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

Fernando Díaz, Jason Wolf, Reinaldo A. de Brito

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Article numberevad071
Number of pages19
JournalGenome biology and evolution
Volume15
Issue number5
Early online date8 May 2023
DOIs
Publication statusPublished - 31 May 2023

Bibliographical note

Funding Information:
We would like to thank FAPESP (Fundaçao do Amparo à Pesquisa do Estado de São Paulo) Grants #2010/20455-4, #2014/50940-2, #2018/06611-5 and the Science without Borders program at CAPES (Processo PVE 056/2013) for financial support. R.A.B. is a CNPq Productivity fellow (#315287/2020-9).


© The Author(s) 2023.

Data Availability Statement

All RNAs-seq reads underlying this article have been deposited in the Sequence Read Archive at NCBI under BioProject ID PRJNA934045.

Keywords

  • cis/trans regulation
  • hybrid incompatibility
  • introgression
  • RNA-seq
  • speciation with gene flow
  • transgressive expression

ASJC Scopus subject areas

  • General Medicine

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