Evolution of branched regulatory genetic pathways: directional selection on pleiotropic loci accelerates developmental system drift

Abstract

Developmental systems are regulated by a web of interacting loci. One common and useful approach in studying the evolution of development is to focus on classes of interacting elements within these systems. Here, we use individual-based simulations to study the evolution of traits controlled by branched developmental pathways involving three loci, where one locus regulates two different traits. We examined the system under a variety of selective regimes. In the case where one branch was under stabilizing selection and the other under directional selection, we observed "developmental system drift": the trait under stabilizing selection showed little phenotypic change even though the loci underlying that trait showed considerable evolutionary divergence. This occurs because the pleiotropic locus responds to directional selection and compensatory mutants are then favored in the pathway under stabilizing selection. Though developmental system drift may be caused by other mechanisms, it seems likely that it is accelerated by the same underlying genetic mechanism as that producing the Dobzhansky-Muller incompatibilities that lead to speciation in both linear and branched pathways. We also discuss predictions of our model for developmental system drift and how different selective regimes affect probabilities of speciation in the branched pathway system.

Hybrid Incompatibility Despite Pleiotropic Constraint in a Sequence-Based Bioenergetic Model of Transcription Factor Binding

“…This finding supports the "selection, pleiotropy, and compensation model" (Pavlicev and Wagner 2012) in which compensation for the pleiotropic side effects of adaptation drives DSD in the loci underlying conserved traits. Although we find that compensatory evolution may be constrained by the bioenergetics of the interacting loci, our results support the general conclusion of Johnson and Porter (2007) that directional selection on pleiotropic loci accelerates DSD. An important lesson from the discovery of DSD is that it can obscure sources of selection and lessen the utility of candidate-gene approaches (True and Haag 2001).…”

“…Likewise, the addition of a trait under stabilizing selection should constrain TF change compared to the case of a single positively selected trait. If adaptive change occurs at the pleiotropic TF locus, it will select for compensation at the conserved regulatory target (Johnson and Porter 2007), resulting in hybrid misregulation at both interactions in the three-locus network.To quantify the extent of pleiotropic constraint, we compare two different TF architectures. In the first, the TF consists of a single DNA-binding domain that binds to the cis-regulatory regions of two downstream loci associated with separate traits as illustrated in Figure 1A.…”

Evolutionary meandering of intermolecular interactions along the drift barrier

“…Provided the degree of overall affinity remains within certain bounds, the degrees of freedom beyond the drift barrier present ample opportunities for unbounded molecular wandering of the individual motifs. Such within-species drift will passively give rise to incompatibilities among isolated lineages as the reciprocal partners in heterospecific combinations no longer recognize each other (49,50).…”

Hybrid sterility and evolution in Hawaiian Drosophila: differential gene and allele-specific expression analysis of backcross males

“…Further research is also necessary to examine the potential for a smaller number of genes to create the initial incompatible developmental pathways that then lead to other changes in developmental and gene expression patterns to create hybrid male sterility (Coyne and Orr, 2004;Johnson, 2000). The comparison of gamete formation between more species in a phylogenetic context could shed light into how gene expression patterns and the gamete physiological and developmental systems evolve over time within and between species (Porter and Johnson, 2002;Johnson and Porter, 2007).…”

“…Theoretical models suggest that the effects of accumulation of regulatory incompatibilities in the architecture of transcriptional networks can be a part of hybrid incompatibilities directly influencing the process of speciation (Porter and Johnson, 2002;Johnson and Porter, 2007). Techniques such as microarrays have been used to characterize gene expression, and have uncovered several genes that are deregulated in hybrids between species, especially in D. mauritiana and D. simulans (Michalak and Noor, 2003;Moehring et al, 2007).…”