Evolutionary expansion of apical extracellular matrix is required for the elongation of cells in a novel structure.

Sarah Jacquelyn Smith,Mark Rebeiz,Lance A Davidson

doi:10.7554/elife.55965

Abstract

One of the fundamental gaps in our knowledge of how novel anatomical structures evolve is understanding the origins of the morphogenetic processes that form these features. Here, we traced the cellular development of a recently evolved morphological novelty, the posterior lobe of D. melanogaster. We found that this genital outgrowth forms through extreme increases in epithelial cell height. By examining the apical extracellular matrix (aECM), we also uncovered a vast matrix associated with the developing genitalia of lobed and non-lobed species. Expression of the aECM protein Dumpy is spatially expanded in lobe-forming species, connecting the posterior lobe to the ancestrally derived aECM network. Further analysis demonstrated that Dumpy attachments are necessary for cell height increases during posterior lobe development. We propose that the aECM presents a rich reservoir for generating morphological novelty and highlights a yet unseen role for aECM in regulating extreme cell height.

Highlights

Biologists have long been mesmerized by the appearance of morphological novelties, new structures that appear to lack homologs in other species groups (Moczek, 2008; Wagner and Lynch, 2010)
The posterior lobe grows from the lateral plate epithelium
We found that fluorescein conjugated Vicia villosa lectin (VVA), which labels N-acetylgalactosamine (Tian and Ten Hagen, 2007), roughly mirrors the complex three-dimensional shape of the Dumpy apical extracellular matrix (ECM) (aECM) network covering the center of the genitalia and strongly associates with the posterior lobe (Figure 5C, Figure 5—figure supplement 2)

Summary

Introduction

Biologists have long been mesmerized by the appearance of morphological novelties, new structures that appear to lack homologs in other species groups (Moczek, 2008; Wagner and Lynch, 2010). Understanding the morphogenetic basis of a novelty is critical to identifying the most important aspects of the gene regulatory networks that contributed to its origin. Developmental Biology Evolutionary Biology contribute to the development of conserved structures, such as eggshell breathing tubes (Osterfield et al, 2015) and the migration of sex comb precursors (Atallah et al, 2009; Tanaka et al, 2009) in Drosophila Overall, these studies have illustrated how evolutionary comparative approaches can reveal morphogenetic processes critical to the sculpting of anatomical structures. Our work demonstrates how the formation of a morphological novelty is associated with changes in the aECM, which integrates posterior lobe cells into a larger pre-existing aECM network necessary for its formation

Results

Discussion

Materials and methods

Funding Funder National Institutes of Health