High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

Abstract

The males and females of many dioecious plants differ in morphological (Dawson and Geber 1999; Barrett and Hough 2013; Tonnabel et al. 2017), physiological (Juvany and Munne-Bosch 2015), life-history (Delph 1999), and defence traits (Cornelissen and Stiling 2005). Ultimately, such sexual dimorphism must largely be due to differential gene expression between the sexes (Ellegren and Parsch 2007), but little is known about how sex-biased genes are recruited and how their expression evolves over time. We measured gene expression in leaves of males and females of ten species sampled across the South African Cape genus Leucadendron, which shows repeated changes in sexual dimorphism and includes the most extreme differences between males and females in flowering plants (Midgley 2010; Barrett and Hough 2013; Tonnabel et al. 2014). Even in the most dimorphic species in our sample, fewer than 2% of genes showed sex-biased gene expression (SBGE) in vegetative tissue, with surprisingly little correspondence between SBGE and vegetative dimorphism across species. The identity of sex-biased genes in Leucadendron was highly species-specific, with a rapid turnover among species. In animals, sex-biased genes often evolve more quickly than unbiased genes in their sequences and expression levels (Ranz et al. 2003; Khaitovich et al. 2005; Ellegren and Parsch 2007; Voolstra et al. 2007; Harrison et al. 2015; Naqvi et al. 2019), consistent with hypotheses invoking rapid evolution due to sexual selection. Our phylogenetic analysis in Leucadendron, however, clearly indicates that sex-biased genes are recruited from a class of genes with ancestrally rapid rates of expression evolution, perhaps due to low evolutionary or pleiotropic constraints. Nevertheless, we also find evidence for adaptive evolution of expression levels once sex bias evolves. Thus, although the expression of sex-biased genes is ultimately responsive to selection, high rates of expression evolution might usually predate the evolution of sex bias.