Evolution of Ovipositor Length in Drosophila suzukii Is Driven by Enhanced Cell Size Expansion and Anisotropic Tissue Reorganization

Abstract

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.

An Atlas of Transcription Factors Expressed in Male Pupal Terminalia ofDrosophila melanogaster

“…However, we are ultimately interested in the connections between transcription factors and the effectors that dictate cell behavior (Smith et al 2018). Recent work has implicated a variety of cellular mechanisms in the formation of genital structures, including changes in cell size and cell intercalations in the developing ovipositor (Green et al 2019) and the influence of the apical extracellular matrix in the developing posterior lobe (Smith et al 2019). In the future, we hope to characterize the functional roles of transcription factors in both cellular dynamics and adult morphology, and elucidate how the expression and function of these genes are tuned to generate new or different structures over evolutionary time.…”

Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii

“…The adaptation of D. suzukii to ripe fruits has been accompanied by the evolution of a large serrated ovipositor, which penetrates the surface of ripe fruit and deposits an egg ( Atallah et al, 2014 ; Green et al, 2019 ). A recent study showed that changes in the olfactory and mechanosensory systems contribute to the adaptation of D. suzukii to its new niche ( Karageorgi et al, 2017 ).…”

Susceptibility of Drosophila suzukii larvae to the combined administration of the entomopathogens Bacillus thuringiensis and Steinernema carpocapsae

“…D. suzukii is one of the most important emerging pests of soft-skinned fruit such as raspberries, blackberries, strawberries, blueberries, cherries, grapes, and peaches 20 . The adult female lays her eggs into the fruit through the ovipositor by perforating the skin, and the larvae develop by feeding on the fruit flesh 21 .…”