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Abstract Hybrid incompatibilities are a critical component of species barriers and may arise due to negative interactions between divergent regulatory elements in parental species. We used a comparative approach to identify common themes in the regulatory phenotypes associated with hybrid male sterility in two divergent rodent crosses, dwarf hamsters and house mice. We investigated three potential characteristic gene expression phenotypes in hybrids including the propensity of transgressive differentially expressed genes toward over or underexpression, the influence of developmental stage on patterns of misexpression, and the role of the sex chromosomes on misexpression phenotypes. In contrast to near pervasive overexpression in hybrid house mice, we found that misexpression in hybrid dwarf hamsters was dependent on developmental stage. In both house mouse and dwarf hamster hybrids, however, misexpression increased with the progression of spermatogenesis, although to varying extents and with potentially different consequences. In both systems, we detected sex chromosome-specific overexpression in stages of spermatogenesis where inactivated X chromosome expression was expected, but the hybrid overexpression phenotypes were fundamentally different. Importantly, misexpression phenotypes support the presence of multiple developmental blocks to spermatogenesis in dwarf hamster hybrids, including a potential role of meiotic stalling or breakdown early in spermatogenesis. Collectively, we demonstrate that while there are some similarities in hybrid expression phenotypes of house mice and dwarf hamsters, there are also clear differences that point toward unique mechanisms underlying hybrid male sterility. Our results highlight the potential of comparative approaches in helping to understand the causes and consequences of disrupted gene expression in speciation.
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Hybridization and gene expression: Beyond differentially expressed genes
Gene expression has a key role in reproductive isolation, and studies of hybrid gene expression have identified mechanisms causing hybrid sterility. Here, we review the evidence for altered gene expression following hybridization and outline the mechanisms shown to contribute to altered gene expression in hybrids. Transgressive gene expression, transcending that of both parental species, is pervasive in early generation sterile hybrids, but also frequently observed in viable, fertile hybrids. We highlight studies showing that hybridization can result in transgressive gene expression, also in established hybrid lineages or species. Such extreme patterns of gene expression in stabilized hybrid taxa suggest that altered hybrid gene expression may result in hybridization‐derived evolutionary novelty. We also conclude that while patterns of misexpression in hybrids are well documented, the understanding of the mechanisms causing misexpression is lagging. We argue that jointly assessing differences in cell composition and cell‐specific changes in gene expression in hybrids, in addition to assessing changes in chromatin and methylation, will significantly advance our understanding of the basis of altered gene expression. Moreover, uncovering to what extent evolution of gene expression results in altered expression for individual genes, or entire networks of genes, will advance our understanding of how selection moulds gene expression. Finally, we argue that jointly studying the dual roles of altered hybrid gene expression, serving both as a mechanism for reproductive isolation and as a substrate for hybrid ecological adaptation, will lead to significant advances in our understanding of the evolution of gene expression.
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- PAR ID:
- 10495751
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Molecular Ecology
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/mec.17303
