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Biased learning affects mate choice in a butterfly.

ABSTRACT: Early acquisition of mate preferences or mate-preference learning is associated with signal diversity and speciation in a wide variety of animal species. However, the diversity of mechanisms of mate-preference learning across taxa remains poorly understood. Using the butterfly Bicyclus anynana we uncover a mechanism that can lead to directional sexual selection via mate-preference learning: a bias in learning enhanced ornamentation, which is independent of preexisting mating biases. Naïve females mated preferentially with wild-type males over males with enhanced wing ornamentation, but females briefly exposed to enhanced males mated significantly more often with enhanced males. In contrast, females exposed to males with reduced wing ornamentation did not learn to prefer drab males. Thus, we observe both a learned change of a preexisting mating bias, and a bias in ability to learn enhanced male ornaments over reduced ornaments. Our findings demonstrate that females are able to change their preferences in response to a single social event, and suggest a role for biased learning in the evolution of visual sexual ornamentation.

SUBMITTER: Westerman EL

PROVIDER: S-EPMC3390860 | biostudies-literature | 2012 Jul

REPOSITORIES: biostudies-literature

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Biased learning affects mate choice in a butterfly.

Westerman Erica L EL Hodgins-Davis Andrea A Dinwiddie April A Monteiro Antónia A

Proceedings of the National Academy of Sciences of the United States of America 20120611 27

Early acquisition of mate preferences or mate-preference learning is associated with signal diversity and speciation in a wide variety of animal species. However, the diversity of mechanisms of mate-preference learning across taxa remains poorly understood. Using the butterfly Bicyclus anynana we uncover a mechanism that can lead to directional sexual selection via mate-preference learning: a bias in learning enhanced ornamentation, which is independent of preexisting mating biases. Naïve female ...[more]

PMID: 22689980

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Project description:Three experiments were conducted examining whether an artificially selected "gold" color variant in female "models" affects mate choice copying behavior in sailfin mollies (Poecilia latipinna). Experiment I consisted of a pair of female preference assays, first assessing preference for male body size, followed by a mate choice copying assay that paired a model female with the smaller, non-preferred male from the initial preference test. Female subjects were divided into three groups that used either a wildtype female model, an artificially selected "gold" variant (cultivated within the aquarium fish trade) model, or control wherein no model was presented. Results showed females consistently copied the model's choice, switching preferences from the larger to smaller male when paired with a model regardless of color. In the second experiment wildtype females were presented with a pair of size-matched dummy males both of which paired with model females (one gold and the other wild type). Subjects consistently preferred the male previously paired with the gold- over the male with the wildtype-model, suggesting pre-existing sensory/perceptual biases may have affected their mate choice copying behavior. Previous studies have offered evidence for the spread of novel traits in males via sensory exploitation. However, these results indicate such biases may influence courtship behavior in circumstances where the novel trait is expressed in females as well. For the third experiment, wildtype females were presented with a choice between gold vs wildtype dummy males, the results of which revealing significant preferences for gold. In a follow-up assay pairing a wild type model with the non-preferred wildtype male, females maintained their preference for gold males despite the conflicting social driver of mate choice copying. These data offer evidence for the existence of a perceptual/cognitive bias in the context of mate choice copying, favoring the gold phenotype and/or novelty in general.

Project description:BackgroundMetapopulation persistence in fragmented landscapes is assured by dispersal of individuals between local populations. In this scenario the landscape topography, although usually neglected, may have an important role in shaping dispersal throughout the matrix separating habitat patches. Due to inter-sexual differences in optimal reproductive strategies, i.e., males maximizing the number of mating opportunities and females maximizing the offspring survival chances, topography-related constraints are expected to exert a different effect on male and female dispersal behaviour. We tested sex-biased topography effects on butterfly dispersal, with the following hypotheses: (1) females are constrained by topography in their movements and avoid hill crossing; (2) male dispersal is primarily driven by two-dimensional spatial structure of the habitat patches (i.e. their geometric locations and sizes) and little influenced by topography.MethodsFollowing intensive mark-recapture surveys of Maculinea (= Phengaris) nausithous and M. teleius within a landscape characterised by an alternation of hills and valleys, we investigated sex-specific patterns in their inter-patch movement probabilities derived with a multi-state recapture model. In particular, we (1) analysed the fit of dispersal kernels based on Euclidean (= straight line) vs. topography-based (= through valley) distances; (2) compared movement probabilities for the pairs of patches separated or not by topographic barriers; and (3) tested the differences in the downward and upward movement probabilities within the pairs of patches.ResultsEuclidean distances between patches proved to be a substantially stronger predictor of inter-patch movement probabilities in males, while inter-patch distances measured along valleys performed much better for females, indicating that the latter tend to predominantly follow valleys when dispersing. In addition, there were significantly lower probabilities of movements across hills in females, but not in males.ConclusionsBoth above results provide support for the hypothesis that topography restricts dispersal in females, but not in males. Since the two sexes contribute differently to metapopulation functioning, i.e., only female dispersal can result in successful (re)colonisations of vacant patches, the topography effects exerted on females should be considered with particular attention when landscape management and conservation actions are designed in order to maintain the functional connectivity of metapopulation systems.

Project description:Males of many insects, including butterflies, produce mate-guarding devices, such as mating plugs, to prolong guarding and prevent future female matings in the male's absence. In a few butterflies, large external mate-guarding devices, that is, sphragides, occur. Gór et al. (Behaviour, 160, 2023 and 515-557) found conspicuously large size and morphological variation of mate-guarding devices within a single population of the potentially polyandrous Clouded Apollo (Parnassius mnemosyne, L.) butterfly. They termed the externally visible male-produced devices as Copulatory opening APpendices (CAP) consisting of small devices, termed small CAPs and the much larger shield (i.e. sphragis). Our aim was to reveal CAP replacement dynamics within females during their lifetime and to understand how male investment into small CAPs or shields was (i) related to CAP persistence on the female, that is securing paternity, (ii) associated with female quality, measured as size and (iii) with actual adult sex ratio. We investigated a univoltine Clouded Apollo population to estimate CAP replacement risks, using multistate survival models, in an extensive observational study through 6 years based on mark-recapture. Shields were the most frequent mate-guarding devices and were more persistent than small CAPs, often lasting for life, excluding future matings. Thus, most females bearing a shield were deprived of postcopulatory female choice, and the genetic variance in their offspring could be reduced compared to those bearing small CAPs, thus mating more often. The ratio of shields to all CAPs gradually decreased towards the end of the flight period. Males were more prone to produce a shield when mating females with wider thoraces and when the ratio of males (i.e. competition) was higher in the population. To our best knowledge, this is the first quantitative study to investigate potential factors on which male investment in mate-guarding devices may depend, and how the variation in these devices impacts CAP persistence on females.

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Biased learning affects mate choice in a butterfly.

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Biased learning affects mate choice in a butterfly.

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