Developmental system drift and flexibility in evolutionary trajectories

Abstract

SUMMARYThe comparative analysis of homologous characters is a staple of evolutionary developmental biology and often involves extrapolating from experimental data in model organisms to infer developmental events in non-model organisms. In order to determine the general importance of data obtained in model organisms, it is critical to know how often and to what degree similar phenotypes expressed in different taxa are formed by divergent developmental processes. Both comparative studies of distantly related species and genetic analysis of closely related species indicate that many characters known to be homologous between taxa have diverged in their morphogenetic or gene regulatory underpinnings. This process, which we call "developmental system drift" (DSD), is apparently ubiquitous and has significant implications for the flexibility of developmental evolution of both conserved and evolving characters. Current data on the population genetics and molecular mechanisms of DSD illustrate how the details of developmental processes are constantly changing within evolutionary lineages, indicating that developmental systems may possess a great deal of plasticity in their responses to natural selection.

The frailty of adaptive hypotheses for the origins of organismal complexity

“…One could even argue that the stringency of natural selection is reduced in complex organisms with behavioral and/or growth-form flexibilities that allow individuals to match their phenotypic capabilities to the local environment. Some of these shortcomings have recently attracted attention, and a scaffold for connecting evolutionary genetics, genomics, and developmental biology is slowly beginning to emerge (59)(60)(61)(62)(63)(64)(65)(66).…”

“…Thus, the new regulatory architecture emerges beneath a constant phenotype, without any bottleneck in fitness during the transitional phase of mixed genotypes. Such neutral transitions may help explain apparent cases of ''developmental system drift,'' whereby closely related species achieved similar morphological structures by substantially different mechanisms (59,63,(71)(72)(73)(74).…”

Distinct developmental mechanisms underlie the evolutionary diversification of Drosophila sex combs

“…This would involve several independent transitions between rotating and prespecified sex combs, as well as multiple origins of transverse sex combs. The first scenario can best be described as convergent morphological evolution, whereas the second implies multiple instances of developmental system drift (preservation of an ancestral phenotype despite the divergence of underlying developmental pathways) (29). Despite the different hypotheses of morphological change, both scenarios involve independent origin and loss of particular modes of development over short evolutionary distances.…”

“…Not only can different mechanisms produce similar morphology, but one or both of these mechanisms have evolved independently in two or more separate lineages. Similarities in the adult appearance between rotating and prespecified sex combs may reflect either convergent morphological evolution or developmental system drift (29). However, any conceivable scenario of sex comb evolution requires multiple transitions between transverse, rotating, and prespecified modes of development, demonstrating that complex developmental pathways can be highly plastic on short evolutionary time scales.…”

Oxygen-induced social behaviours inPristionchus pacificushave a distinct evolutionary history and genetic regulation fromCaenorhabditis elegans

“…Detailed comparisons of multiple developmental and physiological processes between these two nematodes provided important molecular insights. While previous studies did not focus on phenotypic convergence and rather aimed for an understanding of the evolution of developmental processes (evo-devo), they revealed the originally surprising, but common principle of developmental systems drift (DSD), the notion that developmental processes leading to similar and homologous morphological features are still specified by non-homologous molecular processes [3]. One key example of DSD is vulva development in C. elegans and P. pacificus, which results in a homologous organ system that is formed by homologous precursor cells but is regulated by distinct signalling pathways [4].…”