Density-dependent selection mediates harvest-induced evolution

Harvesting has been demonstrated to cause rapid, yield-decreasing trait change towards slower somatic growth and earlier maturation in wild populations. These changes are largely considered to result from direct, density-independent harvest selection on traits. Here, we show that exact same trait changes may also indirectly result from a harvest-induced relaxation of density-dependent ( K ) natural selection for faster growth and delayed maturation. We exposed 12 pond populations of medaka fish ( Oryzias latipes ) to contrasted size-selective harvesting during 5 years, and show that harvesting effectively changed juvenile natural mortality from density-dependent to density- in dependent. We then laboratory-reared medaka progeny under contrasted food levels mimicking the environmental effects of a harvest-induced density gradient. Interaction between past harvest regime and present food environment on progeny traits revealed that harvest-induced trait changes in medaka resulted from selection in a low-food environment only, i.e., were driven by relaxed K -selection only, not by direct harvest selection. Feeding trials further demonstrated that trait changes were associated with reorganizations in rates of food acquisition, assimilation and allocation that were contingent upon the food environments. This is the first study to demonstrate that harvesting can induce undesirable distortions of natural selection that impair productivity traits. We conclude that sustaining harvesting yields over extended time scales requires a preservation of high population densities. Significance statement Fisheries management often opposes a density-dependent approach which prioritize the preservation of high population densities, and an evolutionary approach which consider that alleviating change towards smaller body sizes is paramount to the sustainability of harvesting. The evolutionary approach consider harvest-induced body downsizing to be density-independent, i.e., to result only from direct harvest selection against large-bodied individuals. Here, we show instead that harvest-induced body downsizing may be density-dependent because, by decreasing population density, fishing relaxes natural, density-dependent selection for large-bodied individuals. Therefore, preserving population numbers and alleviating body downsizing in harvested populations are not independent lines of management, but are in fact two necessary and complementary routes to reaching the same management objectives.