Pollinator abundance shapes sexual selection in an angiosperm

Abstract

Sexual selection is a cornerstone of evolutionary biology potentially operating in all sexually-reproducing organisms. Modern developments in the field revealed that this selective force extends beyond Darwins initial focus on access to mates in terms of competition for access to gametes of the other sex. Despite its presumed universality, sexual selection theory remains largely untested in plants compared to animals. This gap may partly stem from challenges in quantifying sexual selection using approaches that account for a critical plant-specific factor: the reliance on pollinators as third-party agents for accessing mates. Here, we quantified sexual selection along consecutive episodes of selection in the hermaphroditic plant Brassica rapa by integrating the monitoring of pollinator movements with genetic paternity analyses in experimental populations. Our approach identifies pollen competition for ovules as the primary arena for sexual selection in B. rapa. Darwinian competition for access to mates constitutes a secondary force, and was stronger in the male compared to the female sex function, as predicted by classic theory. Importantly, experimentally induced variation in pollinator abundance modulated the balance between pre- and post-pollination sexual selection. Under reduced pollinator abundance, the opportunity for selection on mate acquisition increased. Crucially, we demonstrate that ignoring pollinator movements among plants leads to erroneous quantification of pre-pollination sexual selection. We argue that a unifying theory of sexual selection requires a more comprehensive quantification of pre- and post-pollination episodes of selection, taking into account the specificities of gamete transfer in plants.