Evolution and Molecular Control of Hybrid Incompatibility in Plants

Abstract

Postzygotic reproductive isolation (RI) plays an important role in speciation. According to the stage at which it functions and the symptoms it displays, postzygotic RI can be called hybrid inviability, hybrid weakness or necrosis, hybrid sterility, or hybrid breakdown. In this review, we summarized new findings about hybrid incompatibilities in plants, most of which are from studies on Arabidopsis and rice. Recent progress suggests that hybrid incompatibility is a by-product of co-evolution either with "parasitic" selfish elements in the genome or with invasive microbes in the natural environment. We discuss the environmental influences on the expression of hybrid incompatibility and the possible effects of environment-dependent hybrid incompatibility on sympatric speciation. We also discuss the role of domestication on the evolution of hybrid incompatibilities.

Keywords: Bateson-Dobzhansky–Muller model; Hybrid incompatibility; Speciation genes; evolutionary force; evolutionary genetics; postzygotic reproductive barriers.

FIGURE 1

Different forms of postzygotic reproductive isolation (RI).

FIGURE 2

Genetic models of hybrid incompatibilities that occur in sporophytes (A,B,E) and gametophytes (C,D,F) at F₁ generation (A–D) or later generation (E,F). (A) Classic two-locus interaction Bateson-Dobzhansky–Muller (BDM) model. Ancestral genes were independently mutated and sustained in parallel populations isolated by geographic barrier. The mutations are compatible to their own genetic contexts. However, mixture of these mutations are deleterious to the hybrids and leads to hybrid incompatibility. (B) The allelic interaction BDM model. Distinct from the two-locus involved BDM model, disharmonious interaction occurs between different alleles at one locus. (C) The sporo-gametophytic interaction model. Allelic interaction cause gamete abortion in the hybrids. The selfish nature of S allele can kill gametes with genotype S^a. The S and S^a alleles are likely evolved from a wild-compatible allele Sⁿ, which is compatible with either S and S^a. No fertility issue can be observed in SSⁿ and S^aSⁿ hybrids. Alternatively, Sⁿ allele may also be the intermediate form of S and S^a during evolution. For example, after the ancestral allele S mutating to Sⁿ, a second mutation of Sⁿ produces S^a. (D) The duplicate gametic lethal model. At least one functional copy of the duplicated loci of S1 and S2 is required for gamete development. To avoid confusing of s₁ and s₂, the functional alleles (S₁ and S₂) are illustrated as +₁ and +₂ in the figure. (E) The duplicate recessive lethal model to elucidate genetic control of sporophytic F₂ hybrid dysfunction. Duplicated A₁ and A₂ are essential to plants. Mutation at one locus is tolerated in plants due to the redundancy. However, if two populations carry mutations at different loci, their offspring with genotype a₁a₁a₂a₂ will show inferiority, owing to lack of any functional copy of A₁ or A₂. (F) A more complicated genetic model controlling F₂ hybrid sterility identified in rice. During evolution, a regulator Su was evolved to suppress the selfish nature of the S allele described in (C) in a sporophytic manner. Only the ss^a hybrids without SU showed sterility. The red arrows in (A–C) indicate deleterious genetic interactions between loci or alleles. The yellow and gray ovals in (D–F) indicate fertile and sterile pollens, respectively.

FIGURE 3

Diagram of how environmentally conditioned hybrid incompatibility contributes to sympatric speciation. Arrows indicate gene flow between individuals. Blue and yellow dots indicate individuals with different genotypes that inhabit the same region. Initially, individuals with different genotype are compatible with each other. Along with environmental changes (such as decreasing temperature), environmentally conditioned genetic incompatibility leads to hybrid incompatibility between different genotypes.