Abstract
Genome-wide assays of expression between species and their hybrids have identified genes that become either over- or underexpressed relative to the parental species (i.e., transgressive). Transgressive expression in hybrids is of interest because it highlights possible changes in gene regulation linked to hybrid dysfunction. Previous studies in Drosophila that used long-diverged species pairs with complete or nearly complete isolation (i.e., full sterility and partial inviability of hybrids) and high-levels of genome misregulation have found correlations between expression and coding sequence divergence. The work highlighted the possible effects of directional selection driving sequence divergence and transgressive expression. Whether the same is true for taxa at early stages of divergence that have only achieved partial isolation remains untested. Here, we reanalyze previously published genome expression data and available genome sequence reads from a pair of partially isolated subspecies of Drosophila to compare expression and sequence divergence. We find a significant correlation in rates of expression and sequence evolution, but no support for directional selection driving transgressive expression in hybrids. We find that most transgressive genes in hybrids show no differential expression between parental subspecies and used SNP data to explore the role of stabilizing selection through compensatory mutations. We also examine possible misregulation through cascade effects that could be driven by interacting gene networks or co-option of off-target cis-regulatory elements.
Highlights
Studies that have addressed the genetic basis of incompatibilities in hybrids between species, or diverging populations, have traditionally resorted to mapping loci and interactions between them (Coyne and Orr, 1989; Masly and Presgraves, 2007; Presgraves, 2008; Victoria Cattani and Presgraves, 2012; Dufresnes et al, 2016)
We found a significant correlation for expression differences between subspecies and non-synonymous sequence divergence (N = 604; Spearman’s ρ = 0.091, P = 0.026) but not between differences in expression and synonymous substitutions (Spearman’s ρ = -0.046, P = 0.261)
The analysis showed no significant correlations between sequence divergence and expression difference (N = 35; dN, ρ = 0.078, P = 0.655; dS, FIGURE 2 | Scenarios of regulatory divergence for cis and trans regulatory elements. (A) Gene 1 shows compensatory cis and trans mutations, denoted by asterisks, wherein D. p. bogotana experiences an initial mutation in cis followed by a mutation in trans restoring gene expression to similar levels between parental subspecies
Summary
Studies that have addressed the genetic basis of incompatibilities in hybrids between species, or diverging populations, have traditionally resorted to mapping loci and interactions between them (Coyne and Orr, 1989; Masly and Presgraves, 2007; Presgraves, 2008; Victoria Cattani and Presgraves, 2012; Dufresnes et al, 2016) This approach has been fruitful in that a few major protein-coding genes have been identified (Ting et al, 1998; Masly et al, 2006; Mihola et al, 2009; Phadnis and Allen Orr, 2009), and in some cases, the effect of these major genes require interactions with other genetic factors. The reduced fitness of hybrids serves as a postzygotic barrier among divergent taxa
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