Summary Morphological diversity is dominated by variation in body proportion [ 1 ], which can be described with scaling relationships and mathematical equations, following the pioneering work of D’Arcy Thompson [ 2 ] and Julian Huxley [ 3 ]. Yet, the cellular processes underlying divergence in size and shape of morphological traits between species remain largely unknown [ 4 , 5 , 6 , 7 , 8 ]. Here, we compare the ovipositors of two related species, Drosophila melanogaster and D. suzukii . D. suzukii has switched its egg-laying niche from rotting to ripe fruit [ 9 ]. Along with this shift, the D. suzukii ovipositor has undergone a significant change in size and shape [ 10 ]. 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 difference mostly arises in a 6-h time window during pupal development. We observe that the developing ovipositors of the two species comprise an almost identical number of cells, with a similar profile of cell shapes and orientations. After cell division stops, we find that the ovipositor area continues to grow in both species through the isotropic expansion of cell apical area and the anisotropic cellular reorganization of the tissue. Remarkably, we find that the lengthening of the D. suzukii ovipositor compared to that of D. melanogaster results from the combination of the accelerated expansion of apical cell size and the enhanced anisotropic rearrangement of cells in the tissue. Therefore, the quantitative fine-tuning of morphogenetic processes can drive evolutionary changes in organ size and shape.

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.