, “Review. Sympatric, parapatric or allopatric: the most important way to classify speciation?” Philosophical Transactions of the Royal Society B, vol. 363, no. 1506, pp. 2997–3007, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus