The role of sexual selection in flowering plant origin and evolution and the potential significance of female competition and selection in ovules

Abstract

Ever since Erasmus and Charles Darwin laid down the foundations of the concept, sexual selection has largely been regarded as a matter of male competition and female selection. While their role in plant evolution and the elusive origin of flowering plants has largely been neglected in contrast to the situation with animals, there is a growing body of evidence accumulated over the past 50 years supporting the hypothesis that, together with the flower and the carpel, increased pollination has led to an intensification of the competition between the fittest (and faster) pollen tubes and their selection by the surrounding maternal tissue. In contrast, the potential role of female competition was historically seldom considered but started to re-emerge a decade ago in both animal and plant evolution. Here, I review a large body of the vast embryological literature to re-evaluate unusual developmental traits in the plant female germline, traditionally considered as teratological occurrences of mere systematic interest, in the light of the current phylogenetic framework for flowering plants. After a summary of the basic tenets of sexual selection and the role of male competition and maternal selection in shaping plant evolution and diversity, I show how recent insights into the deepest nodes of flowering plant phylogeny and confirmation of their systematic relationships over the past 30 years have led to major shifts in our understanding of the reproductive biology of their most recent common ancestor. I also show that a re-evaluation of these unusual developmental traits in the female germline, especially in early-diverging lineages of flowering plants, may potentially be correlated with some floral structural traits. On the basis of these results, I argue that there is circumstantial evidence for mechanisms of female intrasexual competition and selection in individual ovules of flowering plants that are similar to those between pollen tubes competing inside the carpel. I also argue that although they may have evolved independently multiple times in unrelated lineages, they could also be the ‘burning embers’ of plesiomorphic traits that would have been largely selected against after the evolution of their most recent common ancestor.