Evolution of interspecies unilateral incompatibility in the relatives of Arabidopsis thaliana

Abstract

The evolutionary concurrence of intraspecies self-incompatibility (SI) and explosive angiosperm radiation in the Cretaceous have led to the hypothesis that SI was one of the predominant drivers of rapid speciation in angiosperms. Interspecies unilateral incompatibility (UI) usually occurs when pollen from a self-compatible (SC) species is rejected by the pistils of a SI species, while the reciprocal pollination is compatible (UC). Although this SI × SC type UI is most prevalent and viewed as a prezygotic isolation barrier to promote incipient speciation of angiosperms, comparative evidence to support such a role is lacking. We show that SI × SI type UI in SI species pairs is also common in the well-characterized accessions representing the four major lineages of the Arabidopsis genus and is developmentally regulated. This allowed us to reveal a strong correlation between UI strength and species divergence in these representative accessions. In addition, analyses of a SC accession and the pseudo-self-compatible (psc) spontaneous mutant of Arabidopsis lyrata indicate that UI shares, at least, common pollen rejection pathway with SI. Furthermore, genetic and genomic analyses of SI × SI type UI in A. lyrata × A. arenosa species pair showed that two major-effect quantitative trait loci are the stigma and pollen-side determinant of UI, respectively, which could be involved in heterospecies pollen discrimination. By revealing a close link between UI and SI pathway, particularly between UI and species divergence in these representative accessions, our findings establish a connection between SI and speciation. Thus, the pre-existence of SI system would have facilitated the evolution of UI and accordingly promote speciation.

Mating system variation in hybrid zones: facilitation, barriers and asymmetries to gene flow

“…In addition to the classic evidence for this rule (e.g. Lewis & Crowe, ), recent studies have shown that this pattern of cross‐incompatibility holds in the wild tomato clade (Solanaceae, Baek et al ., ), and in the mustards (Brassicaceae, Li et al ., ). However, studies in additional taxa are needed for a more thorough characterization of the occurrence of this ‘rule’.…”

“…As such, the SI × SC rule does not appear immediately, but rather requires sufficient divergence such that the Cullin function breaks down, an observation consistent with the fact that some SC populations/accessions can fertilize SI plants (Hogenboom, ). The mechanism of UI is less well understood in mustards (Brassicaceae), but is likely caused by the same pollen rejection pathway responsible for rejecting self‐pollen (Li et al ., ). Finally, in the Polemoniaceae, the strong correlation between self‐specific and interspecific incompatibility is likely due to the pistil‐controlled strength of pollen adherence to the stigma (Roda & Hopkins, ).…”

Darwin's ‘mystery of mysteries’: the role of sexual selection in plant speciation

“…Indeed, style length comparisons between selfer and outcrosser species revealed that outcrossers had longer styles (Diaz & Macnair, 1999; Runions & Geber, 2000), consistent with the idea that sexual selection is weaker in selfing species in comparison to outcrossers. Interspecific crosses between several SI and SC Arabidopsis species revealed that pollen of SI species could germinate on an SC stigma, while in the reciprocal crosses pollen of SC species did not germinate when the maternal plant was an SI species (Li et al ., 2018). This suggests that females of SI species are choosier than SC females in the signalling crosstalk between pollen and stigma.…”

“…In plants, whether sexual selection can lead to sexual trait divergence and the establishment of reproductive barriers has yet to be documented through empirical evidence. Divergent mate preferences in animals can act as a reproductive barrier (Boughman, 2001), and a similar process may take place in plants (Baek et al ., 2015; Li et al ., 2018). Nevertheless, the specificities of sexual selection in plants (the sexual mechanisms themselves, the diversity of life‐history traits, and the mating systems involved) may also contribute to the establishment of reproductive barriers that might be specific to plants.…”

Against the Odds: Hybrid Zones between Mangrove Killifish Species with Different Mating Systems

“…In fact, sperm from outcrossers and/or species with higher levels of sperm competition are more successful at fertilization [12][13][14]. The WISO hypothesis could, therefore, explain the patterns of UI often observed in the 'SI × SC rule' that, despite some exceptions [9,15], is commonly observed in plants [11,[16][17][18][19][20]. The 'SI × SC rule' has also been detected in some artificial interspecific crosses of Caenorhabditis nematodes, with males of outcrossing species having more competitive sperm than selfing males [14].…”