Reorganizations in the apical extracellular matrix underlie morphological diversification in Drosophila genital structures
Authors: Ben Vincent; Lance Davidson; Mark Rebeiz
Affiliation: University of Pittsburgh
Keywords: l. evo-devo; q. epithelial sheets
Identifying the genetic changes that cause morphological differences between species is a major goal of evolutionary and developmental biology. While many groups have found success by investigating differences in pigmentation or the regressive loss of entire structures, we know less about the genes and pathways involved in the diversification of three-dimensional body parts. The posterior lobe in the Drosophila melanogaster clade is an ideal system to investigate morphological evolution – this genital structure exhibits staggering diversity among the Drosophila melanogaster subgroup, including the sister species Drosophila mauritiana and Drosophila simulans, and we can track its development by dissecting and staining pupal terminalia. Previous work has shown that the posterior lobe develops in Drosophila melanogaster as a result of cell elongation – individual cells span all the way from the base of the lobe to its tip – and posterior lobe morphology is controlled in part by the apical extracellular matrix (aECM) component Dumpy. We therefore tested whether the aECM also underlies posterior lobe diversification between Drosophila simulans and Drosophila mauritiana. By labeling the aECM with fluorescent lectins, we have found that it forms attachments to the posterior lobe and other genital structures during early development, and these attachments are more extensive in Drosophila simulans, the species with the larger lobe. We also found that the lobe-specific gene expression pattern for dumpy is expanded in Drosophila simulans, which suggests that these morphological changes are controlled at the level of transcriptional regulation. Finally, we have built cellular simulations of posterior lobe development to investigate the role of the aECM in cellular elongation – whether it exerts an active contractile force on these cells or simply functions as a passive scaffold – and whether that role has changed between species. Our results suggest that morphological diversity may be generated by alterations in extracellular matrix organization during development, and that we can find the genes controlling this process within quantitative trait loci associated with genital evolution.