How broad is the selfing syndrome? Insights from convergent evolution of gene expression across species and tissues in the Capsella genus

Abstract

The shift from outcrossing to selfing is one of the main evolutionary transitions in plants. It is accompanied by profound effects on reproductive traits, the so-called selfing syndrome. Because the transition to selfing also implies deep genomic and ecological changes, one also expects to observe a genomic selfing syndrome.We took advantage of the three independent transitions from outcrossing to selfing in the Capsella genus to characterize the overall impact of mating system change on RNA expression, in flowers but also in leaves and roots. We quantified the extent of both selfing and genomic syndromes, and tested whether changes in expression corresponded to adaptation to selfing or to relaxed selection on traits that were constrained in outcrossers.Mating system change affected gene expression in all three tissues but more so in flowers than in roots and leaves. Gene expression in selfing species tended to converge in flowers but diverged in the two other tissues. Hence, convergent adaptation to selfing dominates in flowers, whereas genetic drift plays a more important role in leaves and roots.The effect of mating system transition is not limited to reproductive tissues and corresponds to both adaptation to selfing and relaxed selection on previously constrained traits.

Parallel evolution of morphological and genomic selfing syndromes accompany the breakdown of heterostyly

“…In flowering plants, evolutionary transitions from outcrossing to predominant selfing are associated with a set of predictable changes in both morphological traits and genetic features of the genome. These convergent and parallel changes have been termed the ‘morphological selfing syndrome’ and the ‘genomic selfing syndrome’, respectively (Sicard & Lenhard, 2011; Cutter, 2019; Tsuchimatsu & Fujii, 2022; Zhang et al ., 2022). Species with moderate‐to‐high selfing rates often exhibit smaller flowers, a loss of herkogamy (stigma‐anther separation), reduced pollen production and pollinator rewards (e.g.…”

“…scent and nectar) compared with related outcrossing species and populations (Lloyd, 1965; Morgan & Barrett, 1989; Ritland & Ritland, 1989; Liao et al ., 2022; Zeng et al ., 2022). Concomitantly, persistent selfing usually results in changes in genetic parameters, including reduced heterozygosity and nucleotide diversity, increased linkage disequilibrium, accumulation of deleterious mutations and changes in gene expression (Charlesworth & Wright, 2001; Wright et al ., 2008; Glémin & Galtier, 2012; Barrett et al ., 2014; Shimizu & Tsuchimatsu, 2015; Zhang et al ., 2022). The evolution of morphological and genomic syndromes accompanying the transition from outcrossing to selfing can involve both adaptive and nonadaptive processes (Cutter, 2019; Rifkin et al ., 2019; Liao et al ., 2022; Tsuchimatsu & Fujii, 2022; Zhang et al ., 2022).…”

“…Concomitantly, persistent selfing usually results in changes in genetic parameters, including reduced heterozygosity and nucleotide diversity, increased linkage disequilibrium, accumulation of deleterious mutations and changes in gene expression (Charlesworth & Wright, 2001; Wright et al ., 2008; Glémin & Galtier, 2012; Barrett et al ., 2014; Shimizu & Tsuchimatsu, 2015; Zhang et al ., 2022). The evolution of morphological and genomic syndromes accompanying the transition from outcrossing to selfing can involve both adaptive and nonadaptive processes (Cutter, 2019; Rifkin et al ., 2019; Liao et al ., 2022; Tsuchimatsu & Fujii, 2022; Zhang et al ., 2022). However, determining the relative contributions of positive selection vs genetic drift underpinning morphological and genetic changes accompanying the evolution of selfing syndromes remains a challenge.…”

Can changes in ploidy drive the evolution to allogamy in a selfing species complex?

“…Intermediate states between both strategies – known as mixed mating systems – are ubiquitous in the wild (Goodwillie et al ., 2005). However, even though mixed mating is common (Aide, 1986; Barrett & Eckert, 1990), a transition towards selfing is expected to occur in most plant groups according to the evolutionary history of many taxa (Levin & Kerster, 1974; Zhang et al ., 2022). The adaptive consequences of selfing are known since classical works from Darwin and Fisher, who hypothesised a high spreading ability of self-fertilisation alleles because of the transmission of the whole genetic material and the independence of mates and pollination vectors, conferring a reproductive assurance and granting colonising opportunities (Darwin, 1877; Fisher, 1949; Lloyd, 1979; Lloyd, 1992; Holsinger, 1996).…”

Transcriptional convergence after repeated duplication of an amino acid transporter gene leads to the independent emergence of the black husk/pericarp trait in barley and rice

“…It remains unclear how phenotypic convergence may evolve independently from different genes; secondly, most associations between genomic convergence and phenotype adaptation were based on simple functional assumptions and lack empirical validation. Notably, these challenges also apply to other cases of phenotypic convergence currently reported in plants: metal toxicity tolerance in Arabidopsis (Preite et al ., 2019 ), seed colour in common bean (McClean et al ., 2018 ), the transition of outcrossing to selfing (Zhang et al ., 2022 ), perenniality in rice and sorghum (Hu et al ., 2003 ) and the development of plant shoot lateral organs (Naramoto et al ., 2019 ). The limited cases of convergence evolution indicate that our understanding of plant phenotypic evolution remains fragmentary.…”