Evolution of ovipositor length inDrosophila suzukiiis 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.

Limited thermal plasticity and geographical divergence in the ovipositor of Drosophila suzukii

“…This should be tested experimentally by evaluating the relative performance on a variety of substrates, of the cold-and hot-generated ovipositors. Other factors like the existence of alternative selective pressures imposed on the ovipositor morphology such as sexual coevolution [49] and pleiotropic genetic effects during the ovipositor development [56] might limit such morphological adaptation.…”

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

“…2) as anticipated from their uniquely enlarged ovipositor plates [8,20,21]. D. suzukii and D. subpulchrella have shifted their oviposition sites from rotting to ripening fruits, and the shift has promoted the evolution in various traits including the ovipositor morphology as well as the mechanosensory and chemosensory perception [8,20,21,[26][27][28][29][30]. The ovipositor is an essential device for the flies to deposit eggs to the appropriate substrate; therefore, the changes in ovipositor shape should accompany an adjustment of oviprovector morphology to support egg-laying effectively.…”

“…During the ovipositor morphogenesis at the pupal stage, Green et al [21] have analyzed the size and number of the external cell layer of the ovipositor plate. They concluded that an accelerated cell size expansion instead of an enhanced cell division causes the enlargement of the ovipositors in D.…”

“…Motivated by the presence of Svb in the cells on the inner surface of the developing ovipositor in D. melanogaster, we next asked 1) if the known genes in the network are expressed in the developing female genitalia of D. suzukii and D. subpulchrella, and 2) if any of the trichome-related genes contribute to the morphological differences of the oviprovector scales between these species. The ovipositor morphogenesis takes place at early pupal stages in Drosophila at around 30-54 h APF [21].…”

Gene expression during genital morphogenesis in the ground beetle Carabus maiyasanus

“…Although many studies have investigated selection factors influencing genital morphology, the genetic and developmental backgrounds for diverse genital morphologies remain largely unknown. Previous studies on genes involved in genital morphogenesis and interspecific differences in genital morphology have dealt with mainly Drosophila flies (Sánchez & Guerrero, ; Coutelis et al ., ; Chatterjee et al ., ; Masly et al ., ; Tanaka et al ., ; Green et al ., ), and a few other insects such as the milkweed bugs Oncopeltus fasciatus , the red flour beetle Tribolium castaneum and Onthophagus dung beetles (Aspiras et al ., ; Macagno & Moczek, ). To understand the evolutionary process of species‐specific genital morphology, which is related to species diversity in insects, more studies on the genetic backgrounds and developmental processes of genital morphology in various insects are necessary.…”