Evolution of stickleback feeding behaviour: Genetics of population divergence at different ontogenetic stages

Journal of Evolutionary Biology

Volumn 26, Issue 5, 2013, Pages 955-962

  Herczeg, G ^a,b   Ab Ghani, N I ^a   Merila J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Animal personality; Behavioural consistency; Nine spined stickleback; Ontogeny; Predation

Indexed keywords

DIVERGENCE; FEEDING; FEEDING BEHAVIOR; FISH; FITNESS; GENETIC VARIATION; GENETICS; HYBRID; MATERNAL EFFECT; ONTOGENY; POPULATION GENETICS; PREDATION; TELEOST;

ANIMAL; ARTICLE; CROSS BREEDING; EVOLUTION; FEEDING BEHAVIOR; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; PRINCIPAL COMPONENT ANALYSIS; SMEGMAMORPHA; STATISTICAL MODEL;

ANIMALS; BIOLOGICAL EVOLUTION; CROSSES, GENETIC; FEEDING BEHAVIOR; FEMALE; LINEAR MODELS; MALE; PRINCIPAL COMPONENT ANALYSIS; SMEGMAMORPHA;

ANIMALIA; PUNGITIUS; PUNGITIUS PUNGITIUS;

EID: 84876970174     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12103     Document Type: Article

References (57)

1. Ab Ghani, N.I., Herczeg, G. & Merilä, J. 2012. Body size divergence in nine-spined sticklebacks: disentangling additive genetic and maternal effects. Biol. J. Linn. Soc. 107: 521-528.
2. Ab Ghani, N.I., Herczeg, G., Leinonen, T. & Merilä, J. 2013. Evidence for genetic differentiation in timing of maturation among nine-spined stickleback populations. J. Evol. Biol. (in press), doi:10.1111/jeb.12085.
3. Åbjörnsson, K., Hansson, L.A. & Brönmark, C. 2004. Responses of prey from habitats with different predator regimes: local adaptation and heritability. Ecology 85: 1859-1866.
4. Abrams, P.A. & Rowe, L. 1996. The effects of predation on the age and size of maturity of prey. Evolution 50: 1052-1061.
5. Bǎnǎrescu, P.M. & Paepke, H.-J. 2001. The Freshwater Fishes of Europe, vol. 5/III. AULAVerlag, Wiebelsheim, Germany.
6. Bell, A.M. 2007. Future directions in behavioural syndrome research. Proc. Biol. Sci. 274: 755-761.
7. Dingemanse, N.J., Both, C., Drent, P.J., van Oers, K. & van Noordwijk, A.J. 2002. Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim. Behav 64: 929-938.
8. Dingemanse, N.J., Van der Plas, F., Wright, J., Réale, D., Schrama, M., Roff, D.A. et al. 2009. Individual experience and evolutionary history of predation affects expression of heritable variation in fish personality and morphology. Proc. Biol. Sci. 276: 1285-1293.
9. Dingemanse, N.J., Kazem, A.J.N., Réale, D. & Wright, J. 2010. Behavioural reaction norms: where animal personality meets individual plasticity. Trends Ecol. Evol. 25: 81-89.
10. Dingemanse, N.J., Barber, I., Wright, J. & Brommer, J.E. 2012. Quantitative genetics of behavioural reaction norms: genetic correlations between personality and behavioural plasticity vary across stickleback populations. J. Evol. Biol. 25: 485-496.
11. Drent, P.J., van Oers, K. & van Noordwijk, A.J. 2003. Realized heritability of personalities in the great tit (Parus major). Proc. R. Soc. Lond. B 270: 45-51.
12. Foster, S.A. 1999. The geography of behaviour: an evolutionary perspective. Trends Ecol. Evol. 14: 190-195.
13. Foster, S.A. & Endler, J.A. 1999. Geographic Variation in Behavior: Perspectives on Evolutionary Mechanisms. Oxford University Press, New York.
14. Garamszegi, L.Z., Markó, G. & Herczeg, G. 2012. A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol. Ecol. 26: 1213-1235.
15. Giles, N. & Huntingford, F.A. 1984. Predation risk and inter-population variation in anti-predator behaviour in the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 32: 264-275.
16. Gosling, S.D. 2001. From mice to men: what can we learn about personality from animal research. Psychol. Bull. 127: 45-86.
17. Green, B.S. 2008. Maternal effects in fish populations. Adv. Mar. Biol. 54: 1-105.
18. Herczeg, G. & Välimäki, K. 2011. Intraspecific variation in behaviour: effects of evolutionary history, ontogenetic experience and sex. J. Evol. Biol. 24: 2434-2444.
19. Herczeg, G., Gonda, A. & Merilä, J. 2009a. Evolution of gigantism in nine-spined sticklebacks. Evolution 63: 3190-3200.
20. Herczeg, G., Gonda, A. & Merilä, J. 2009b. Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J. Evol. Biol. 22: 544-552.
21. Herczeg, G., Gonda, A. & Merilä, J. 2010a. Rensch's rule inverted - female-driven gigantism in nine-spined stickleback (Pungitius pungitius). J. Anim. Ecol. 79: 581-588.
22. Herczeg, G., Turtiainen, M. & Merilä, J. 2010b. Morphological divergence of North-European nine-spined sticklebacks (Pungitius pungitius): signatures of parallel evolution. Biol. J. Linn. Soc. 101: 413-416.
23. Herczeg, G., Gonda, A., Kuparinen, A. & Merilä, J. 2012. Contrasting growth strategies of pond versus marine populations of nine-spined stickleback (Pungitius pungitius): a combined effect of predation and competition? Evol. Ecol. 26: 109-122.
24. Huntingford, F.A., Wright, P.J. & Tierney, J.F. 1994. Adaptive variation in antipredator behaviour in threespine stickleback. In: The Evolutionary Biology of Threespine Stickleback (M.A. Bell & S.A. Foster, eds), pp. 277-296. Oxford University Press, New York.
25. Kahilainen, K., Malinen, T., Tuomaala, A. & Lehtonen, H. 2004. Diel and seasonal habitat and food segregation of three sympatric Coregonus lavaretus forms in a subarctic lake. J. Fish Biol. 64: 418-434.
26. Kaplan, R.H. 1998. Maternal effects, developmental plasticity and life history evolution. In: Maternal Effects as Adaptations (T.A. Mousseau & C.W. Fox, eds), pp. 244-260. Oxford University Press, New York.
27. Lacey, E.P. 1998. What is an environmentally induced parental effect? In: Maternal Effects as Adaptations (T.A. Mousseau & C.W. Fox, eds), pp. 54-66. Oxford University Press, New York.
28. Laugen, A.T., Laurila, A. & Merilä, J. 2002. Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits. Biol. J. Linn. Soc. 76: 61-70.
29. Lima, S.L. & Dill, L.M. 1990. Behavioural decisions made under the risk of predation - a review and prospectus. Can. J. Zool. 68: 619-640.
30. Littell, R.C., Rendergast, J. & Natarajan, R. 2000. Modeling covariance structure in the analysis of repeated measures data. Stat. Med. 19: 1793-1819.
31. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. & Schabenberger, O. 2006. SAS for Mixed Models, 2nd edn. SAS Institute Inc., Cary, NC.
32. Lynch, M. & Walsh, B. 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
33. Magurran, A.E. & Seghers, B.H. 1991. Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118: 214-234.
34. Magurran, A.E. & Seghers, B.H. 1994. Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata. Behaviour 128: 121-134.
35. Mathis, A., Chivers, D.P. & Smith, R.J.F. 1993. Population differences in responses of fathead minnows (Pimephales promelas) to visual and chemical stimuli from predators. Ethology 93: 31-40.
36. Mousseau, T.A. & Fox, C.W. 1998. Maternal Effects as Adaptations. Oxford University Press, New York.
37. van Oers, K., Drent, P.J., de Jong, G. & van Noordwijk, A.J. 2004. Additive and nonadditive genetic variation in avian personality traits. Heredity 93: 496-503.
38. Östlund-Nilsson, S., Mayer, I. & Huntingford, F.A. 2007. Biology of the Three-spined Stickleback. CRC Press, Boca Raton, FL.
39. Réale, D., Reader, S.M., Sol, D., McDougall, P.T. & Dingemanse, N.J. 2007. Integrating animal temperament within ecology and evolution. Biol. Rev. 82: 291-318.
40. Riechert, S.E. & Hedrick, A.V. 1990. Levels of predation and genetically based antipredator behaviour in the spider, Agelenopsis aperta. Anim. Behav. 40: 679-687.
41. Rodel, H.G. & Monclus, R. 2011. Long-term consequences of early development on personality traits: a study in European rabbits. Behav. Ecol. 22: 1123-1130.
42. Roff, D.A. 1992. The Evolution of Life Histories. Chapman & Hall, New York.
43. Rossiter, M. 1998. The role of environmental variation in parental effects expression. In: Maternal Effects as Adaptations (T.A. Mousseau & C.W. Fox, eds), pp. 112-134. Oxford University Press, New York.
44. Shikano, T., Shimada, Y., Herczeg, G. & Merilä, J. 2010. History vs. habitat type: explaining the genetic structure of European nine-spined stickleback (Pungitius pungitius) populations. Mol. Ecol. 19: 1147-1161.
45. Shimada, Y., Shikano, T., Kuparinen, A., Gonda, A., Leinonen, T. & Merilä, J. 2011. Quantitative genetics of body size and timing of maturation in two-nine-spined stickleback (Pungitius pungitius) populations. PLoS ONE 6: e28859.
46. Sih, A. & Bell, A.M. 2008. Insights from behavioral syndromes for behavioral ecology. Adv. Study Behav. 38: 277-281.
47. Sih, A., Bell, A.M. & Johnson, J.C. 2004a. Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19: 372-378.
48. Sih, A., Bell, A.M., Johnson, J.C. & Ziemba, R.E. 2004b. Behavioral syndromes: an integrative overview. Q. Rev. Biol. 79: 241-277.
49. Smith, B.R. & Blumstein, D.T. 2008. Fitness consequences of personality: a meta-analysis. Behav. Ecol. 19: 448-455.
50. Stearns, S.C. 1992. The Evolution of Life Histories. Oxford University Press, New York.
51. Storfer, A. & Sih, A. 1998. Gene flow and ineffective antipredatory behavior in a stream-breeding salamander. Evolution 52: 558-565.
52. Trillmich, F. & Hudson, R. 2011. The emergence of personality of animals: the need for a developmental approach. Dev. Psychobiol. 53: 505-509.
53. Urban, M.C. 2008. Salamander evolution across a latitudinal cline in gape-limited predation risk. Oikos 117: 1037-1049.
54. Välimäki, K. & Herczeg, G. 2012. Ontogenetic and evolutionary effects of predation and competition on nine-spined stickleback (Pungitius pungitius) body size. J. Anim. Ecol. 81: 859-867.
55. Werner, E.E. & Gilliam, J.F. 1984. The ontogenetic niche and species interactions in size structured populations. Annu. Rev. Ecol. Syst. 15: 393-425.
56. Wilson, D.S. 1998. Adaptive individual differences within single populations. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353: 199-205.
57. Wright, S. 1978. Variability within and among populations. In: Evolution and the genetics of populations (S. Wright, ed.), pp. 336-347. University Chicago Press, Chicago, IL.