Dataset Information

Hybrid Incompatibilities and Transgressive Gene Expression Between Two Closely Related Subspecies of Drosophila.

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.

SUBMITTER: Go AC

PROVIDER: S-EPMC7758320 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Publications

Hybrid Incompatibilities and Transgressive Gene Expression Between Two Closely Related Subspecies of <i>Drosophila</i>.

Go Alwyn C AC Civetta Alberto A

Frontiers in genetics 20201210

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 <i>Drosophila</i> that used long-diverged species pairs with complete or nearly complete isolation (i.e., full sterility and partial inviability of hybri ...[more]

PMID: 33362859

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Project description:Horizontal gene transfer and recombination play a major role in microbial evolution and have been detected in diverse groups, including many of medical relevance such as HIV and dengue virus. In the absence of mechanistic barriers, the evolutionary success of a particular recombination event is determined by whether the recombinant genotype suffers a fitness cost through the disruption of favorable epistatic interactions within the genome, and if so, the extent to which this fitness cost might be mitigated by subsequent compensatory evolution. To investigate the importance of epistatic interactions between genes and the evolutionary viability of a homologous recombination event between diverged ancestral genotypes, we constructed two recombinant microvirid bacteriophages by exchanging their alleles of the gene encoding the coat protein. The coding sequences for this gene differ by approximately 8% at the amino acid level and were interchanged between two ancestral phages related to varphiX174 and well adapted to their culture conditions. Because the recombinant phages showed drastically reduced fitnesses, we further explored their evolutionary viability by subjecting replicate lines of each of them to selection. We found that all four lineages achieved fitnesses commensurate with ancestral fitnesses in as few as 60 generations, and on average, the first substitution accounted for more than half of the total fitness recovery. Fitness recovery required three to five substitutions in each lineage, and overall eight of the nine essential phage genes were involved, suggesting extensive epistatic interactions throughout the genome. Interestingly, the proteins with the most extensive and apparent physical interactions with the exchanged protein in the viral capsid did not appear to have much of a role in fitness recovery. This result appears to be a consequence of the conservation of the amino acid residues involved in the interactions. It suggests that strong epistatic interactions are less important than weaker, transient ones in producing genic incompatibilities because they preclude variability in the interacting regions of the proteins.

Project description:BackgroundDuring the speciation process several types of isolating barriers can arise that limit gene flow between diverging populations. Studying recently isolated species can inform our understanding of how and when these barriers arise, and which barriers may be most important to limiting gene flow. Here we focus on Drosophila suboccidentalis and D. occidentalis, which are closely related mushroom-feeding species that inhabit western North America and are not known to overlap in geographic range. We investigate patterns of reproductive isolation between these species, including premating, postmating prezygotic, and postzygotic barriers to gene flow.ResultsUsing flies that originate from a single population of each species, we find that the strength of premating sexual isolation between these species is asymmetric: while D. occidentalis females mate with D. suboccidentalis males at a reduced but moderate rate, D. suboccidentalis females discriminate strongly against mating with D. occidentalis males. Female hybrids will mate at high rates with males of either species, indicating that this discrimination has a recessive genetic basis. Hybrid males are accepted by females of both species. We do not find evidence for postmating prezygotic or postzygotic isolating barriers, as females use the sperm of heterospecific males and both male and female hybrids are fully fertile.ConclusionsPremating isolation is substantial but incomplete, and appears to be the primary form of reproductive isolation between these species. If these species do hybridize, the lack of postzygotic barriers may allow for gene flow between them. Given that these species are recently diverged and are not known to be sympatric, the level of premating isolation is relatively strong given the lack of intrinsic postzygotic isolation. Further work is necessary to characterize the geographic and genetic variation in reproductive isolating barriers, as well as to determine the factors that drive reproductive isolation and the consequences that isolating barriers as well as geographic isolation have had on patterns of gene flow between these species.

Dataset Information

Hybrid Incompatibilities and Transgressive Gene Expression Between Two Closely Related Subspecies of Drosophila.

Publications

Hybrid Incompatibilities and Transgressive Gene Expression Between Two Closely Related Subspecies of <i>Drosophila</i>.

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