Human-induced evolution caused by unnatural selection through harvest of wild animals

Abstract

Human harvest of phenotypically desirable animals from wild populations imposes selection that can reduce the frequencies of those desirable phenotypes. Hunting and fishing contrast with agricultural and aquacultural practices in which the most desirable animals are typically bred with the specific goal of increasing the frequency of desirable phenotypes. We consider the potential effects of harvest on the genetics and sustainability of wild populations. We also consider how harvesting could affect the mating system and thereby modify sexual selection in a way that might affect recruitment. Determining whether phenotypic changes in harvested populations are due to evolution, rather than phenotypic plasticity or environmental variation, has been problematic. Nevertheless, it is likely that some undesirable changes observed over time in exploited populations (e.g., reduced body size, earlier sexual maturity, reduced antler size, etc.) are due to selection against desirable phenotypes-a process we call "unnatural" selection. Evolution brought about by human harvest might greatly increase the time required for over-harvested populations to recover once harvest is curtailed because harvesting often creates strong selection differentials, whereas curtailing harvest will often result in less intense selection in the opposing direction. We strongly encourage those responsible for managing harvested wild populations to take into account possible selective effects of harvest management and to implement monitoring programs to detect exploitation-induced selection before it seriously impacts viability.

Fig. 1.

Human harvest can have a variety of direct and indirect genetic effects on populations, and it has the potential to affect the future yield and viability of exploited populations.

Fig. 2.

Reduction in frequency of the silver morph of the fox in eastern Canada resulting from the preferential harvest by hunters of the more valuable silver morph (69, 70). The points represent data presented by Elton (69). The lines represent the expected change in frequencies of the 3 phenotypes via selection at a single locus assuming that the silver fox morph has a 3% survival disadvantage per generation relative to the red and cross morphs. The initial frequency of the R allele was 0.3 and the mean generation interval was 2 years (70).

Fig. 3.

Potential consequences of natural, sexual, and fishing-induced selection in exploited sockeye salmon. (A) Typical morphological phenotypes for adult male and female sockeye salmon. BL, body length; BD, body depth. (B) Hypothetical relative fitness, as measured by reproductive success, among breeders that vary in body length and body depth. (Top) Sexual selection favors individual breeders with higher BL and BD phenotypes. (Middle) Natural selection favors individual breeders with intermediate BL and larger BD phenotypes. (Bottom) Individuals with larger values of BL and especially BD are more vulnerable to fishing mortality. (C) Potential evolution of the genetic covariance matrix (G) for the bivariate body length (BL)–body depth (BD) phenotype under combined natural, sexual, and fishing-induced selection. The box represents the bivariate adaptive landscape (in the sense of ref. 89). G is represented by the oval. Under natural and sexual selection on BL and BD in the absence of fishing, G will tend to move toward the “global” optimum bivariate phenotype A. When the population is subjected to substantial selective fishing mortality that targets potential breeders of larger BL and BD, G will tend to move toward the “local” alternative optimum bivariate phenotype A*. Natural and sexual selection impose a selection gradient on the bivariate phenotype, which tends to oppose the selection gradient imposed by selective fishing. The result is a suboptimal phenotype in the wild breeding population that might deviate substantially from A. Note the difference in elevation and steepness of fitness for the 2 alternative fitness optima.