A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila

Charless C Fowlkes,Mark D Biggin,Cris L Luengo Hendriks,David W Knowles,Soile V E Keränen,Meghan D Bragdon,Lisa Simirenko,Michael B Eisen,Miriah Meyer,Angela H Depace,Kelly B Eckenrode,Clara Henriquez,Zeba Wunderlich,Artyom Kopp

doi:10.1371/journal.pgen.1002346

Abstract

Differences in the level, timing, or location of gene expression can contribute to alternative phenotypes at the molecular and organismal level. Understanding the origins of expression differences is complicated by the fact that organismal morphology and gene regulatory networks could potentially vary even between closely related species. To assess the scope of such changes, we used high-resolution imaging methods to measure mRNA expression in blastoderm embryos of Drosophila yakuba and Drosophila pseudoobscura and assembled these data into cellular resolution atlases, where expression levels for 13 genes in the segmentation network are averaged into species-specific, cellular resolution morphological frameworks. We demonstrate that the blastoderm embryos of these species differ in their morphology in terms of size, shape, and number of nuclei. We present an approach to compare cellular gene expression patterns between species, while accounting for varying embryo morphology, and apply it to our data and an equivalent dataset for Drosophila melanogaster. Our analysis reveals that all individual genes differ quantitatively in their spatio-temporal expression patterns between these species, primarily in terms of their relative position and dynamics. Despite many small quantitative differences, cellular gene expression profiles for the whole set of genes examined are largely similar. This suggests that cell types at this stage of development are conserved, though they can differ in their relative position by up to 3–4 cell widths and in their relative proportion between species by as much as 5-fold. Quantitative differences in the dynamics and relative level of a subset of genes between corresponding cell types may reflect altered regulatory functions between species. Our results emphasize that transcriptional networks can diverge over short evolutionary timescales and that even small changes can lead to distinct output in terms of the placement and number of equivalent cells.

Highlights

Transcriptional programs specify and elaborate cell identity during animal development, as a single cell gives rise to the hundreds of cell types that comprise the adult animal
Gene expression during animal development is highly dynamic in space and time and occurs in the context of a gene regulatory network; the expression of any given gene is dependent on the spatiotemporal expression patterns of many others
We take the first step by comparing gene expression patterns at high spatial and temporal resolution between embryos of three species of fruit flies

Summary

Introduction

Transcriptional programs specify and elaborate cell identity during animal development, as a single cell gives rise to the hundreds of cell types that comprise the adult animal. Variation in the timing, spatial location, and level of transcription is thought to be a major source of molecular variation for morphological changes during evolution [1,2,3]. Gene expression during animal development is highly dynamic in space and time and occurs in the context of a gene regulatory network; the expression of any given gene is dependent on the spatiotemporal expression patterns of many others. This poses a fundamental problem for comparing gene expression patterns between species.

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Results

Discussion

Conclusion