Evolution of ovipositor length in Drosophila suzukii is driven by enhanced cell size expansion and anisotropic tissue reorganization

Abstract

Morphological diversity is dominated by variation in body proportion. Yet the cellular processes underlying differential growth of morphological traits between species remain largely unknown. Here we compare the ovipositors of two closely related species, Drosophila melanogaster and D. suzukii. D. suzukii has switched its egg-laying niche from rotting to ripe fruit. Along with this shift, the D. suzukii ovipositor has undergone a significant change in size and shape. Using an allometric approach we find that, while adult ovipositor width has hardly changed between the species, D. suzukii ovipositor length is almost double that of D. melanogaster. We show that this size difference mostly arises during a 6-hour time window in the middle of pupal development. We observe that the developing ovipositors of the two species comprise an almost identical number of cells, with a very similar profile of cell shapes and orientations. After cell division stops, we find that the ovipositor area continues to grow through the isotropic expansion of cell apical area. Remarkably, at one point, the rate of cell apical area expansion is more than 4 times faster in D. suzukii than in D. melanogaster. In addition, we find that an anisotropic cellular reorganization of the developing ovipositor results in a net elongation of the tissue, despite the isotropic expansion of cell size, and is enhanced in D. suzukii. Therefore, the quantitative fine-tuning of shared, morphogenetic processes -the rate of cell size expansion and the cellular rearrangements-can drive macroscopic evolutionary changes in organ size and shape.