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      The costs and benefits of multiple mating in a mostly monandrous wasp

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          Abstract

          The taxonomically widespread nature of polyandry remains a puzzle. Much of the empirical work regarding the costs and benefits of multiple mating to females has, for obvious reasons, relied on species that are already highly polyandrous. However, this makes it difficult to separate the processes that maintain the current level of polyandry from the processes that facilitate its expression and initiated its evolution. Here we consider the costs and benefits of polyandry in Nasonia vitripennis, a species of parasitoid wasp that is “mostly monandrous” in the wild, but which evolves polyandry under laboratory culture conditions. In a series of six experiments, we show that females gain a direct fecundity and longevity benefit from mating multiply with virgin males. Conversely, mating multiply with previously mated males actually results in a fecundity cost. Sexual harassment may also represent a significant cost of reproduction. Harassment was, however, only costly during oviposition, resulting in reduced fecundity, longevity, and disrupted sex allocation. Our results show that ecological changes, in our case associated with differences in the local mating structure in the laboratory can alter the costs and benefits of mating and harassment and potentially lead to shifts in mating patterns.

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          Why do females mate multiply? A review of the genetic benefits.

          The aim of this review is to consider the potential benefits that females may gain from mating more than once in a single reproductive cycle. The relationship between non-genetic and genetic benefits is briefly explored. We suggest that multiple mating for purely non-genetic benefits is unlikely as it invariably leads to the possibility of genetic benefits as well. We begin by briefly reviewing the main models for genetic benefits to mate choice, and the supporting evidence that choice can increase offspring performance and the sexual attractiveness of sons. We then explain how multiple mating can elevate offspring fitness by increasing the number of potential sires that compete, when this occurs in conjunction with mechanisms of paternity biasing that function in copula or post-copulation. We begin by identifying cases where females use pre-copulatory cues to identify mates prior to remating. In the simplest case, females remate because they identify a superior mate and 'trade up' genetically. The main evidence for this process comes from extra-pair copulation in birds. Second, we note other cases where pre-copulatory cues may be less reliable and females mate with several males to promote post-copulatory mechanisms that bias paternity. Although a distinction is drawn between sperm competition and cryptic female choice, we point out that the genetic benefits to polyandry in terms of producing more viable or sexually attractive offspring do not depend on the exact mechanism that leads to biased paternity. Post-copulatory mechanisms of paternity biasing may: (1) reduce genetic incompatibility between male and female genetic contributions to offspring; (2) increase offspring viability if there is a positive correlation between traits favoured post-copulation and those that improve performance under natural selection; (3) increase the ability of sons to gain paternity when they mate with polyandrous females. A third possibility is that genetic diversity among offspring is directly favoured. This can be due to bet-hedging (due to mate assessment errors or temporal fluctuations in the environment), beneficial interactions between less related siblings or the opportunity to preferentially fertilise eggs with sperm of a specific genotype drawn from a range of stored sperm depending on prevailing environmental conditions. We use case studies from the social insects to provide some concrete examples of the role of genetic diversity among progeny in elevating fitness. We conclude that post-copulatory mechanisms provide a more reliable way of selecting a genetically compatible mate than pre-copulatory mate choice. Some of the best evidence for cryptic female choice by sperm selection is due to selection of more compatible sperm. Two future areas of research seem likely to be profitable. First, more experimental evidence is needed demonstrating that multiple mating increases offspring fitness via genetic gains. Second, the role of multiple mating in promoting assortative fertilization and increasing reproductive isolation between populations may help us to understand sympatric speciation.
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            The evolution of polyandry: multiple mating and female fitness in insects.

            Theory suggests that male fitness generally increases steadily with mating rate, while one or a few matings are sufficient for females to maximize their reproductive success. Contrary to these predictions, however, females of the majority of insects mate multiply. We performed a meta-analysis of 122 experimental studies addressing the direct effects of multiple mating on female fitness in insects. Our results clearly show that females gain directly from multiple matings in terms of increased lifetime offspring production. Despite a negative effect of remating on female longevity in species without nuptial feeding, the positive effects (increased egg production rate and fertility) more than outweigh this negative effect for moderate mating rates. The average direct net fitness gain of multiple mating was as high as 30-70%. Therefore, the evolutionary maintenance of polyandry in insects can be understood solely in terms of direct effects. However, our results also strongly support the existence of an intermediate optimal female mating rate, beyond which a further elevated mating rate is deleterious. The existence of such optima implies that sexual conflict over the mating rate should be very common in insects, and that sexually antagonistic coevolution plays a key role in the evolution of mating systems and of many reproductive traits. We discuss the origin and maintenance of nuptial feeing in the light of our findings, and suggest that elaborate and nutritional ejaculates may be the result of sexually antagonistic coevolution. Future research should aim at gaining a quantitative understanding of the evolution of female mating rates. Copyright 2000 The Association for the Study of Animal Behaviour.
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              Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology.

              W Hamilton (1967)
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                Author and article information

                Contributors
                rb78@st-andrews.ac.uk
                Journal
                Evolution
                Evolution
                10.1111/(ISSN)1558-5646
                EVO
                Evolution; International Journal of Organic Evolution
                John Wiley and Sons Inc. (Hoboken )
                0014-3820
                1558-5646
                April 2015
                08 April 2015
                : 69
                : 4 ( doiID: 10.1111/evo.2015.69.issue-4 )
                : 939-949
                Affiliations
                [ 1 ] School of BiologyUniversity of St Andrews United Kingdom
                Article
                EVO12636
                10.1111/evo.12636
                4989449
                25756346
                c651ddf3-a7a3-4de2-929a-efb0a50f5bdb
                © 2015 The Authors Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                Open access.

                History
                : 28 November 2014
                : 22 February 2015
                Page count
                Pages: 11
                Funding
                Funded by: NERC DTG studentship
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                evo12636
                April 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:18.08.2016

                Evolutionary Biology
                local mate competition,polyandry,sexual selection,sex allocation
                Evolutionary Biology
                local mate competition, polyandry, sexual selection, sex allocation

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