Gene expression and pollen performance indicate altered postmating selection between Solanum species with different mating systems

Abstract

Postmating prezygotic (PMPZ) traits play an important role in mating success, especially in species where gametes from multiple males compete. Despite this, the effect of mating system transitions, and attendant shifts in the intensity of sexual selection, on specific PMPZ traits and their underlying loci is still poorly understood. Here we assessed differences in pollen PMPZ traits and tissue-specific gene expression (in leaf, pollen, and style) between two closely related plant species with different mating systems--Solanum lycopersicum (selfing) & Solanum pennellii (outcrossing). We focused on species differences in loci with known roles in pollen tube growth rate, including pectin methylesterases (PMEs) and their inhibitors (PMEIs), and in- vitro & in-vivo pollen tube growth rates. Among the gene expression differences observed between species, we found that the expression domain of pollen-biased genes was much narrower in the selfing species S. lycopersicum compared to the outcrossing species S. pennellii, including for most reproductive PMEs and PMEIs. In addition, S. pennellii had faster pollen tube growth rates in-vivo, while S. lycopersicum had faster in-vitro pollen tube growth rates. We propose that the lower expression of pollen tube development genes in S. lycopersicum style tissue, and reduced in-vivo pollen performance, is a result of reduced allocation to stylar mechanisms that modulate pollen tube growth, potentially consistent with relaxed selection on cryptic female choice in the selfing species. Article SummaryThis study investigates the evidence for differential postmating sexual selection in plants, by analyzing reproductive gene expression and pollen performance in two Solanum species with different mating systems. It finds that species differ systematically in pollen tube growth rates, and that pollen ( male)-biased genes have higher secondary expression in stylar ( female) tissues in the outcrossing species. These observations are consistent with the outcrossing species experiencing stronger selection on female reproductive tract traits that influence male postmating performance. This study evaluates key expectations of sexual selection on postmating traits but does so in the uncommon context of flowering plants.