Abstract

Darwin was the first to recognize that sexual selection is a strong evolutionary force. Exaggerated traits allow same-sex individuals to compete over access to mates and provide a mechanism by which mates are selected. It is relatively easy to appreciate how inter- and intrasexual selection work in organisms with the sensory capabilities to perceive physical or behavioural traits that signal mate quality or mate compatibility, and to assess the relative quality of competitors. It is therefore not surprising that most studies of sexual selection have focused on animals with separate sexes and obvious adaptations that function in the context of reproductive competition. Yet, many sexual organisms are both male and female at the same time, often lack sexual dimorphism and never come into direct contact at mating. How does sexual selection act in such species, and what can we learn from them? Here, we address these questions by exploring the potential for sexual selection in simultaneous hermaphrodites, sperm- and broadcast spawners, plants and fungi. Our review reveals a range of mechanisms of sexual selection, operating primarily after gametes have been released, which are common in many of these groups and also quite possibly in more familiar (internally fertilizing and sexually dimorphic) organisms.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.

Highlights

  • In The descent of man, and selection in relation to sex Darwin [1] wrote that ‘In the lowest classes the two sexes are not rarely united in the same individual, and secondary sexual characters cannot be developed. [. . .] it is almost certain that these animals have too imperfect senses and much too low mental powers to feel mutual rivalry, or to appreciate each other’s beauty or other attractions’ ( p. 321)

  • Simultaneous hermaphrodites are not subjected to sexual selection

  • As we show in §§4 and 5, an increasing body of evidence from these systems challenges this assumption by demonstrating a range of putative mechanisms of sexual selection moderated exclusively by interactions operating after gamete release

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Summary

Introduction

In The descent of man, and selection in relation to sex Darwin [1] wrote that ‘In the lowest classes the two sexes are not rarely united in the same individual, and secondary sexual characters cannot be developed. [. . .] it is almost certain that these animals have too imperfect senses and much too low mental powers to feel mutual rivalry, or to appreciate each other’s beauty or other attractions’ ( p. 321). From the beginning the study of sexual selection has been biased towards the usual suspects: sexually dimorphic, internally fertilizing animals. It took the widespread use of DNA fingerprinting technologies to unequivocally determine paternity before the active role of females in mating was truly appreciated (nicely summarized in Birkhead’s book [3]). Unlike the more conventional study organisms, all or most selection acts after the gametes have been released They include many simultaneous hermaphroditic animals in which mating partners interact directly, spermcasters and broadcast spawners as well as wind-pollinated plants that never meet during reproduction, plants that require a third ‘force’ (i.e. pollinators), and the immensely diverse fungi, including yeasts, moulds and mushrooms. We conclude by arguing that the lessons learned from moving out of one’s comfort zone and venturing into the lesser-known realms of sexual selection can provide critical insights into the mechanisms of (gamete-level) sexual selection in more familiar taxonomic groups

When you are both male and female
When partners do not interact directly
When a third force is needed
Fungi do it too
Findings
Concluding remarks
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