Strong evidence for positive and negative correlational selection revealed by recreating ancestral variation.

The study of adaptation helps explain biodiversity and predict future evolution. Yet the process of adaptation can be difficult to observe due to limited phenotypic variation in contemporary populations. Furthermore, the scarcity of male fitness estimates has made it difficult to both understand adaptation and evaluate sexual conflict hypotheses. We addressed both issues in our study of two anther position traits in wild radish (Raphanus raphanistrum): anther exsertion (long filament - corolla tube lengths) and anther separation (long - short filament lengths). These traits affect pollination efficiency and are particularly interesting due to the unusually high correlations among their component traits. We measured selection through male and female fitness on wild radish plants from populations artificially selected to recreate ancestral variation in each anther trait. We found little evidence for conflicts between male and female function. We found strong evidence for stabilizing selection on anther exsertion and disruptive selection on anther separation, indicating positive and negative correlational selection on the component traits. Intermediate levels of exsertion are likely an adaptation to best contact small bees. The function of anther separation is less clear, but future studies might investigate pollen placement on pollinators and compare species possessing multiple stamen types.

Tests of adaptation: functional studies of pollen removal and estimates of natural selection on anther position in wild radish.

BACKGROUND: There are a number of difficulties associated with the study of adaptation. One is a lack of variation in the trait, which is common in adaptations because past selection has removed unfit variants. This lack of variation makes it difficult to determine the relationship between trait variation and fitness. Another difficulty is proving causation in this trait-fitness relationship, because a correlated trait might be the actual adaptation. These difficulties can be ameliorated at least partially by combining studies of natural variation with studies of experimentally manipulated traits and traits whose variance has been augmented by artificial selection. SCOPE: We review here a number of our studies on the adaptive value of two aspects of anther position in wild radish (Raphanus raphanistrum, Brassicaceae): anther exsertion, i.e. the degree to which anthers protrude from the mouth of the corolla tube, and anther height dimorphism, i.e. the difference in lengths of the filaments between the two short and four long stamens. We have used both functional analyses, in which the response variable is pollen removal, and measurements of selection, in which the response variable is lifetime male fitness estimated by molecular genetic paternity analyses. In these studies we use both the natural variation in populations as well as manipulated variation, the latter through both stamen removal and artificial selection, to re-create the ancestral trait conditions. CONCLUSIONS: Our work provides convincing evidence that intermediate anther exsertion values are adaptive, and that this is probably an adaptation to a subset of the pollinator fauna, small bees. The picture for anther height dimorphism is much less clear, as the weight of current evidence suggests that current values of this trait might actually be maladaptive; however, if this is true it is difficult to understand how the dimorphism is maintained across the family Brassicaceae.