Rapid Speciation via Parallel, Directional Selection on Regulatory Genetic Pathways

Abstract

Regulatory genetic pathways are ubiquitous in organisms and play a central role in the realization of the phenotype during development. We explored the proposition that these pathways can provide a plausible source of the epistatic variation that has been implicated in the evolution of postzygotic reproductive isolation. We modeled gene regulation as a matching function between the product of one locus and the promoter site of the next locus in the pathway, with binding strength determining the amount of product. When the phenotype is subject to parallel selection in a pair of independent populations, we "nd that the "tnesses of F and F hybrids often drop to very low values as the populations respond in genetically di!erent and incompatible ways. The simulations support the predictions of the analytical models. Hybrid "tness reduction occurs more often as the number of loci in the pathway increases, and as the binding site interactions become more complex. Less hybrid "tness reduction is seen when the populations start with imperfect binding in the pathway. In contrast, when we constructed the phenotype without gene regulation using multiplicative rules, isomorphic to the additive phenotype commonly assumed in evolutionary models, we found no appreciable F "tness reduction and only slight F "tness reduction. The interaction of genetic drift and mutation, even at very high rates, did not reduce hybrid "tness at all on the time-scales we considered. Clearly, the evolution of regulatory genetic pathways can play an important role in speciation, but much more empirical information is needed on the e!ect of allelic variability in regulatory site interactions before this role is fully understood. Academic Press

Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids

“…Several fixed nucleotide differences are located in the gene region around to exon 12a, which is a spliced exon required for isoform Taf1-2. The sequence divergence might therefore affect alternative splicing efficiency (52), promoter-binding affinity, chromatin modification, or other processes that could contribute to hybrid male sterility as a quantitative trait (53,54). The role of Taf1 in hybrid male sterility is perhaps not surprising in light of the rapid evolution and functional diversification of testes-specific TAFs in Drosophila (55).…”

Genotype-dependent variation of mitochondrial transcriptional profiles in interpopulation hybrids

“…In this way, neutral variation may segregate within lineages and eventually diverge from sister groups. However, the reduced complexity of the mitochondrial transcriptional regulatory network compared with nuclear regulatory networks may reduce the applicability of such a model with regard to mitochondrial transcription (8). An alternative model describing the generation of hybrid incompatibilities was proposed by Kimura (35).…”

“…Expression of many genes is disrupted in hybrids and can have strongly deleterious effects (4)(5)(6). Epistatic interactions are ubiquitous in all regulatory networks (7), and their dysfunction in hybrids is often envisioned as a product of altered interaction strength between transcription factors and their binding sites evolving under a DobzhanskyMuller or compensatory evolution model (8)(9)(10)(11). However, identification of specific transcription factors, RNA polymerases, or cis-regulatory motifs underlying these observations has proven difficult.…”

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).…”