The response of correlated traits following cessation of fishery-induced selection

Abstract

The application of evolutionary principles to the management of fisheries has gained considerable attention recently. Harvesting of fish may apply directional or disruptive selection to key life-history traits, and evidence for fishery-induced evolution is growing. The traits that are directly selected upon are often correlated (genetically or phenotypically) with a suite of interrelated physiological, behavioral, and morphological characters. A question that has received comparatively little attention is whether or not, after cessation of fishery-induced selection, these correlated traits revert back to previous states. Here, we empirically examine this question. In experiments with the Atlantic silverside, Menidia menidia, we applied size-selective culling for five generations and then maintained the lines a further five generations under random harvesting. We found that some traits do return to preharvesting levels (e.g., larval viability), some partially recover (e.g., egg volume, size-at-hatch), and others show no sign of change (e.g., food consumption rate, vertebral number). Such correlations among characters could, in theory, greatly accelerate or decelerate the recovery of fish populations. These results may explain why some fish stocks fail to recover after fishing pressure is relaxed.

Literature cited Allendorf, F. W., and J. J. Hard. 2009. Human-induced evolution caused by unnatural selection through harvest of wild animals. Proceedings of the National Academy of Sciences of the United States of America106:9987–9994. Ando, D., S. Mano, N. Koide, and M. Nakajima. 2008. Estimation of heritability and genetic correlation of number of abdominal and caudal vertebrae in masu salmon. Fishery Science74:293–298. Biro, P. A., M. V. Abrahams, J. R. Post, and E. A. Parkinson. 2004. Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proceedings. Biological Sciences271:2233–2237. Bochdansky, A. B., P. Grønkjær, P. Pepin, and W. C. Leggett. 2008. Food limitation in larval fish: ontogenetic variation in feeding scope and its potential effect on survival. Marine Ecology Progress Series367:239–248. Chiba, S., S. A. Arnott, and D. O. Conover. 2007. Coevolution of foraging behavior with intrinsic growth rate: risk-taking in naturally and artificially selected growth genotypes of Menidia menidia. Oecologia154:237–246. Conover, D. O., and S. B. Munch. 2002. Sustaining fisheries yields over evolutionary time scales. Science297:94–96. Conover, D. O., S. A. Arnott, M. R. Walsh, and S. B. Munch. 2005. Darwinian fishery science: lessons from the Atlantic silverside (Menidia menidia). Canadian Journal of Fisheries and Aquatic Sciences62:730–737. Conover, D. O., S. B. Munch, and S. A. Arnott. 2009. Reversal of evolutionary downsizing caused by selective harvest of large fish. Proceedings. Biological Sciences276:2015–2020. Edeline, E., S. M. Carlson, L. C. Stige, I. J. Winfield, J. M. Fletcher, J. B. James, T. O. Haugen et al.2007. Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection. Proceedings of the National Academy of Sciences of the United States of America104:15799–15804. Estes, S., and H. Teotónio. 2009. The experimental study of reverse evolution. In T. Garland, and M. R. Rose, eds. Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, pp. 135–171. University of California Press, Berkeley, CA. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to Quantitative Genetics, 4th edn. Pearson, Essex. Hard, J. J.2004. Evolution of Chinook salmon life history under size-selective harvest. In A. P. Hendry, and S. C. Stearns, eds. Evolution Illuminated: Salmon and their Relatives, pp. 315–337. Oxford University Press, New York. Hard, J. J., M. R. Gross, M. Heino, R. Hilborn, R. G. Kope, R. Law, and J. D. Reynolds. 2008. Evolutionary consequences of fishing and their implications for salmon. Evolutionary Applications1:388–408. Henryon, M., A. Jokumsen, P. Berg, I. Lund, P. B. Pedersen, N. J. Olesen, and W. J. Slierendrecht. 2002. Genetic variation for growth rate, feed conversion efficiency, and disease resistance exists within a farmed population of rainbow trout. Aquaculture209:59–76. Houde, E. D.1989. Subtleties and episodes in the early life of fishes. Journal of Fish Biology35(Suppl. A):29–38. Hutchings, J. A.2005. Life history consequences of overexploitation to population recovery in Northwest Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences62:824–832. Hutchings, J. A., and D. J. Fraser. 2008. The nature of fisheries- and farming-induced evolution. Molecular Ecology17:294–313. Jeffery, W. R.2001. Cavefish as a model system in evolutionary developmental biology. Developmental Biology231:1–12. Jørgensen, C., K. Enberg, E. S. Dunlop, R. Arlinghaus, D. S. Boukal, K. Brander, B. Ernande et al.2007. Managing evolving fish stocks. Science318:1247–1248. Kause, A., D. Tobin, D. F. Houlihan, S. A. M. Martin, E. A. Mäntysaari, O. Ritola, and K. Ruohonen. 2006. Feed efficiency of rainbow trout can be improved through selection: different genetic potential on alternative diets. Journal of Animal Science84:807–817. Law, R.2000. Fishing, selection, and phenotypic evolution. ICES Journal of Marine Science57:659–668. Law, R.2007. Fisheries-induced evolution: present status and future directions. Marine Ecology Progress Series335:271–277. Law, R., and C. A. Rowell. 1993. Cohort-structured populations, selection responses, and exploitation of the North Sea cod. In T. K. Stokes, J. M. McGlade, and R. Law, eds. The Exploitation of Evolving Resources, pp. 155–173. Springer-Verlag, Berlin. Mertz, G., and R. A. Myers. 1998. A simplified formulation for fish production. Canadian Journal of Fisheries and Aquatic Sciences55:478–484. Munch, S. B., M. R. Walsh, and D. O. Conover. 2005. Harvest selection, genetic correlations, and evolutionary changes in recruitment: one less thing to worry about?Canadian Journal of Fisheries and Aquatic Sciences62:802–810. Pepin, P., and R. A. Myers. 1991. Significance of egg and larval size to recruitment variability of temperate marine fish. Canadian Journal of Fisheries and Aquatic Sciences48:1820–1828. Su, G.-S., L.-E. Liljedahl, and G. A. E. Gall. 2002. Genetic correlations between body weight at different ages and with reproductive traits in rainbow trout. Aquaculture213:85–94. Swain, D. P.2011. Life-history evolution and elevated natural mortality in a population of Atlantic cod (Gadus morhua). Evolutionary Applications4:18–29. Teotónio, H., M. Matos, and M. R. Rose. 2002. Reverse evolution of fitness in Drosophila melanogaster. Journal of Evolutionary Biology15:608–617. Thrower, F. P., J. J. Hard, and J. E. Joyce. 2004. Genetic architecture of growth and early life-history transitions in anadromous and derived freshwater populations of steelhead. Journal of Fish Biology65(Suppl. A):286–307. Walker, S. P. W., C. A. Ryen, and M. I. McCormick. 2007. Rapid larval growth predisposes sex change and sexual size dimorphism in a protogynous hermaphrodite, Parapercis snyderi Jordan & Starks 1905. Journal of Fish Biology71:1347–1357. Walsh, M. R., S. B. Munch, S. Chiba, and D. O. Conover. 2006. Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecology Letters9:142–148.