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      Non‐visual cues and indirect strategies that enable discrimination of asymmetric mates

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          Abstract

          The postulates of developmental instability–sexual selection hypothesis is intensely debated among evolutionary biologists, wherein despite a large amount of empirical data, evidence for or against it has been largely inconclusive. A key assumption of this hypothesis is that animals assess symmetry in potential mates as an indicator of genetic quality (developmental stability), and consequently use this information to discriminate against those with higher asymmetries while choosing mates. However, the perceptional basis that must underlie such discriminatory behavior (is symmetry a signal or is symmetry signaled) is not clearly defined. It is also argued that since asymmetry levels in natural populations are very low, the low signal‐to‐noise ratio would make accurate assessment of symmetry both difficult and costly. Rather than attempting to validate this hypothesis or even as to whether animals assess mate symmetry, this review simply aims to examine the plausibility that animals perceive symmetry (directly or indirectly) and consequently discriminate against asymmetric mates in response to perceived irregularities during courtship. For this, we review mate choice and courtship literature to identify potential sensory cues that might advertise asymmetry or lead to discrimination of asymmetric individuals. Although signaling associated with mate choice is commonly multimodal, previous studies on asymmetry have mainly focused on visual perception. In the light of a recent study (Vijendravarma et al., 2022, Proceedings of the National Academy of Sciences of the United States of America, 119, e2116136119), this review attempts to balance this bias by emphasizing on non‐visual perception of asymmetry. In conclusion, we discuss the methodological challenges associated with testing the role of multimodal cues in detecting mate asymmetry, and highlight the importance of considering ecological, behavioral, and evolutionary aspects of animals while interpreting empirical data that test such hypothesis.

          Abstract

          We review how multimodal non‐visual cues can signal morphological asymmetry of potential mates during courtship in diverse species across taxa. We also discuss how extended phenotypes and mate choice copying aid females to indirectly assess and discriminate against asymmetric males. With the current emphasis on multimodal communication during courtship, this review is well timed to rekindle interest in the role of symmetry during mate choice.

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          Most cited references108

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          Fluctuating Asymmetry: Measurement, Analysis, Patterns

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            Potential disadvantages of using socially acquired information.

            The acquisition and use of socially acquired information is commonly assumed to be profitable. We challenge this assumption by exploring hypothetical scenarios where the use of such information either provides no benefit or can actually be costly. First, we show that the level of incompatibility between the acquisition of personal and socially acquired information will directly affect the extent to which the use of socially acquired information can be profitable. When these two sources of information cannot be acquired simultaneously, there may be no benefit to socially acquired information. Second, we assume that a solitary individual's behavioural decisions will be based on cues revealed by its own interactions with the environment. However, in many cases, for social animals the only socially acquired information available to individuals is the behavioural actions of others that expose their decisions, rather than the cues on which these decisions were based. We argue that in such a situation the use of socially acquired information can lead to informational cascades that sometimes result in sub-optimal behaviour. From this theory of informational cascades, we predict that when erroneous cascades are costly, individuals should pay attention only to socially generated cues and not behavioural decisions. We suggest three scenarios that might be examples of informational cascades in nature.
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              The role of chemical communication in mate choice.

              Chemical signals are omnipresent in sexual communication in the vast majority of living organisms. The traditional paradigm was that their main purpose in sexual behaviour was to coordinate mate and species recognition and thus pheromones were conserved in structure and function. In recent years, this view has been challenged by theoretical analyses on the evolution of pheromones and empirical reports of mate choice based on chemical signals. The ability to measure precisely the quantity and quality of chemicals emitted by single individuals has also revealed considerable individual variation in chemical composition and release rates, and there is mounting evidence that prospecting mates respond to this variation. Here, we review the evidence for pheromones as indicators of mate quality and examine the extent of their use in individual mate assessment. We begin by briefly defining the levels of mate choice--species recognition, mate recognition and mate assessment. We then explore the degree to which pheromones satisfy the key criteria necessary for their evolution and maintenance as cues in mate assessment; that is, they should exhibit variation across individuals within a sex and species; they should honestly reflect an individual's quality and thus be costly to produce and/or maintain; they should display relatively high levels of heritability. There is now substantial empirical evidence that pheromones can satisfy all these criteria and, while measurements of the actual metabolic cost of pheromone production remain to some degree lacking, trade-offs between pheromone production and various fitness-related characters such as growth rate, immunocompetence and longevity have been reported for a range of species. In the penultimate section, we outline the growing number of studies where the consequences of chemical-based mate assessment have been investigated, specifically focussing on the reported direct and genetic benefits accrued by the receiver. Finally, we highlight potential areas for future research and in particular emphasise the need for interdisciplinary research that combines exploration of chemical, physiological and behavioural processes to further our understanding of the role of chemical cues in mate assessment.
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                Author and article information

                Contributors
                roshankumar.vijendravarma@gmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                01 April 2022
                April 2022
                : 12
                : 4 ( doiID: 10.1002/ece3.v12.4 )
                : e8790
                Affiliations
                [ 1 ] Institut Curie – Centre de Recherche, Genetics and Developmental Biology Unit INSERM U934 / CNRS UMR3215 Paris France
                Author notes
                [*] [* ] Correspondence

                Roshan Kumar Vijendravarma, Université Paris Cité, Institut Jacques Monod, F‐75013 Paris, France.

                Email: roshankumar.vijendravarma@ 123456gmail.com

                Author information
                https://orcid.org/0000-0002-3274-0682
                https://orcid.org/0000-0002-2365-2103
                Article
                ECE38790
                10.1002/ece3.8790
                8975790
                6bb3f16d-9f29-45d2-a148-72e368c89e7b
                © 2022 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 May 2021
                : 16 March 2022
                Page count
                Figures: 3, Tables: 0, Pages: 12, Words: 9927
                Funding
                Funded by: Q‐life interdisciplinary grant
                Award ID: Q‐life ANR‐17‐CONV‐0005
                Funded by: European Research Council Advanced Grant , doi 10.13039/501100000781;
                Award ID: # 694677
                Categories
                Behavioural Ecology
                Review Article
                Review Articles
                Custom metadata
                2.0
                April 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.3 mode:remove_FC converted:01.04.2022

                Evolutionary Biology
                developmental instability,extended phenotype,fluctuating asymmetry,mate choice,mate choice copying,multimodal courtship,non‐visual cues,sexual selection

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