The hourglass and the early conservation models - co-existing evolutionary patterns in vertebrate development

TL;DR

This study compares early conservation and hourglass models of vertebrate development, revealing that different molecular features follow distinct evolutionary constraints, supporting both models simultaneously.

Contribution

The paper introduces a modular gene expression analysis approach, clarifying how different genomic features conform to either the hourglass or early conservation models.

Findings

Hourglass pattern observed at regulatory region level

Early development genes show less duplication and birth

Late development genes exhibit least conservation

Abstract

Developmental constraints have been postulated to limit the space of feasible phenotypes and thus shape animal evolution. These constraints have been suggested to be the strongest during either early or mid-embryogenesis, which corresponds to the early conservation model or the hourglass model, respectively. Conflicting results have been reported, but in recent studies of animal transcriptomes the hourglass model has been favored. Studies usually report descriptive statistics calculated for all genes over all developmental time points. This introduces dependencies between the sets of compared genes, and may lead to biased results. Here we overcome this problem using an alternative modular analysis. We used the Iterative Signature Algorithm to identify distinct modules of genes co-expressed specifically in consecutive stages of zebrafish development. We then performed a detailed comparison of several gene properties between modules, allowing for a less biased and more powerful analysis. Notably, our analysis corroborated the hourglass pattern only at the regulatory level, with sequences of regulatory regions being most conserved for genes expressed in mid-development, but not at the level of gene sequence, age or expression, in contrast to some previous studies. The early conservation model was supported with gene duplication and birth that were the most rare for genes expressed in early development. Finally, for all gene properties we observed the least conservation for genes expressed in late development or adult, consistent with both models. Overall, with the modular approach, we showed that different levels of molecular evolution follow different patterns of developmental constraints. Thus both models are valid, but with respect to different genomic features.