Genome-wide misexpression associated with hybrid sterility in Mimulus (monkeyflower)

Abstract

Divergence in gene expression regulation is common between closely related species and may give rise to incompatibilities in their hybrid progeny. In this study, we investigated the relationship between regulatory evolution within species and reproductive isolation between species. We focused on a well-studied case of hybrid sterility between Mimulus guttatus and M. nasutus, two closely related yellow monkeyflower species, that is caused by two epistatic loci, hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2). We quantified and compared global transcript abundance across male and female reproductive tissues (i.e. stamens and carpels) of M. guttatus and M. nasutus, as well as sterile and fertile progeny from an advanced M. nasutus-M. guttatus introgression line that carries the hms1-hms2 incompatibility. We observed substantial variation in transcript abundance between M. guttatus and M. nasutus, including distinct but overlapping patterns of tissue-biased expression, providing evidence for regulatory divergence between these species. Furthermore, we found pervasive genome-wide misexpression exclusively associated with hybrid sterility - only observed in the affected tissues (i.e. stamens) of sterile introgression hybrids. Examining patterns of allele-specific expression in sterile and fertile hybrids, we found evidence of cis- and trans- regulatory divergence, as well as cis-trans compensatory evolution (likely to be driven by stabilizing selection). However, regulatory divergence does not appear to cause misexpression in sterile hybrids, which instead likely manifests as a downstream consequence of sterility itself.