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      Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice

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          Abstract

          Sex-specific pheromones are known to play an important role in butterfly courtship, and may influence both individual reproductive success and reproductive isolation between species. Extensive ecological, behavioural and genetic studies of Heliconius butterflies have made a substantial contribution to our understanding of speciation. Male pheromones, although long suspected to play an important role, have received relatively little attention in this genus. Here, we combine morphological, chemical and behavioural analyses of male pheromones in the Neotropical butterfly Heliconius melpomene. First, we identify putative androconia that are specialized brush-like scales that lie within the shiny grey region of the male hindwing. We then describe putative male sex pheromone compounds, which are largely confined to the androconial region of the hindwing of mature males, but are absent in immature males and females. Finally, behavioural choice experiments reveal that females of H. melpomene, H. erato and H. timareta strongly discriminate against conspecific males which have their androconial region experimentally blocked. As well as demonstrating the importance of chemical signalling for female mate choice in Heliconius butterflies, the results describe structures involved in release of the pheromone and a list of potential male sex pheromone compounds.

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          Reproductive isolation caused by colour pattern mimicry.

          Speciation is facilitated if ecological adaptation directly causes assortative mating, but few natural examples are known. Here we show that a shift in colour pattern mimicry was crucial in the origin of two butterfly species. The sister species Heliconius melpomene and Heliconius cydno recently diverged to mimic different model taxa, and our experiments show that their mimetic coloration is also important in choosing mates. Assortative mating between the sister species means that hybridization is rare in nature, and the few hybrids that are produced are non-mimetic, poorly adapted intermediates. Thus, the mimetic shift has caused both pre-mating and post-mating isolation. In addition, individuals from a population of H. melpomene allopatric to H. cydno court and mate with H. cydno more readily than those from a sympatric population. This suggests that assortative mating has been enhanced in sympatry.
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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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              On the scent of speciation: the chemosensory system and its role in premating isolation.

              Chemosensory speciation is characterized by the evolution of barriers to genetic exchange that involve chemosensory systems and chemical signals. Here, we review some representative studies documenting chemosensory speciation in an attempt to evaluate the importance and the different aspects of the process in nature and to gain insights into the genetic basis and the evolutionary mechanisms of chemosensory trait divergence. Although most studies of chemosensory speciation concern sexual isolation mediated by pheromone divergence, especially in Drosophila and moth species, other chemically based behaviours (habitat choice, pollinator attraction) can also play an important role in speciation and are likely to do so in a wide range of invertebrate and vertebrate species. Adaptive divergence of chemosensory traits in response to factors such as pollinators, hosts and conspecifics commonly drives the evolution of chemical prezygotic barriers. Although the genetic basis of chemosensory speciation remains largely unknown, genomic approaches to chemosensory gene families and to enzymes involved in biosynthetic pathways of signal compounds now provide new opportunities to dissect the genetic basis of these complex traits and of their divergence among taxa.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                7 November 2017
                2017
                : 5
                : e3953
                Affiliations
                [1 ]Department of Zoology, University of Cambridge , Cambridge, Cambridgeshire, United Kingdom
                [2 ]Smithsonian Tropical Research Institute , Panama
                [3 ]Institute of Organic Chemistry, Technische Universität Braunschweig , Braunschweig, Germany
                [4 ]Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario , Bogota, Colombia
                [5 ]Department of Integrative Biology, University of Texas at Austin , Austin, TX, United States of America
                [6 ]Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München , Munich, Germany
                Article
                3953
                10.7717/peerj.3953
                5680698
                094b5a63-e491-4e9a-a6b8-ecfe0598458d
                ©2017 Darragh et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 19 May 2017
                : 2 October 2017
                Funding
                Funded by: Natural Environment Research Council
                Funded by: Doctoral Training Partnership
                Funded by: Manmohan Singh studentship
                Funded by: Junior Research Fellowship
                Funded by: European Research Council
                Award ID: 339873
                Funded by: Universidad del Rosario FIUR
                Award ID: QDN-DG001
                Funded by: COLCIENCIAS
                Award ID: FP44842-5-2017
                Funded by: Smithsonian Tropical Research Institute and NSF
                Award ID: DEB 1257689
                KD is funded by a Natural Environment Research Council Doctoral Training Partnership. SJ was funded by a Manmohan Singh studentship from St John’s College. RMM was funded by a Junior Research Fellowship at King’s College, Cambridge. CDJ and RMM are supported by a European Research Council grant number 339873 Speciation Genetics. MFG, CS and CPD were funded by the Universidad del Rosario FIUR grant QDN-DG001 and COLCIENCIAS (Grant FP44842-5-2017). WOM was supported by the Smithsonian Tropical Research Institute and NSF grant DEB 1257689. CRM was supported by a STRI Predoctoral Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Animal Behavior
                Entomology
                Evolutionary Studies

                heliconius,pheromone,sexual selection,mate choice,androconia,lepidoptera,reproductive isolation

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