Misregulation of Gene Expression and Sterility in Interspecies Hybrids: Causal Links and Alternative Hypotheses

Abstract

Understanding the origin of species is of interest to biologist in general and evolutionary biologist in particular. Hybrid male sterility (HMS) has been a focus in studies of speciation because sterility imposes a barrier to free gene flow between organisms, thus effectively isolating them as distinct species. In this review, I focus on the role of differential gene expression in HMS and speciation. Microarray and qPCR assays have established associations between misregulation of gene expression and sterility in hybrids between closely related species. These studies originally proposed disrupted expression of spermatogenesis genes as a causative of sterility. Alternatively, rapid genetic divergence of regulatory elements, particularly as they relate to the male sex (fast-male evolution), can drive the misregulation of sperm developmental genes in the absence of sterility. The use of fertile hybrids (both backcross and F1 progeny) as controls has lent support to this alternative explanation. Differences in gene expression between fertile and sterile hybrids can also be influenced by a pattern of faster evolution of the sex chromosome (fast-X evolution) than autosomes. In particular, it would be desirable to establish whether known X-chromosome sterility factors can act as trans-regulatory drivers of genome-wide patterns of misregulation. Genome-wide expression studies coupled with assays of proxies of sterility in F1 and BC progeny have identified candidate HMS genes but functional assays, and a better phenotypic characterization of sterility phenotypes, are needed to rigorously test how these genes might contribute to HMS.

Speciation and the developmental alarm clock

“…Genes that control male-biased traits may evolve especially rapidly due to sexual selection or mutational biases ('faster male' theory), or gene regulatory networks controlling male traits may be unusually sensitive to genetic perturbation in hybrids ('fragile males'), or genes linked the X-chromosome may evolve especially fast ('faster X') (Charlesworth et al 1987, Wu andDavis 1993). Consequently, Xlinked genes may show distinct patterns of misexpression in hybrids (Moehring et al 2007, Turner et al 2014, Civetta 2016, Sanchez-Ramirez et al 2020. Developmental pathways related to spermatogenesis seem especially sensitive to disruption in hybrids, perhaps being predisposed to disproportionate compensatory cis-trans regulatory coevolution (Mack et al 2016, Mack and Nachman 2017).…”

Did sex chromosome turnover promote divergence of the major mammal groups?

“…Sex chromosomes are known to have major effects on speciation in terms of Haldane's Rule and the large X effect, explored in detail in Drosophila but evident also in mammals 11, 12. New comparative genetic data document many vertebrates in which autosomes in one species have become sex chromosomes in another, as well as many rearrangements of sex chromosomes and autosomes.…”

Support for the dominance theory inDrosophilatranscriptomes

“…Disruption of gene expression has been extensively documented in Drosophila hybrids and it is often the case that rapidly evolving genes enriched in male functions tend to be overrepresented among misexpressed genes in sterile hybrid males (REILAND AND NOOR 7 GOMES AND CIVETTA 2015). While the potential link between faster--male theory (WU AND DAVIS 1993;WU et al 1996) and hybrid misexpression has been explored (NOOR 2005;HAERTY AND SINGH 2006;ORTIZ--BARRIENTOS et al 2007;CIVETTA 2016), the dominance theory for hybrid transcriptomes remains untested. Here we examine genome--wide patterns of transcript abundance in females and males of Drosophila yakuba, D. santomea and their interspecific hybrids using RNAseq technology for genes with variable degrees of sex--biased expression.…”