Local adaptation to salinity in the three-spined stickleback?

Journal of Evolutionary Biology

Volumn 27, Issue 2, 2014, Pages 290-302

  Defaveri, J ^a   Merila J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Gasterosteus aculeatus; Genetic differentiation; Growth; Local adaptation; Mortality; Salinity

Indexed keywords

EXPERIMENTAL DESIGN; GENE FLOW; GENETIC DRIFT; GROWTH RATE; LOCAL ADAPTATION; MARINE ENVIRONMENT; MORTALITY; OSMOREGULATION; SALINITY TOLERANCE; TELEOST;

GASTEROSTEUS ACULEATUS; SPINACHIA SPINACHIA; VERTEBRATA;

SEA WATER;

ADAPTATION; ANIMAL; ARTICLE; BODY SIZE; CHEMISTRY; FEMALE; GASTEROSTEUS ACULEATUS; GENE FLOW; GENETIC DRIFT; GENETIC VARIABILITY; GENETICS; GROWTH; HISTOLOGY; LOCAL ADAPTATION; MALE; MORTALITY; PHYSIOLOGY; SALINITY; SMEGMAMORPHA;

GASTEROSTEUS ACULEATUS; GENETIC DIFFERENTIATION; GROWTH; LOCAL ADAPTATION; MORTALITY; SALINITY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BODY SIZE; FEMALE; GENE FLOW; GENETIC DRIFT; MALE; SEAWATER; SMEGMAMORPHA;

EID: 84892863249     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12289     Document Type: Article

References (76)

1. Baker, J.A., Heins, D.C., Foster, S.A. & King, R.W. 2008. An overview of life-history variation in female threespine stickleback. Behaviour 145: 579-602.
2. Barrett, R.D.H. & Hoekstra, H. 2011. Molecular spandrels: tests of adaptation at the genetic level. Nat. Rev. Genet. 12: 767-780.
3. Barrett, R.D.H., Rogers, S.M. & Schluter, D. 2009. Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback. Evolution 63: 2831-2837.
4. Belanger, G., Guderly, H. & FitzGerald, G.J. 1987. Salinity during embryonic development influences the response to salinity of Gasterosteus aculeatus L. (trachurus). Can. J. Zool. 65: 451-454.
5. Blanquart, F., Gandon, S. & Nuismer, S.L. 2012. The effects of migration and drift on local adaptation to a heterogeneous environment. J. Evol. Biol. 25: 1351-1363.
6. Blanquart, F., Kaltz, O., Nuismer, S. & Gandon, S. 2013. A practical guide to measuring local adaptation. Ecol. Lett. 16: 1195-1205.
7. Borland, M. 1986. Size-assortative mating in threespine sticklebacks from two sites on the Salmon River, British Columbia. Master's thesis. University of British Columbia, Vancouver, BC.
8. Campeau, S., Guderley, H. & Fitzgerald, G. 1984. Salinity tolerances and preferences of fry of two species of sympatric sticklebacks: possible mechanisms of habitat segregation. Can. J. Zool. 62: 1048-1105.
9. Conover, D.O. 1998. Local adaptation in marine fishes: evidence and implications for stock enhancement. Bull. Mar. Sci. 62: 477-493.
10. Conover, D.O. & Present, T.M.C. 1990. Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83: 316-324.
11. Conover, D.O. & Schultz, E.T. 1995. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol. Evol. 10: 248-252.
12. Conover, D.O., Clarke, L.M., Munch, S.B. & Wagner, G.N. 2006. Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J. Fish Biol. 69: 21-47.
13. Conte, G.L. & Schluter, D. 2013. Experimental confirmation that body size determines mate preference via phenotype matching in a stickleback species pair. Evolution 67: 1477-1484.
14. DeFaveri, J. & Merilä, J. 2013. Evidence for adaptive phenotypic divergence in Baltic Sea sticklebacks. J. Evol. Biol. 26: 1700-1715.
15. DeFaveri, J., Jonsson, P.R. & Merilä, J. 2013. Heterogeneous genomic differentiation in marine threespine sticklebacks: adaptation along an environmental gradient. Evolution 67: 2530-2546.
16. Endler, J.A. 1973. Gene flow and population differentiation. Science 179: 243-250.
17. Fraser, D.J., Weir, L.K., Bernatchez, L., Hansen, M.M. & Taylor, E.B. 2011. Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106: 404-420.
18. Gaggiotti, O.E., Bekkevold, D., Jørgensen, H.B., Foll, M., Carvalho, G.R., Andre, C. et al. 2009. Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63: 2939-2951.
19. Gomes-Mestre, I. & Tejedo, M. 2003. Local adaptation of an anuran amphibian to osmotically stressful environments. Evolution 57: 1889-1899.
20. Goudet, J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm.
21. Grosberg, R. & Cunningham, C.W. 2001. Genetic structure in the sea. In: Marine Community Ecology (M.D. Bertness, S. Gaines & M.E. Hay, eds), pp. 61-84. Sinauer, Sunderland, MA.
22. Guderly, H.E. 1994. Physiological ecology and evolution of the threespine stickleback. In: The Evolutionary Biology of the Threespine Stickleback (M.A. Bell & S.A. Foster, eds), pp. 85-113. Oxford University Press, Oxford.
23. Gutz, M. 1970. Experimental studies on adaptation to salinity shown by the different races of the three-spined stickleback (Gasterosteus aculeatus L.). Internat. Rev. Gesamten Hydrobiol. Hydrogr. 55: 845-894.
24. Hauser, L. & Carvalho, G.R. 2008. Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish. 9: 333-362.
25. Hemmer-Hansen, J., Nielsen, E.E., Frydenberg, J. & Loeschcke, V. 2007. Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity 99: 592-600.
26. Hereford, J. 2009. A quantitative survey of local adaptation and fitness trade-offs. Am. Nat. 173: 579-588.
27. Hice, L.A., Duffy, T.A., Munch, S.B. & Conover, D.O. 2012. Spatial scale and divergent patterns of variation in adapted traits in the ocean. Ecol. Lett. 15: 568-575.
28. Hutchings, J.A., Swain, D.P., Rowe, S., Eddington, J.D., Puvanendran, V. & Brown, J.A. 2007. Genetic variation in life-history reaction norms in a marine fish. Proc. R. Soc. Lond., B, Biol. Sci. 274: 1693-1699.
29. Jørgensen, A.T., Hansen, B.W., Vismann, B., Jacobsen, L., Skov, C., Berg, S., et al. 2010. High salinity tolerance in eggs and fry of a brackish Esox lucius population. Fisheries Manag. Ecol. 17: 554-560.
30. Jørgensen, H.B., Hansen, M.M., Bekkevold, D., Ruzzante, D.E. & Loeschcke, V. 2005. Marine landscapes and population genetic structure of herring (Clupea harengus L.) in the Baltic Sea. Mol. Ecol. 14: 3219-3234.
31. Karås, P. & Klingsheim, V. 1997. Effects of temperature and salinity on embryonic development of turbot (Scophthalmus maximus L.) from the North Sea, and comparisons with Baltic populations. Helgol. Meeresunters 51: 241-247.
32. Kawecki, T.J. & Ebert, D. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7: 1225-1241.
33. Kuhlman, D. & Quantz, G. 1980. Some effects of temperature and salinity on the embryonic development and incubation time of the turbot, Scophthalrnus maximus L., from the Baltic Sea. Meeresforschung 28: 172-178.
34. Langerhans, R.B. & DeWitt, T.J. 2004. Shared and unique features of evolutionary diversification. Am. Nat. 164: 335-349.
35. Leimu, R. & Fischer, M. 2008. A meta-analysis of local adaptation in plants. PLoS ONE 3: e4010.
36. Leinonen, T., Cano, J.M. & Merilä, J. 2006. Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespined sticklebacks. J. Evol. Biol. 19: 1803-1812.
37. Leinonen, T., Cano, J.M. & Merilä, J. 2011. Genetics of body shape and armour variation in threespine sticklebacks. J. Evol. Biol. 24: 206-218.
38. ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat. Rev. Genet. 14: 179-190.
39. Limborg, M.T., Pedersen, J.S., Hemmer-Hansen, J., Hemmer-Hansen, J., Tomkiewicz, J. & Bekkevold, D. 2009. Genetic population structure of European sprat Sprattus sprattus: differentiation across a steep environmental gradient in a small pelagic fish. Mar. Ecol. Prog. Ser. 379: 213-224.
40. Limborg, M.T., Heylar, S.J., DeBruyn, M., Taylor, M.I., Nielsen, E.E., Ogden, R. et al. 2012. Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol. Ecol. 21: 3686-3703.
41. Lind, M.I., Ingvarsson, P.K., Johansson, H., Hall, D. & Johansson, F. 2011. Gene flow and selection on phenotypic plasticity in an island system of Rana temporaria. Evolution 65: 684-697.
42. Marchinko, K.B. & Schluter, D. 2007. Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution 61: 1084-1090.
43. Marcil, J., Swain, D.P. & Hutchings, J.A. 2006. Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.). Biol. J. Linn. Soc. 88: 351-365.
44. McCairns, R.J.S. & 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.
45. McCairns, R.J.S. & Bernatchez, L. 2010. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64: 1029-1047.
46. McCairns, R.J.S. & Bernatchez, L. 2012. Plasticity and heritability of morphological variation within and between parapatric stickleback demes. J. Evol. Biol. 25: 1097-1112.
47. McGuigan, K., Nishimura, N., Currey, M., Hurwit, D. & Cresko, W.A. 2011. Cryptic genetic variation and body size evolution in threespine stickleback. Evolution 65: 1203-1211.
48. Moloney, K.A., Holzapfel, C., Tielbörger, K., Jeltsch, F. & Schurr, F.M. 2009. Rethinking the common garden in invasion research. Perspect. Plant Ecol. Evol. Syst. 11: 311-320.
49. Münzing, J. 1963. The evolution of variation and distributional patterns in European populations of the three-spined stickleback, Gasterosteus aculeatus. Evolution 17: 320-332.
50. Nagel, L. & Schluter, D. 1998. Body size, natural selection, and speciation in sticklebacks. Evolution 52: 209-218.
51. Nielsen, E.E., Nielsen, P.H., Meldrup, D. & Hansen, M.M. 2004. Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol. Ecol. 13: 585-595.
52. Nielsen, E.E., Hemmer-Hansen, J., Larsen, P.F. & Bekkevold, D. 2009. Population genomics of marine fishes: identifying adaptive variation in space and time. Mol. Ecol. 18: 3128-3150.
53. Nissling, A. & Westin, L. 1991a. Egg mortality and hatching rate of Baltic cod (Gadus morhua) in different salinities. Mar. Biol. 111: 29-32.
54. Nissling, A. & Westin, L. 1991b. Egg buoyancy of Baltic cod (Gadus morhua) and its implications for cod stock fluctuations in the Baltic. Mar. Biol. 111: 33-35.
55. Nissling, A., Kryvi, H. & Vallin, L. 1994. Variation in egg buoyancy of Baltic cod Gadus morhua and its implications for egg survival in prevailing conditions in the Baltic Sea. Mar. Ecol. Prog. Ser. 110: 67-74.
56. Nosil, P. 2012. Ecological Speciation. Oxford University Press, Oxford.
57. Nosil, P., Funk, D.J. & Ortiz-Barrientos, D. 2009. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18: 375-402.
58. Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M.H.H., Oksanen, M.J. et al. 2007. The vegan package. Community ecology package. Disponível em: http://www.R-project.org. Acesso em 10.01 (2007): 2008.
59. Pespeni, M.H., Sanford, E., Gaylord, B., Hill, T.M., Hosfelt, J.D., Jaris, H.K. et al. 2013. Evolutionary change during experimental ocean acidification. Proc. Natl. Acad. Sci. USA. 110: 6937-6942.
60. Ricker, W.E. 1975. Computation and interpretation of biological statistic of fish populations. Bull. Fish. Res. Board. Can. 191: 1-382.
61. Rohlf, F.J. 2006. tpsDig, version 2.10. Department of Ecology and Evolution, State University of New York, Stony Brook.
62. Rossiter, M. 1996. Incidence and consequences of inherited environmental effects. Annu. Rev. Ecol. Evol. Syst. 27: 451-476.
63. Salinas, S. & Munch, S.B. 2012. Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol. Lett. 15: 159-163.
64. Sanford, E. & Kelly, M.W. 2011. Local adaptation in marine invertebrates. Ann. Rev. Mar. Sci. 3: 509-535.
65. Savolainen, O., Pyhäjärvi, T. & Knürr, T. 2007. Gene flow and local adaptation in trees. Annu. Rev. Ecol. Evol. Syst. 38: 595-619.
66. Schluter, D. 2000. Ecological character displacement in adaptive radiation. Am. Nat. 156: S4-S16.
67. Schultz, E.T., Reynolds, K.E. & Conover, D.O. 1996. Countergradient variation in growth among newly hatched Fundulus heteroclitus: geographic differences revealed by common-environment experiments. Funct. Ecol. 10: 366-374.
68. Shimada, Y., Shikano, T. & Merilä, J. 2011. A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol. Biol. Evol. 28: 181-193.
69. Spence, R., Wootton, R.J., Przybylski, M., Zie{ogonek}ba, G., Macdonald, K. & Smith, C. 2012. Calcium and salinity as selective factors in plate morph evolution of the three-spined stickleback (Gasterosteus aculeatus). J. Evol. Biol. 25: 1965-1974.
70. Storz, J.F. & Wheat, C.W. 2010. Integrating evolutionary and functional approaches to infer adaptation at specific loci. Evolution 64: 2489-2509.
71. Thrall, P.H., Burdon, J.J. & Bever, J.D. 2002. Local adaptation in the Linum marginale-it Melampsora lini host-pathogen interaction. Evolution 56: 1340-1351.
72. Via, S. 2012. Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Phil. Trans. R. Soc. B 367: 451-460.
73. Westin, L. & Nissling, A. 1991. Effects of salinity on spermatozoa motility, percentage of fertilized eggs and egg development of Baltic cod (Gadus morhua), and implication for cod stock fluctuations in the Baltic. Mar. Biol. 108: 5-9.
74. ST. Genetics 183: 1055-1063.
75. Winkler, J.D. & Van Buskirk, J. 2012. Influence of experimental venue on phenotype: multiple traits reveal multiple answers. Funct. Ecol. 26: 513-521.
76. Wootton, R.J. 1984. A Functional Biology of Sticklebacks. University of California Press, Berkeley and Los Angeles, CA.