Slow evolution of sex‐biased genes in the reproductive tissue of the dioecious plant Salix viminalis

Abstract

The relative rate of evolution for sex‐biased genes has often been used as a measure of the strength of sex‐specific selection. In contrast to studies in a wide variety of animals, far less is known about the molecular evolution of sex‐biased genes in plants, particularly in dioecious angiosperms. Here, we investigate the gene expression patterns and evolution of sex‐biased genes in the dioecious plant Salix viminalis. We observe lower rates of sequence evolution for male‐biased genes expressed in the reproductive tissue compared to unbiased and female‐biased genes. These results could be partially explained by the lower codon usage bias for male‐biased genes leading to elevated rates of synonymous substitutions compared to unbiased genes. However, the stronger haploid selection in the reproductive tissue of plants, together with pollen competition, would also lead to higher levels of purifying selection acting to remove deleterious variation. Future work should focus on the differential evolution of haploid‐ and diploid‐specific genes to understand the selective dynamics acting on these loci.

Sex‐biased gene expression in flowers, but not leaves, reveals secondary sexual dimorphism in Populus balsamifera

“…Although Darolti et al . () suggested that haploid selection of genes expressed in gametes may be responsible for stronger purifying selection and lower dN/dS, we found that the values of dN/dS for genes with pollen‐limited expression did not differ from those of unbiased genes. Several studies have revealed evidence for positive selection driving the evolution of sex‐biased genes in animals (Pröschel et al ., ; Baines et al ., ; Dorus et al ., ; Grath & Parsch, ; Harrison et al ., ), and two studies found evidence for positive selection in sex‐biased genes of plants.…”

“…There are fewer comparisons of sex‐biased gene expression across reproductive and vegetative tissues in dioecious plants. In Silene latifolia , 17% of genes are differentially expressed in flowers, whereas < 2% are differentially expressed in leaves (Zemp et al ., ), and, in Salix viminalis , 43% of genes in catkins are differentially expressed, whereas only 0.09% of genes exhibit sex bias in leaves (Darolti et al ., ). In the current study of P. balsamifera , we found that 36% of genes expressed in catkins showed sex bias, whereas 0.003% showed sex bias in leaves.…”

“…This pattern of sex‐biased expression stands in contrast with that of two insect‐pollinated dioecious species, Silene latifolia and Asparagus officinalis , which exhibited more male‐biased genes in flowers (Harkess et al ., ; Zemp et al ., ). In Salix viminalis , which is both wind and insect pollinated, the numbers of male‐ and female‐biased genes were roughly even (Darolti et al ., ). The differences in the direction of sex bias among these studies may partially result from the greater number of secondary sexual traits associated with insect attraction, which, in turn, may be more strongly influenced by sexual selection (Moore & Pannell, ; Delph & Herlihy, ) than are wind‐pollinated poplar flowers.…”

“…Recent studies in plants have shown that most sex‐limited and sex‐biased genes do not reside on the sex chromosomes (Harkess et al ., ; Zemp et al ., ; Pucholt et al ., ). However, in both Silene latifolia and Salix viminalis , genes on sex chromosomes more commonly exhibit sex‐biased expression than do autosomal genes (Zemp et al ., ; Darolti et al ., ), and, in Salix , Asparagus and Silene , sex‐biased gene expression is more common in floral tissues (Liu et al ., ; Harkess et al ., ; Zemp et al ., ; Pucholt et al ., ) than in vegetative tissues (Hough et al ., ; Robinson et al ., ; Zemp et al ., ; Pucholt et al ., ; Darolti et al ., ; but see Zluvova et al ., ). For example, in Silene latifolia flowers, ~17% of genes exhibit sex‐biased expression, but < 2% of genes are sex biased in leaf tissues (Zemp et al ., ).…”

Not all sex‐biased genes are the same

“…Unlike most similar studies in other organisms, including dioecious willows (Darolti et al ., ), there were twice as many female‐biased genes compared to male‐biased genes. This result demonstrates the usefulness of studying species from many domains of life, reproductive modes, and life histories.…”