Temporal variation in divergent selection on spine number in threespine stickleback.

Short-term temporal cycles in ecological pressures, such as shifts in predation regime, are widespread in nature yet estimates of temporal variation in the direction and intensity of natural selection are few. Previous work on threespine stickleback (Gasterosteus aculeatus) has revealed that dorsal and pelvic spines are a defense against gape-limited predators but may be detrimental against grappling insect predators. In this study, we examined a 15-year database from an endemic population of threespine stickleback to look for evidence of temporal shifts in exposure to these divergent predation regimes and correlated shifts in selection on spine number. For juveniles, we detected selection for increased spine number during winter when gape-limited avian piscivores were most common but selection for decreased spine number during summer when odonate predation was more common. For subadults and adults, which are taken primarily by avian piscivores, we predicted selection should generally be for increased spine number in all seasons. Among 59 comparisons, four selection differentials were significant (Bonferroni corrected) and in the predicted direction. However, there was also substantial variability in remaining differentials, including two examples with strong selection for spine reduction. These reversals were associated with increased tendency of the fish to shift to a benthic niche, as determined from examination of stomach contents. These dietary data suggest that increased encounter rates with odonate predation select for spine reduction. Strong selection on spine number was followed by changes in mean spine number during subsequent years and a standard quantitative genetic formula revealed that spine number has a heritable component. Our results provide evidence of rapid morphological responses to selection from predators and suggest that temporal variation in selection may help maintain variation within populations. Furthermore, our findings indicate that variable selection can be predicted if the agents of selection are known.