Reproductive Capacity Evolves in Response to Ecology through Common Changes in Cell Number in Hawaiian Drosophila

Lifetime reproductive capacity is a critical fitness component. In insects, female reproductive capacity is largely determined by the number of ovarioles, the egg-producing subunits of the ovary [e.g., 1]. Recent work has provided insights into ovariole number regulation in Drosophila melanogaster. However, whether mechanisms discovered under laboratory conditions explain evolutionary variation in natural populations is an outstanding question. We investigated potential effects of ecology on the developmental processes underlying ovariole number evolution among Hawaiian Drosophila, a large adaptive radiation wherein the highest and lowest ovariole numbers of the family have evolved within 25 million years. Previous studies proposed that ovariole number correlated with oviposition substrate [2-4] but sampled largely one clade of these flies and were limited by a provisional phylogeny and the available comparative methods. We test this hypothesis by applying phylogenetic modeling to an expanded sampling of ovariole numbers and substrate types and show support for these predictions across all major groups of Hawaiian Drosophila, wherein ovariole number variation is best explained by adaptation to specific substrates. Furthermore, we show that oviposition substrate evolution is linked to changes in the allometric relationship between body size and ovariole number. Finally, we provide evidence that the major changes in ovarian cell number that regulate D. melanogaster ovariole number also regulate ovariole number in Hawaiian drosophilids. Thus, we provide evidence that this remarkable adaptive radiation is linked to evolutionary changes in a key reproductive trait regulated at least partly by variation in the same developmental parameters that operate in the model species D. melanogaster.