Beyond speciation genes: an overview of genome stability in evolution and speciation

Abstract

Genome stability ensures individual fitness and reliable transmission of genetic information. Hybridization between diverging lineages can trigger genome instability, highlighting its potential role in post-zygotic reproductive isolation. We argue that genome instability is not merely one of several types of hybrid incompatibility, but rather that genome stability is one of the very first and most fundamental traits that can break down when two diverged genomes are combined. Future work will reveal how frequent and predictable genome instability is in hybrids, how it affects hybrid fitness, and whether it is a direct cause or consequence of speciation.

Figure 1. Schematic representation of genome instability mechanisms contributing to post-zygotic reproductive isolation

A. Mito-nuclear incompatibilities may lead to increased reactive oxygen species production. A nucleus-encoded protein (light blue) is incompatible with a mitochondria-encoded protein (green). These two proteins interact together in the electron transport chain in sub-optimal ways due to amino acid changes between two lineages. This leads to inefficient oxidative phosphorylation and release of reactive oxygen species (yellow stars), which causes DNA damage. B. DNA mismatch proteins halt meiotic recombination between divergent sequences (here, between divergent homologous chromosomes in red and blue), reducing fertility of hybrids. C. Different Robertsonian chromosome rearrangements occur between diverging lineages (top panel). Upon secondary contact, these form complex and unstable arrangements during hybrid meiosis, reducing fertility (lower panel). D. Transposable element derepression in hybrids. Diverging lineages carry different transposable elements. Maternally loaded piRNAs initiate transposable element repression, maintaining silencing in the zygote (left panel). Paternally contributed transposable elements may be derepressed if the female fails to load repressive piRNAs. This leads to transposable element mobilization with potentially deleterious consequences for the progeny (right panel).