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      Quantifying inbreeding avoidance through extra-pair reproduction

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          Abstract

          Extra-pair reproduction is widely hypothesized to allow females to avoid inbreeding with related socially paired males. Consequently, numerous field studies have tested the key predictions that extra-pair offspring are less inbred than females’ alternative within-pair offspring, and that the probability of extra-pair reproduction increases with a female's relatedness to her socially paired male. However, such studies rarely measure inbreeding or relatedness sufficiently precisely to detect subtle effects, or consider biases stemming from failure to observe inbred offspring that die during early development. Analyses of multigenerational song sparrow ( Melospiza melodia) pedigree data showed that most females had opportunity to increase or decrease the coefficient of inbreeding of their offspring through extra-pair reproduction with neighboring males. In practice, observed extra-pair offspring had lower inbreeding coefficients than females’ within-pair offspring on average, while the probability of extra-pair reproduction increased substantially with the coefficient of kinship between a female and her socially paired male. However, simulations showed that such effects could simply reflect bias stemming from inbreeding depression in early offspring survival. The null hypothesis that extra-pair reproduction is random with respect to kinship therefore cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra-pair reproduction requires reevaluation given such biases.

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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 genetic basis of inbreeding depression.

            Data on the effects of inbreeding on fitness components are reviewed in the light of population genetic models of the possible genetic causes of inbreeding depression. Deleterious mutations probably play a major role in causing inbreeding depression. Putting together the different kinds of quantitative genetic data, it is difficult to account for the very large effects of inbreeding on fitness in Drosophila and outcrossing plants without a significant contribution from variability maintained by selection. Overdominant effects of alleles on fitness components seem not to be important in most cases. Recessive or partially recessive deleterious effects of alleles, some maintained by mutation pressure and some by balancing selection, thus seem to be the most important source of inbreeding depression. Possible experimental approaches to resolving outstanding questions are discussed.
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              Females increase offspring heterozygosity and fitness through extra-pair matings.

              Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality; however, the nature of these genetic benefits is debated. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes---'good genes'--or from interactions between the maternal and paternal genomes--'compatible genes'. Evidence for the latter process is accumulating: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding--measured as average heterozygosity--is a strong fitness predictor. Females should thus benefit from mating with genetically dissimilar males. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.
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                Author and article information

                Contributors
                Role: Associate Editor
                Role: Handling Editor
                Journal
                Evolution
                Evolution
                evo
                Evolution; International Journal of Organic Evolution
                Blackwell Publishing Ltd (Oxford, UK )
                0014-3820
                1558-5646
                January 2015
                03 December 2014
                : 69
                : 1
                : 59-74
                Affiliations
                [1 ]School of Biological Sciences, Institute of Biological and Environmental Sciences, Zoology Building, University of Aberdeen Tillydrone Avenue, Aberdeen, AB24 2TZ, Scotland
                [3 ]Department of Forest and Conservation Sciences, University of British Columbia Vancouver, BC, V6T 1Z4, Canada
                [4 ]Institute of Evolutionary Biology and Environmental Studies, University of Zurich Winterthurerstrasse 190, 8057, Zurich, Switzerland
                Author notes
                Article
                10.1111/evo.12557
                4312944
                25346331
                cf1c6fc7-c856-4549-9d07-4002dc816178
                © 2014 The Author(s). 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.

                History
                : 27 May 2014
                : 11 October 2014
                Categories
                Original Articles

                Evolutionary Biology
                inbreeding depression,kinship,mate choice,paternity,polyandry,relatedness
                Evolutionary Biology
                inbreeding depression, kinship, mate choice, paternity, polyandry, relatedness

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