Abstract

BackgroundWhile males usually benefit from as many matings as possible, females often evolve various methods of resistance to matings. The prevalent explanation for this is that the cost of additional matings exceeds the benefits of receiving sperm from a large number of males. Here we demonstrate, however, a strongly deviating pattern of polyandry.Methodology/Principal FindingsWe analysed paternity in the marine snail Littorina saxatilis by genotyping large clutches (53–79) of offspring from four females sampled in their natural habitats. We found evidence of extreme promiscuity with 15–23 males having sired the offspring of each female within the same mating period.Conclusions/SignificanceSuch a high level of promiscuity has previously only been observed in a few species of social insects. We argue that genetic bet-hedging (as has been suggested earlier) is unlikely to explain such extreme polyandry. Instead we propose that these high levels are examples of convenience polyandry: females accept high numbers of matings if costs of refusing males are higher than costs of accepting superfluous matings.

Highlights

  • In many species, females mate with more than one male to decrease their risk of only receiving sperm of poor quality or with low compatibility, to increase the probability of receiving sperm with sexually selected ‘‘good genes’’, to avoid inbreeding and to increase genetic diversity of the offspring [1,2,3,4,5,6]

  • Benefits of multiple matings are likely to decline with number of males owing to sampling effects, that is, additional matings will only marginally contribute with genes of better quality [2], unless postcopulatory mate-choice, such as cryptic female choice and sperm competition, is extremely effective [5]

  • We have shown that polyandry in the marine snail L. saxatilis is exceptionally high, among the highest ever recorded

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Summary

Introduction

Females mate with more than one male to decrease their risk of only receiving sperm of poor quality or with low compatibility, to increase the probability of receiving sperm with sexually selected ‘‘good genes’’, to avoid inbreeding and to increase genetic diversity of the offspring [1,2,3,4,5,6]. Benefits of matings are traded off against costs of additional matings [1] These are possible reasons why, in a majority of studied species, multiple mating means that a female mates with more than one but seldom more than a few males [3,7,8,9,10]. In some species of single-queen social insects and high-density flies, females mate ten times or more as many males than in other species [11,12,13], which may be explained by increased genetic variation among offspring [14], nutritional benefits [15–16, but see 17–18 for examples of where nuptial gifts instead have detrimental effects on females], or convenience polyandry where costs of resisting matings exceed the costs of additional matings [19]. The prevalent explanation for this is that the cost of additional matings exceeds the benefits of receiving sperm from a large number of males.

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