Abstract:

Background & Aims: Reproductive isolation is a key hallmark of speciation and species maintenance, but "reproductive isolation genes" are often equated with "speciation genes." Reproductive isolation genes constitute a broad set: any genetic element that is significantly differentiated between populations and reduces effective interspecific progeny at any stage of the life cycle belongs to this set, and they accumulate over divergence time. Speciation genes, by contrast, are the founding genes within this set that earliest establish initial reproductive isolation at the origin of lineage divergence and initiate independent evolution, and they must simultaneously satisfy "participating in reproductive isolation" and "earliest driving divergence." 

Review Results: Reproductive isolation between closely related species is often incomplete, arising from the sequential action and synergistic accumulation of multiple barriers. In dichotomous divergence, later-stage postzygotic isolation genes may originate from linkage hitchhiking or temporal accumulation, becoming "hitchhikers/reinforcers"; prezygotic isolation driven by natural selection (including sexual selection) is more likely to initiate divergence. Geographic isolation is not a necessary condition, but it can block gene flow and accelerate selection-mediated divergence. In homoploid hybrid speciation (not involving changes in chromosome ploidy between species or subspecies), the identification of speciation genes is relatively easier, benefiting from advances in the mechanism understanding and technical methods. Its genetic logic is similar to the free assortment of non-allelic genes and traits in F₂ generations of intraspecific crosses, for example, crosses between AABBCCDD and aabbccdd to produce the genotype AAbbCCdd, but F₂ generations of interspecific (or intersubspecific) crosses often suffer individual death due to reproductive isolation, failing to exhibit Mendelian expected genotype or phenotype ratios, yet displaying extremely diverse array of recombinant and novel traits due to non-allelic recombination even totally new non-allelic gene interactions. If the multi-locus highly differentiated recombinant genes in hybrid offspring with these phenotypes that are fixed through iterative fertility restoration are associated with reproductive isolation with parents, they can be regarded as the speciation genes of this process. 

Conclusions: We suggest that future research should shift from static "gene-reproductive trait" associations to dynamic reconstruction of the evolutionary history of reproductive isolation genes, so as to better identify speciation genes; and that iterative distant homoploid hybridization through rich non-allelic recombination can create novel recombinant or novel traits, providing a new avenue for agricultural breeding and materials similar to ‘creating mutants’ for dissecting the underlying molecular genetic mechanisms, including new gene interactions and others.

Key words: Incomplete reproductive isolation, speciation genes, dichotomous divergence, homoploid hybrid speciation, non-allelic recombination, new gene interaction