Hybridization and gene expression: Beyond differentially expressed genes

Abstract

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.

Keywords: RNAseq; evolutionary novelty; gene networks; speciation; transcriptomics.

FIGURE 1

Factors affecting gene expression. (a) Epigenetic modifications can occur at the histone level, with specific modifications generating open (blue) and closed (red) chromatin states. Alternatively, cytosine DNA methylation at regulatory CpG islands, short stretches of palindromic cytosine followed by guanine nucleotides (CpG) that are often near promoters, can alter gene expression. (b) Inversions and other structural variants can remodel the regulatory landscape surrounding genes, altering the orientation of promoters relative to genes (ancestral promoter orientation in red, inverted orientation in blue). (c) Allele‐specific transposable element (TE) insertions can alter expression by inserting into the regulatory element of the gene adding or disrupting transcription factor‐binding sites, or by triggering TE silencing mechanisms that silence the gene as well. Regulatory elements from other locations in the genome, (d) non‐coding RNAs (ncRNAs), such as Piwi‐interacting RNAs (piRNA) or short interfering RNA (siRNA), and (e) trans‐acting transcription factors interact with cis‐acting allelic variation to fine‐tune gene expression.

FIGURE 2

Survey of hybrid gene expression studies. Each tip of the tree represents two hybridizing taxa, with divergence time between parental taxa indicated in millions of years (mya). The tissue that hybrid gene expression has been evaluated was summarized as a reproductive tissue (e.g. testes or ovaries) or a somatic tissue (e.g. brain, leaf). We indicated whether studies used novel methods such as allele‐specific expression (ASE) or assaying expression over a developmental timeline. We further categorized studies by expression patterns found in hybrids and whether hybridization led to novelty or incompatibility. Where no information on tissue was given, this is denoted by NA. https://www.phylopic.org/permalinks/1286be6838cef3d4d7afbcff2d2baa8d184a026eb85dcde64db00ff61457b82d.

FIGURE 3

Co‐evolved cis‐ and trans‐regulatory elements can be broken up into hybrids, expanding the range of variation in gene expression. First‐generation hybrids (F1) may have expression within the range of parental variation if alleles are additive (shown here) but may also show transgressive expression if alleles have epistatic interactions. Later generation hybrids (F2+) thus have expanded expression variation that can be acted upon by selection.