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Keywords:

  • angiosperm;
  • hybrid;
  • meiotic drive;
  • selfish gene;
  • speciation;
  • sterility

The predominant causes of biological diversification – especially the formation of new species (speciation) – hold a special place in the imagination of evolutionary biologists. Much of the contemporary interest in speciation focuses on understanding the evolutionary origin and genetic basis of barriers to gene flow between closely related species (Coyne & Orr, 2004). In this issue of New Phytologist (pp. 888–900), Koide et al. present an analysis of the fine-scale structure of a transmission ratio distortion locus that causes both pollen and ovule sterility. In addition, with tester crosses, they show that this locus could contribute to F1 semi-sterility between Asian and African rice species complexes. In doing so, they make a significant contribution to the current understanding of the genetic underpinnings of loci that can contribute to postzygotic reproductive barriers among plant species.

‘ ... the origin of postzygotic isolation (i.e. hybrid inviability and sterility) was initially considered paradoxical for evolutionists, including Darwin ...’

Barriers to reproduction between species can act at many different stages. Classically these are divided into two classes – those that act before fertilization and those that act after fertilization (prezygotic and postzygotic barriers, respectively). It is often argued that mechanisms that act before hybridization are the most important, primarily because they exert the greatest influence on restricting gene flow between lineages by acting earlier in the life cycle (Rieseberg & Willis, 2007). Nonetheless, the nature, strength, and genetic basis of postzygotic isolation have continued to attract the attention of researchers, especially in animal systems (Coyne & Orr, 2004), but increasingly also in plants (Rieseberg & Willis, 2007).

Arguably, the reasons for this interest have to do with two characteristics of postzygotic reproductive isolation. First, the origin of postzygotic isolation (i.e. hybrid inviability and sterility) was initially considered paradoxical for evolutionists, including Darwin, because natural selection should never favor the fixation of traits that reduce offspring fitness. This paradox was resolved in the form of a model (commonly called the ‘Dobzhansky–Muller’ (DM) model, after two of its originators; Fig. 1). Under the DM model, hybrid incompatibility is the result of negative interlocus epistasis; that is, dysfunctional interactions between different loci that have diverged in isolation of each other (Fig. 1). The great advantage of the DM model is that it does not require diverging populations to go through a period of reduced fitness during the evolution of genes that cause hybrid inviability or sterility. New variants can be perfectly fit in the background upon which they arose, but are dysfunctional in a genetic background where they have never been tested by natural selection.

image

Figure 1. Dobzhansky–Muller (DM) model for the evolution of hybrid incompatibility (sterility and inviability). An ancestral population with genotype aabb is divided into two independently evolving lineages. New alleles arise and are fixed independently in each lineage (A and B, in lineages 1 and 2, respectively). Hybrid incompatibility is caused by dysfunctional interactions between A and B (i.e. alleles that have never been co-tested before hybridization).

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The DM model therefore proposes that genetic interactions are crucial to the evolution of postzygotic isolation, though it is silent on the specific evolutionary forces and genetic changes involved in this process. Given this, the second, and perhaps the most influential, appeal of postzygotic isolation is that these evolutionary forces and underlying genes are virtually unknown, even in the most well-studied genetic systems. Indeed, the molecular loci underlying hybrid sterility or inviability have been cloned and functionally characterized in only a handful of cases (Coyne & Orr, 2004; Orr et al., 2007); none of these has been in plants. Plant systems have been used to identify quantitative trait loci (QTL) associated with interspecific sterility phenotypes, either genome-wide (Li et al., 1997; Kim & Rieseberg, 1999; Moyle & Graham, 2005; Nakazato et al., 2007) or at individual interacting loci (Sweigart et al., 2006; Matsubara et al., 2007); however, the molecular genetic basis of these QTL is yet to be described.

Koide et al.'s paper goes some way to bridging this gap between chromosomal regions known to be associated with hybrid incompatibility and the molecular genetic loci that underlie them. In their paper, Koide et al. combine fine-mapping, cytology, and tester crosses to examine the basis and possible origins of a transmission ratio distortion (TRD) locus in rice. Classical studies of this locus suggested that the distorting allele (S1) causes abortion of gametes carrying the homologous nondistorting (inline image) allele, when both are found in heterozygotes (Sano, 1990, and references therein). By inducing semi-sterility in F1 hybrids (via abortion of male and female gametes carrying the inline image allele), this transmission ratio distorter has the potential to contribute to postzygotic reproductive isolating barriers between rice species.

In their study, Koide et al. confirm that TRD at the S1 locus induces preferential abortion of both male and female gametes carrying inline image. For TRD via males (mTRD), cytology suggests that abortion is the result of arrest before the second mitotic division in microsporogenesis. For TRD via females (fTRD), abortion is caused by a broader range of phenotypes involving structural or organizational defects in the formation of eggs or embryo sacs. Using segregation ratios of aborted gametes with a linked visible marker, and fine-scale mapping, they infer the TRD locus is composed of at least two components, each influencing either mTRD or fTRD. Using fine-mapping, they narrow the mTRD to an approx. 40 kb region that contains only eight ORFs, an experimentally tractable list of candidates for further functional analysis.

These data are in part exciting because they provide quite a detailed picture of the genetic components of a ‘selfish’ gene: a locus that preferentially promotes its own transmission to the fitness detriment of a carrier heterozygote (Hurst & Werren, 2001). This locus is composed of multiple components that influence male and female TRDs differently, suggesting a cluster of closely linked genes, as has been found in other segregation distorter systems. Perhaps even more interesting, however, is the apparent mechanistic link between ‘selfish’ transmission distortion, and the expression of hybrid sterility between species. Based on the results of tester crosses, Koide et al. propose that alternative alleles are fixed in Asian and African rice species complexes, indicating that the action of the distorter S1 allele found in the African rice complex can contribute to F1 semi-sterility (gamete abortion) between these groups.

A direct link between the evolution of postzygotic isolation and active transmission ratio distorters – such as male killers, meiotic drivers, sex-ratio distorters, centromeric drivers, and other selfish genetic elements – has been proposed theoretically (see Hurst & Werren, 2001; Coyne & Orr, 2004 for reviews). Nonetheless, there is currently little empirical evidence for the predominance of active segregation distortion mechanisms as a cause of hybrid sterility or inviability. For example, while some interspecific transmission ratio distorters have been directly connected to the expression of hybrid sterility phenotypes (Coyne & Orr, 2004), in other cases there is clearly no fitness decrement associated with segregation distorters acting between species (Fishman & Willis, 2005). Other general patterns suggest that active segregation distortion is unlikely to be a ubiquitous force shaping the evolution of postzygotic isolation. For example, centromeres do not seem to be disproportionately associated with the expression of hybrid problems in species crosses (Moyle, 2007), although centromeres are genomic regions that stand to benefit most from transmission distortion under some models (Henikoff et al., 2001).

While Koide et al.'s results are unlikely to resolve questions of the ubiquity of selfish genes in evolving postzygotic reproductive isolation, they do provide interesting data supporting a direct connection between genetic selfishness and the expression of hybrid sterility in this case. Gametic lethality as a result of TRD has been associated with interspecific and intervarietal rice crosses in other studies (Sano, 1990, and references therein), suggesting additional loci might behave similarly in this plant group. Clearly more data, including the dissection and description of the molecular genetic loci underlying hybrid incompatibilities in a wider range of organisms, will be instrumental in resolving how common such processes are in generating postzygotic reproductive isolation. These data will be essential for drawing any strong inferences about general patterns in the evolutionary forces or underlying genes that contribute to reproductive barriers.

Finally, perhaps one of the most difficult goals in speciation research is determining whether loci that could contribute to current reproductive isolation were directly involved in the speciation process itself, rather than accumulating after diverging lineages were already well-isolated species. Genes that fall into the latter class still provide valuable insight into the range of possible mechanisms that can cause hybrid incompatibility. Arguably, however, it is the genes involved in the actual speciation event that are the most intriguing for evolutionary biologists. Koide et al. are appropriately circumspect about the possible role of the S1/inline image locus in the actual lineage splitting of the progenitor of Asian and African rice species complexes. Evidence that the alternative alleles at this locus are fixed in the two species complexes is consistent with these alleles having diverged early in the split of these two groups. Nonetheless, data that can more closely match the timing of the split of these species groups with the evolutionary origin of this locus (perhaps from molecular evolutionary analyses of the eventual underlying gene(s)) will be necessary to resolve this question. Regardless, this study demonstrates that plant systems, especially those with genetic, genomic, and functional tools, are very promising systems for further adding to our understanding of the genetic basis of postzygotic isolation, and the likely evolutionary forces responsible for fixing these genes.

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