Lineage Selection and the Maintenance of Sex.

Damien M De Vienne,Tatiana Giraud,Pierre-Henri Gouyon

doi:10.1371/journal.pone.0066906

Abstract

Sex predominates in eukaryotes, despite its short-term disadvantage when compared to asexuality. Myriad models have suggested that short-term advantages of sex may be sufficient to counterbalance its twofold costs. However, despite decades of experimental work seeking such evidence, no evolutionary mechanism has yet achieved broad recognition as explanation for the maintenance of sex. We explore here, through lineage-selection models, the conditions favouring the maintenance of sex. In the first model, we allowed the rate of transition to asexuality to evolve, to determine whether lineage selection favoured species with the strongest constraints preventing the loss of sex. In the second model, we simulated more explicitly the mechanisms underlying the higher extinction rates of asexual lineages than of their sexual counterparts. We linked extinction rates to the ecological and/or genetic features of lineages, thereby providing a formalisation of the only figure included in Darwin's “The origin of species”. Our results reinforce the view that the long-term advantages of sex and lineage selection may provide the most satisfactory explanations for the maintenance of sex in eukaryotes, which is still poorly recognized, and provide figures and a simulation website for training and educational purposes. Short-term benefits may play a role, but it is also essential to take into account the selection of lineages for a thorough understanding of the maintenance of sex.

Highlights

Some traits are considered to be ‘‘evolutionary dead ends’’, initially developing due to short-term selective advantages, but resulting in lower rates of speciation or high rates of extinction in the long term, resulting in a species level selection [1,2,3]
For example, has been shown to maintain self-incompatibility in plants: the short-term advantages of self-fertilising individuals are offset by lineage selection, because only outcrossing species can be maintained in the long term [4]
It seems unlikely that sex is maintained by such a diversity of short-term causes. These findings suggest that selection may operate at a higher level, favouring lineages with constraints preventing the easy loss of sexual reproduction

Summary

Introduction

Some traits are considered to be ‘‘evolutionary dead ends’’, initially developing due to short-term selective advantages, but resulting in lower rates of speciation or high rates of extinction in the long term, resulting in a species level selection [1,2,3]. For example, has been shown to maintain self-incompatibility in plants: the short-term advantages of self-fertilising individuals are offset by lineage selection, because only outcrossing species can be maintained in the long term [4]. Another example is provided by sociality in spiders, which has short-term benefits, due to cooperation, that are counterbalanced by long-term disadvantages associated with inbreeding in small cooperative units [5]. Body size in mammals provides short-term benefits due to the effects of ecological dominance, but increases the risk of species extinction [7]

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