Support for the Dominance Theory inDrosophilaTranscriptomes

Abstract

Interactions among divergent elements of transcriptional networks from different species can lead to misexpression in hybrids through regulatory incompatibilities, some with the potential to generate sterility. While the possible contribution of faster-male evolution to this misexpression has been explored, the role of the hemizygous X chromosome (i.e., the dominance theory for transcriptomes) remains yet to be determined. Here, we study genome-wide patterns of gene expression in females and males of Drosophila yakuba, Drosophila santomea and their hybrids. We used attached-X stocks to specifically test the dominance theory, and we uncovered a significant contribution of recessive alleles on the X chromosome to hybrid misexpression. Our analyses also suggest a contribution of weakly deleterious regulatory mutations to gene expression divergence in genes with sex-biased expression, but only in the sex toward which the expression is biased (e.g., genes with female-biased expression when analyzed in females). In the opposite sex, we found stronger selective constraints on gene expression divergence. Although genes with a high degree of male-biased expression show a clear signal of faster-X evolution of gene expression, we also detected slower-X evolution in other gene classes (e.g., female-biased genes). This slower-X effect is mediated by significant decreases in cis- and trans-regulatory divergence. The distinct behavior of X-linked genes with a high degree of male-biased expression is consistent with these genes experiencing a higher incidence of positively selected regulatory mutations than their autosomal counterparts.

Comparative transcriptomics between Drosophila mojavensis and D. arizonae reveals transgressive gene expression and underexpression of spermatogenesis-related genes in hybrid testes

“…However, this bias was not observed in D. buzzatii and D. koepferae (~ 4.49 mya) female hybrids 14 . The absence of massive gene deregulation in ovaries could be related to the higher stability of gene expression in females, which is mainly influenced by the slower evolutionary rates of female-biased genes and the presence of two X-chromosomes, as was reported in other Drosophila species 17 , 57 , and this phenomenon could be important in the fertile phenotype observed in these hybrids. Thus, we suggest that in hybrid ovaries from recently diverged species, DEGs tend to be overexpressed, but over time, global deregulation will increase due to the accumulation of genetic changes, and the number of over- and underexpressed genes will become symmetric.…”

“…According to the model of Dobzhansky–Muller 11 , 12 , fixed mutations in genetically isolated populations can result in deleterious epistatic interactions, disrupting regulatory networks and leading to serious consequences in hybrids 2 , 13 – 15 . In addition, according to Haldane’s rule 16 , sterility in hybrids is more likely to affect the heterogametic sex, and the degree and extent of these genetic incompatibilities are related to the time of divergence and are likely the result of divergent regulatory sequences 13 , 15 , 17 , 18 .…”

The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs. autosomes

“…However, it has been experimentally tested (and validated) almost exclusively in Drosophila (e.g. Masly and Presgraves 2007; Cattani and Presgraves 2012; Llopart et al 2018, but see Matsubara et al 2015 for a study in rice). Assessing its generality remains difficult, due to the experimental challenge of measuring the dominance of mutations.…”

Meiotic, genomic and evolutionary properties of crossover distribution in Drosophila yakuba

“…Modifers of crossover rates are known to segregate in natural populations of many species [118,120,128,[198][199][200][201] and models of selection and recombination predict an overall benefit to increasing rates when finite populations are considered (see [202] and references therein). Increased crossover rates could be particularly frequent on the X chromosome because this chromosome would be more likely to take advantage of recesive beneficial modifiers that increase rates relative to autosomes, a possibility that would fit with Drosophila studies showing stronger positive selection acting on the X at both protein and gene expression levels [103,[203][204][205][206][207][208][209][210][211]. At the same time, there is a direct limitation to increasing the number of crossovers in meiosis I given the known increased probability of missegregation and higher rates of ectopic exchange and chromosomal aberrations in multi-chiasma tetrads [212,213].…”