Abstract
Differences between males and females are usually more subtle in dioecious plants than animals, but strong sexual dimorphism has evolved convergently in the South African Cape plant genus Leucadendron. Such sexual dimorphism in leaf size is expected largely to be due to differential gene expression between the sexes. We compared patterns of gene expression in leaves among 10 Leucadendron species across the genus. Surprisingly, we found no positive association between sexual dimorphism in morphology and the number or the percentage of sex-biased genes (SBGs). Sex bias in most SBGs evolved recently and was species specific. We compared rates of evolutionary change in expression for genes that were sex biased in one species but unbiased in others and found that SBGs evolved faster in expression than unbiased genes. This greater rate of expression evolution of SBGs, also documented in animals, might suggest the possible role of sexual selection in the evolution of gene expression. However, our comparative analysis clearly indicates that the more rapid rate of expression evolution of SBGs predated the origin of bias, and shifts towards bias were depleted in signatures of adaptation. Our results are thus more consistent with the view that sex bias is simply freer to evolve in genes less subject to constraints in expression level.
Highlights
Dimorphism in different traits is highly correlated across species of Leucadendron, and reaches extremes in species such as L. rubrum, whose females grow leaves that are on average 13 times larger than males, and in which males produce 75 43 times more inflorescences per stem (Figure 1 A, Bond and Midgley, 1988). 44 45 The possibility of sexual selection occuring in plants has long been controversial, evolutionary processes that act to increase mating success are well documented in plants (Moore and Pannell, 2011)
Interestingly, in certain species of Leucadendron with specialised pollinators, male and female inflorescences and their surrounding leaves differ in attractive cues and provide the same pollinator with different rewards (Hemborg and Bond, 2005), pointing to a further link between reproductive structures and vegetative morphology. 75 The morphological and physiological differences between males and females of sexually dimorphic species are likely to depend on differences in gene expression, either because of divergence in gene content at loci linked to sex or due to differences in gene expression, at autosomal loci (Ellegren and Parsch, 2007; Mank, 2009; Zemp et al, 2016)
We based our analysis on transcriptomes sequenced from species sampled from all major clades of the genus Leucadendron, recapturing variation generated over several tens of millions of years of evolution during the genus’ radiation (Sauquet et al, 2009), which is reflected in up to 3.7% sequence differences at synonymous sites between species
Summary
Sexual dimorphism is common in dioecious plants, affecting a broad range of physiological (Juvany and Munné-Bosch, 2015), morphological (Barrett and Hough, 2013; Dawson and Geber, 1999; Tonnabel et al, 2017), life-history (Delph, 1999), and defence traits (Cornelissen and Stiling, 2005), yet sexual dimorphism in plants tends to be less marked than it is in animals (Barrett and Hough, 2013; Lloyd and Webb, 1977; Moore and Pannell, 2011). Sexual dimorphism in morphology and gene expression may occur in non-reproductive tissues and traits Such 'secondary' sex characters may reflect distinct reproductive strategies in terms of physiology and ecology that are associated with the ancient, primary differences of male and female gametes (Lloyd and Webb, 1977). The male-biased genes in reproductive tissues of many animals, but sometimes female-biased genes, may show elevated rates of amino acid substitution and elevated rates of gene expression divergence (Ellegren and Parsch, 2007; Harrison et al, 2015; Khaitovich et al, 2005; Naqvi et al, 2019; Ranz et al, 2003; Voolstra et al, 2007) This is probably due to frequent adaptive sweeps in cases such as Drosophila (Grath and Parsch, 2016). Our study represents the first phylogenetic analysis of the evolution of sex-biased gene expression for plants, and our results urge caution in invoking adaptive evolution as the sole reason for high rates of expression evolution observed for sex-biased genes
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