Swift laboratory thermal evolution of wing shape (but not size) in Drosophila subobscura and its relationship with chromosomal inversion polymorphism

Abstract

Latitudinal clinal variation in wing size and shape has evolved in North American populations of Drosophila subobscura within about 20 years since colonization. While the size cline is consistent to that found in original European populations (and globally in other Drosophila species), different parts of the wing have evolved on the two continents. This clearly suggests that 'chance and necessity' are simultaneously playing their roles in the process of adaptation. We report here rapid and consistent thermal evolution of wing shape (but not size) that apparently is at odds with that suggestion. Three replicated populations of D. subobscura derived from an outbred stock at Puerto Montt (Chile) were kept at each of three temperatures (13, 18 and 22°C) for 1 year and have diverged for 27 generations at most. We used the methods of geometric morphometrics to study wing shape variation in both females and males from the thermal stocks, and rates of genetic divergence for wing shape were found to be as fast or even faster than those previously estimated for wing size on a continental scale. These shape changes did not follow a neat linear trend with temperature, and are associated with localized shifts of particular landmarks with some differences between sexes. Wing shape variables were found to differ in response to male genetic constitution for polymorphic chromosomal inversions, which strongly suggests that changes in gene arrangement frequencies as a response to temperature underlie the correlated changes in wing shape because of gene-inversion linkage disequilibria. In fact, we also suggest that the shape cline in North America likely predated the size cline and is consistent with the quite different evolutionary rates between inversion and size dines. These findings cast strong doubts on the supposed 'unpredictability' of the geographical dine for wing traits in D. subobscura North American colonizing populations.