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      Flexible mate choice when mates are rare and time is short

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          Abstract

          Female mate choice is much more dynamic than we once thought. Mating decisions depend on both intrinsic and extrinsic factors, and these two may interact with one another. In this study, we investigate how responses to the social mating environment (extrinsic) change as individuals age (intrinsic). We first conducted a field survey to examine the extent of natural variation in mate availability in a population of threespine sticklebacks. We then manipulated the sex ratio in the laboratory to determine the impact of variation in mate availability on sexual signaling, competition, and mating decisions that are made throughout life. Field surveys revealed within season heterogeneity in mate availability across breeding sites, providing evidence for the variation necessary for the evolution of plastic preferences. In our laboratory study, males from both female-biased and male-biased treatments invested most in sexual signaling late in life, although they competed most early in life. Females became more responsive to courtship over time, and those experiencing female-biased, but not male-biased sex ratios, relaxed their mating decisions late in life. Our results suggest that social experience and age interact to affect sexual signaling and female mating decisions. Flexible behavior could mediate the potentially negative effects of environmental change on population viability, allowing reproductive success even when preferred mates are rare.

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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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            Variation in mate choice and mating preferences: a review of causes and consequences.

            The aim of this review is to consider variation in mating preferences among females. We define mating preferences as the sensory and behavioural properties that influence the propensity of individuals to mate with certain phenotypes. Two properties of mating preferences can be distinguished: (1) "preference functions'-the order with which an individual ranks prospective mates and (2) "choosiness'-the effort an individual is prepared to invest in mate assessment. Patterns of mate choices can be altered by changing the costs of choosiness without altering the preference function. We discuss why it is important to study variation in female mating behaviour and identify five main areas of interest: Variation in mating preferences and costs of choosiness could (1) influence the rate and direction of evolution by sexual selection, (2) provide information about the evolutionary history of female preferences, (3) help explain inter-specific differences in the evolution of secondary sexual characteristics, (4) provide information about the level of benefits gained from mate choice, (5) provide information about the underlying mechanisms of mate choice. Variation in mate choice could be due to variability in preference functions, degree of choosiness, or both, and may arise due to genetic differences, developmental trajectories or proximate environmental factors. We review the evidence for genetic variation from genetic studies of heritability and also from data on the repeatability of mate-choice decisions (which can provide information about the upper limits to heritability). There can be problems in interpreting patterns of mate choice in terms of variation in mating preferences and we illustrate two main points. First, some factors can lead to mate choice patterns that mimic heritable variation in preferences and secondly other factors may obscure heritable preferences. These factors are divided into three overlapping classes, environmental, social and the effect of the female phenotype. The environmental factors discussed include predation risk and the costs of sampling; the social factors discussed include the effect of male-male interactions as well as female competition. We review the literature which presents data on how females sample males and discuss the number of cues females use. We conclude that sexual-selection studies have paid far less attention to variation among females than to variation among males, and that there is still much to learn about how females choose males and why different females make different choices. We suggest a number of possible lines for future research.
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              Sexual selection and speciation.

              The power of sexual selection to drive changes in mate recognition traits gives it the potential to be a potent force in speciation. Much of the evidence to support this possibility comes from comparative studies that examine differences in the number of species between clades that apparently differ in the intensity of sexual selection. We argue that more detailed studies are needed, examining extinction rates and other sources of variation in species richness. Typically, investigations of extant natural populations have been too indirect to convincingly conclude speciation by sexual selection. Recent empirical work, however, is beginning to take a more direct approach and rule out confounding variables.
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                Author and article information

                Journal
                Ecol Evol
                Ecol Evol
                ece3
                Ecology and Evolution
                Blackwell Publishing Ltd
                2045-7758
                2045-7758
                September 2013
                22 July 2013
                : 3
                : 9
                : 2820-2831
                Affiliations
                [1 ]Department of Biological Sciences, University of Denver 102 Olin Hall, Denver, Colorado, 80208
                [2 ]Department of Zoology, Michigan State University 203 Natural Science Building, East Lansing, Michigan, 48824-1115
                [3 ]Centre for Ecology and Conservation, Biosciences, College of Life and Environmental Sciences, University of Exeter Penryn, Cornwall, TR10 9EZ, U.K
                [4 ]Department of Zoology, Michigan State University 203 Natural Science Building, East Lansing, Michigan 48824-1115
                Author notes
                Robin M. Tinghitella, Department of Biological Sciences, University of Denver, 102 Olin Hall, Denver, CO 80208. Tel: 303-871-3658; Fax: 303-871-3471; E-mail: robin.tinghitella@ 123456du.edu

                Funding Information This work was supported by Michigan State University, a grant from the BEACON Center for the Study of Evolution in Action to R. M. T. and J. W. B., an National Science Foundation (NSF) CAREER grant to J. W. B., and NSF IOS-0416808.

                Article
                10.1002/ece3.666
                3790532
                24101975
                0eecd555-106d-4c30-836a-af7cdad9075a
                © 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 15 May 2013
                : 11 June 2013
                : 12 June 2013
                Categories
                Original Research

                Evolutionary Biology
                age,mate choice,operational sex ratio,plasticity,stickleback
                Evolutionary Biology
                age, mate choice, operational sex ratio, plasticity, stickleback

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