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Transcriptional Misexpression in Hybrids between Species Linked by Gene Flow Is Associated With Patterns of Sequence Divergence

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Author(s):
Diaz, Fernando ; Wolf, Jason ; de Brito, Reinaldo A.
Total Authors: 3
Document type: Journal article
Source: GENOME BIOLOGY AND EVOLUTION; v. 15, n. 5, p. 19-pg., 2023-05-05.
Abstract

The extent to which hybridization disrupts a gene's pattern of expression likely governs its propensity for introgression, whereas its extent of molecular divergence can itself underlie such disruption. Together, these phenomena shape the landscape of sequence and transcriptional divergence across the genome as species diverge. To understand this process, we characterize gene expression inheritance, regulatory divergence, and molecular divergence in the reproductive transcriptomes of species linked by gene flow: the fruit flies Anastrepha fraterculus and A. obliqua, which show evidence of gene flow despite clear evolutionary divergence. We find that their transcriptional patterns are a mosaic between those typically observed within and between allopatric species. Transcripts showing transgressive expression in hybrids or cis-regulatory divergence between species are associated with greater sequence divergence. This may reflect pleiotropic constraints that make them resistant to gene flow or they may be more likely to experience divergent selection. Although these more divergent gene classes are likely to be important contributors to species differences, they are relatively rare. Instead, most differentially regulated transcripts, including those linked to reproduction, show high degrees of dominance in hybrids and trans-regulated divergence between species, suggesting widespread genetic compatibility that potentially allowed for introgression. These findings provide insights into how postzygotic isolating mechanisms might evolve in the presence of gene flow: regions showing cis-regulatory divergence or transgressive expression contribute to reproductive isolation, whereas regions with dominant expression and trans-regulatory divergence allow for introgression. These patterns create a genomic mosaic of transcriptional regulation that is tied to sequence divergence. (AU)

FAPESP's process: 14/50940-2 - INCT 2014: of the Hymenoptera Parasitoid
Grantee:Angélica Maria Penteado Martins Dias
Support Opportunities: Research Projects - Thematic Grants
FAPESP's process: 18/06611-5 - Comparative Genomics and Phylogenomics of Anastrepha fruit flies, with emphasis on the fraterculus group
Grantee:Reinaldo Otávio Alvarenga Alves de Brito
Support Opportunities: Regular Research Grants
FAPESP's process: 10/20455-4 - Comparative genomics of species of fruit flies from the group fraterculus. II. The next generation
Grantee:Reinaldo Otávio Alvarenga Alves de Brito
Support Opportunities: Regular Research Grants