David M. Shuker

University of St Andrews, Saint Andrews, Scotland, United Kingdom

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Publications (128)531.23 Total impact

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    V Martel · D M Shuker · R A Boulton · D Damiens · G Boivin
    Full-text · Article · May 2016 · Entomologia Experimentalis et Applicata
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    Liam R Dougherty · Leigh W Simmons · David M Shuker
    Full-text · Article · Apr 2016 · Animal Behaviour
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    Liam R. Dougherty · David M. Shuker
    [Show abstract] [Hide abstract] ABSTRACT: Sexual selection has been shown to be the driving force behind the evolution of the sometimes extreme and elaborate genitalia of many species. Sexual selection may arise before and/or after mating, or vary according to other factors such as the social environment. However, bouts of selection are typically considered in isolation. We measured the strength and pattern of selection acting on the length of the male intromittent organ (or processus) in two closely related species of lygaeid seed bug: Lygaeus equestris and Lygaeus simulans. In both species, we measured both pre- and post-copulatory selection. For L. equestris, we also varied the experimental choice design used in mating trials. We found contrasting pre- and post-copulatory selection on processus length in L. equestris. Furthermore, significant pre-copulatory selection was only seen in mating trials in which two males were present. This selection likely arises indirectly due to selection on a correlated trait, as the processus does not interact with the female prior to copulation. In contrast, we were unable to detect significant pre- or post-copulatory selection on processus length in L. simulans. However, a formal meta-analysis of previous estimates of post-copulatory selection on processus length in L. simulans suggests that there is significant stabilising selection across studies, but the strength of selection varies between experiments. Our results emphasise that the strength and direction of sexual selection on genital traits may be multifaceted and can vary across studies, social contexts and different stages of reproduction. Significance statement Animal genitalia vary greatly in size and complexity across species, and selection acting on genital size and shape can be complex. In this study, we show that the length of the penis in two species of seed bug is subject to complex patterns of selection, varying depending on the social context and whether selection is measured before or after mating. In one of the species, we show unexpectedly that penis length is correlated with male mating success, despite the fact that the penis does not interact with the female prior to mating. Our results highlight the fact that genitalia may be subject to both direct and indirect selection at different stages of mating and that to fully understand the evolution of such traits we should combine estimates of selection arising from these multiple episodes.
    Full-text · Article · Mar 2016 · Behavioral Ecology and Sociobiology
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    Rebecca A Boulton · David M Shuker
    [Show abstract] [Hide abstract] ABSTRACT: Research over the past two decades suggests that polyandry is almost ubiquitous in nature. In some cases, females can gain direct and indirect (genetic) fitness benefits from mating with multiple males. However, when females accept superfluous matings without gaining any clear benefit, polyandry has been interpreted as a strategy to mitigate the costs of resisting or avoiding matings, a situation known as convenience polyandry. When females mate out of ‘convenience’ the mating rate is expected to be plastic, since females should mate at a higher rate when the costs of resistance or avoidance are high, for instance when males occur in high densities and/or around resources required by females such as oviposition sites. Here we show that remating in Nasonia vitripennis, a species of wasp that is largely monandrous in the wild but that evolves polyandry under laboratory culture, is dependent upon the availability of hosts for oviposition and upon male density. We found that females mated at a higher rate when male density was high but only if a suitable oviposition substrate was available. Outwardly this seems suggestive of convenience polyandry. However, females that remated under these conditions did not gain more time to oviposit than females that resisted superfluous matings. The results of this study highlight the importance of comprehensively assessing the costs and benefits of mating before attributing the observed behaviour to convenience polyandry. Furthermore, these results add to the growing body of evidence that the ecological context under which sexual interactions occur is critical to the economics of mating.
    Full-text · Article · Feb 2016 · Animal Behaviour
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    Full-text · Dataset · Dec 2015
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    [Show abstract] [Hide abstract] ABSTRACT: Many organisms monitor the annual change in day-length and use this information for the timing of their seasonal response. However, the molecular mechanisms underlying photoperiodic timing are largely unknown. The wasp Nasonia vitripennis is an emerging model organism that exhibits a strong photoperiodic response: short autumnal days experienced by females lead to the induction of developmental arrest (diapause) in their progeny, allowing winter survival of the larvae. How female Nasonia control the developmental trajectory of their offspring is unclear. Here we took advantage of the recent discovery that DNA methylation is pervasive in Nasonia, and tested its role in photoperiodism. We used reduced representation bisulfite sequencing (RRBS) to profile DNA methylation in adult female wasps subjected to different photoperiods, and identified substantial differential methylation at the single base level. We also show that knocking-down DNA methyltransferase 1a (Dnmt1a), Dnmt3, or blocking DNA methylation pharmacologically, largely disrupts the photoperiodic diapause response of the wasps. To our knowledge, this is the first example for a role of DNA methylation in insect photoperiodic timing.
    Full-text · Article · Dec 2015 · Genome Research
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    Fhionna R Moore · David M Shuker · Liam R Dougherty
    [Show abstract] [Hide abstract] ABSTRACT: The vertebrate stress response has been shown to suppress investment in reproductive and immune function and may also lead to a reduced investment in the production of secondary sexual traits. However, it has been difficult to model roles of stress in sexual selection due to the inconsistent results seen in empirical studies testing for the effect of stress on the expression of secondary sexual traits. We conducted a phylogenetically controlled meta-analysis of published associations between physiological correlates of stress and sexual signaling in vertebrates in order to identify any consistent patterns. Our analysis included signaling in both males and females, 4 stress measures, and 4 categories of sexually selected traits (vocalizations, traits that varied in size, traits that varied in coloration, and opposite-sex preference). Across 38 studies of 26 species, there was no significant relationship between physiological correlates of stress and the expression of sexual signals. Mean effect size, however, varied significantly across the 4 types of sexually selected trait. We propose development of a model that incorporates the nuanced effects of species ecology, trait type, ecological context, and the complex nature of the physiological stress response, on the expression of sexually selected traits.
    Full-text · Article · Nov 2015 · Behavioral Ecology
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    [Show abstract] [Hide abstract] ABSTRACT: Linking the evolution of the phenotype to the underlying genotype is a key aim of evolutionary genetics and is crucial to our understanding of how natural selection shapes a trait. Here we consider the genetic basis of sex allocation behaviour in the parasitoid wasp Nasonia vitripennis using a transcriptomics approach. Females allocate offspring sex in line with Local Mate Competition (LMC) theory. Female-biased sex ratios are produced when one or few females lay eggs on a patch. As the number of females contributing offspring to a patch increases, less female-biased sex ratios are favoured. We contrasted the transcriptomic responses of females as they oviposit under conditions known to influence sex allocation: foundress number (a social cue) and the state of the host (parasitised or not). We found, that when females encounter other females on a patch, or assess host quality with their ovipositors, the resulting changes in sex allocation is not associated with significant changes in whole-body gene expression. We also found that the gene expression changes produced by females, as they facultatively allocate sex in response to a host cue and a social cue, are very closely correlated. We expanded the list of candidate genes associated with oviposition behaviour in Nasonia, some of which may be involved in fundamental processes underlying the ability to facultatively allocate sex, including sperm storage and utilisation.
    Full-text · Article · Oct 2015 · G3-Genes Genomes Genetics
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    Liam R Dougherty · David M Shuker
    [Show abstract] [Hide abstract] ABSTRACT: The male intromittent organ of the seed bug Lygaeus simulans ends in a long, sclerotized structure which is used to transfer sperm during mating. Observations suggest that this structure becomes brittle and is liable to breakage after being artificially exposed to the air for an extended period of time. In this study we investigate the frequency of intromittent organ breakage in L. simulans. We first examined the intromittent organ of a sample of males that mated once, and found that breakage was rare. We hypothesised that breakages are likely to be more frequent if a male is able to mate multiple times, and so we next paired males with a female for 21 days in order to provide the opportunity for multiple mating. Almost a quarter (22.5%) of these males exhibited signs of genital breakage. The point of breakage varied: for six males only the tip of the structure (around 6% of its length) was missing, whereas for three males over 50% of the structure was missing. However we were unable to locate any fragments of male genitalia in the reproductive tracts of any females that came into contact with these males. This suggests that breakages do not necessarily occur during mating itself, but instead probably occur as the intromittent organ is being retracted into the genital capsule following mating. In this species breakage may not significantly reduce male reproductive fitness as sperm transfer may still be possible.
    Full-text · Article · Sep 2015 · European Journal of Entomology
  • David M. Shuker
    No preview · Article · Sep 2015
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    Nicola Cook · Bart A Pannebakker · Eran Tauber · David M. Shuker
    [Show abstract] [Hide abstract] ABSTRACT: Abstract The role of epigenetics in the control and evolution of behavior is being increasingly recognized. Here we test whether DNA methylation influences patterns of adaptive sex allocation in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate offspring sex broadly in line with local mate competition (LMC) theory. However, recent theory has highlighted how genomic conflict may influence sex allocation under LMC, conflict that requires parent-of-origin information to be retained by alleles through some form of epigenetic signal. We manipulated whole-genome DNA methylation in N. vitripennis females using the hypomethylating agent 5-aza-2′-deoxycytidine. Across two replicated experiments, we show that disruption of DNA methylation does not ablate the facultative sex allocation response of females, as sex ratios still vary with cofoundress number as in the classical theory. However, sex ratios are generally shifted upward when DNA methylation is disrupted. Our data are consistent with predictions from genomic conflict over sex allocation theory and suggest that sex ratios may be closer to the optimum for maternally inherited alleles.
    Full-text · Article · Aug 2015
  • Gethin M. V. Evans · Toby Nowlan · David M. Shuker
    [Show abstract] [Hide abstract] ABSTRACT: Theory suggests that, under some circumstances, sexual conflict over mating can lead to divergent sexually antagonistic coevolution among populations for traits associated with mating, and that this can promote reproductive isolation and hence speciation. However, sexual conflict over mating may also select for traits (e.g. male willingness to mate) that enhance gene flow between populations, limiting population divergence. In the present study, we compare pre- and post-mating isolation within and between two species characterized by male–female conflict over mating rate. We quantify sexual isolation among five populations of the seed bug Lygaeus equestris collected from Italy and Sweden, and two replicates of a population of the sister-species Lygaeus simulans, also collected from Italy. We find no evidence of reproductive isolation amongst populations of L. equestris, suggesting that sexual conflict over mating has not led to population divergence in relevant mating traits in L. equestris. However, there was strong asymmetric pre-mating isolation between L. equestris and L. simulans: male L. simulans were able to mate successfully with female L. equestris, whereas male L. equestris were largely unable to mate with female L. simulans. We found little evidence for strong post-mating isolation between the two species, however, with hybrid F2 offspring being produced. Our results suggest that sexual conflict over mating has not led to population divergence, and indeed perhaps supports the contrary theoretical prediction that male willingness to mate may retard speciation by promoting gene flow.
    No preview · Article · Aug 2015 · Biological Journal of the Linnean Society
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    Full-text · Dataset · Jul 2015
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    Emily R. Burdfield-Steel · Sam Auty · David M. Shuker
    [Show abstract] [Hide abstract] ABSTRACT: There have been many potential explanations put forward as to why polyandry often persists despite the multiple costs it can inflict on females. One such explanation is avoidance of costs associated with mating with genetically incompatible males. Genetic incompatibility can be thought of as a spectrum from individuals that are genetically too similar (inbreeding) to those that are too dissimilar (outbreeding or hybridization). Here we look for evidence that the level of outbreeding influences the benefits of polyandry in the seed bug Lygaeus equestris. Our system allows us to test for benefits of polyandry at levels of genetic similarity ranging from full siblings to heterospecifics, both in terms of egg production and hatching success. We found that while outbreeding level appeared to have no effect on fitness for intraspecific matings, and polyandry did not appear to result in any increase in fertility or fecundity, hybridization with a closely related species, Lygaeus simulans, carried considerable fitness costs. However, these costs could be rescued with a single mating to a conspecific. Thus, polyandry may be beneficial in populations that co-occur with closely related species and where there is reproductive interference. However, within-species genetic incompatibility is unlikely to be the driving force behind polyandry in this species. Furthermore, the mechanism underlying this rescue of fertility remains unclear as manipulation of male cuticular hydrocarbon profile, a possible mechanism by which females can assess male identity, had no effect on female offspring production.
    Full-text · Article · Jul 2015 · Behavioral Ecology
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    E V Ginny Greenway · Liam R. Dougherty · David M. Shuker
    [Show abstract] [Hide abstract] ABSTRACT: Greenway et al. introduce the concept of mating failure, the failure to produce offspring. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Full-text · Article · Jun 2015 · Current Biology
  • E V Ginny Greenway · David M Shuker
    [Show abstract] [Hide abstract] ABSTRACT: Mating failure, characterised by the lack of production of offspring following copulation, is relatively common across taxa yet is little understood. It is unclear if mating failures are stochastic occurrences between incompatible mating partners or represent a persistent, meaningful phenotype on the part of one or other sex. Here we test this in the seed bug Lygaeus simulans, by sequentially mating families of males with randomly-allocated unrelated females and calculating the repeatability of mating outcome for each individual male and family. Mating outcome is significantly repeatable within individual males but not across full-sib brothers. We conclude that mating failure represents a consistent male-associated phenotype with low heritability in this species, affected by as yet undetermined environmental influences on males. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    No preview · Article · Jun 2015 · Journal of Evolutionary Biology
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    [Show abstract] [Hide abstract] ABSTRACT: It is now clear in many species that male and female genital evolution has been shaped by sexual selection. However, it has historically been difficult to confirm correlations between morphology and fitness, as genital traits are complex and manipulation tends to impair function significantly. In this study,we investigate the functional morphology of the elongate male intromittent organ (or processus) of the seed bug Lygaeus simulans, in two ways. We first use micro-computed tomography (micro-CT) and flash-freezing to reconstruct in high resolution the interaction between the male intromittent organ and the female internal reproductive anatomy during mating.We successfully trace the path of the male processus inside the female reproductive tract. We then confirm that male processus length influences sperm transfer by experimental ablation and show that males with shortened processi have significantly reduced post-copulatory reproductive success. Importantly, male insemination function is not affected by this manipulation per se.We thus present rare, direct experimental evidence that an internal genital trait functions to increase reproductive success and showthat, with appropriate staining, micro-CT is an excellent tool for investigating the functional morphology of insect genitalia during copulation.
    Full-text · Article · May 2015 · Proceedings of the Royal Society B: Biological Sciences
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    [Show abstract] [Hide abstract] ABSTRACT: Sex allocation theory has proved to be one the most successful theories in evolutionary ecology. However, its role in more applied aspects of ecology has been limited. Here we show how sex allocation theory helps uncover an otherwise hidden cost of neonicotinoid exposure in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate the sex of their offspring in line with Local Mate Competition (LMC) theory. Neonicotinoids are an economically important class of insecticides, but their deployment remains controversial, with evidence linking them to the decline of beneficial species. We demonstrate for the first time to our knowledge, that neonicotinoids disrupt the crucial reproductive behaviour of facultative sex allocation at sub-lethal, field-relevant doses in N. vitripennis. The quantitative predictions we can make from LMC theory show that females exposed to neonicotinoids are less able to allocate sex optimally and that this failure imposes a significant fitness cost. Our work highlights that understanding the ecological consequences of neonicotinoid deployment requires not just measures of mortality or even fecundity reduction among non-target species, but also measures that capture broader fitness costs, in this case offspring sex allocation. Our work also highlights new avenues for exploring how females obtain information when allocating sex under LMC. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
    Full-text · Article · Apr 2015 · Proceedings of the Royal Society of London. Series B, Containing papers of a Biological character. Royal Society (Great Britain)
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    [Show abstract] [Hide abstract] ABSTRACT: Reproductive interference arises when individuals of one species engage in reproductive activities with individuals of another, leading to fitness costs in one or both species. Reproductive interference (RI) therefore has two components. First, there must be mis-directed mating interactions. Second, there must be costs associated with these mis-directed interactions. Here we consider RI between four species of true bug in the family Lygaeidae, focusing in particular on the fitness consequences to Lygaeus equestris. The species we consider vary in their relationships with each other, including species in the same or different genus, and with or without natural overlap in their geographic ranges. First we show that inter-specific mating interactions, although not a certain outcome, are common enough to perhaps influence mating behaviour in these species (arising in up to 10 % of inter-specific pairings). Second, we show that reproductive interference can seriously reduce female fitness in L. equestris. Importantly, different species impose different costs of RI on L. equestris, with interactions with male Spilostethus pandurus inflicting fitness costs of similar magnitude to the costs of mating with con-specifics. On the other hand, mating interactions with male Oncopeltus fasciatus appear to have no effect on female fitness. In a follow-up experiment, when we allowed competition amongst just females of S. pandurus and L. equestris, the fitness of the latter was not reduced, arguing more strongly for the role of reproductive interference. However, in our final experiments under mass mating conditions with extended ecological interactions (including scope for competition for resources and cannibalism), the costs of RI were less apparent. Our data therefore suggest that the costs of RI will be context-specific and may act in concert with, or be swamped by, other ecological effects. We suggest that comparative studies of this sort that both mimic naturally occurring reproductive interference events, and also artificially generate new ones, will be necessary if we are to better understand the ecological and evolutionary significance of reproductive interference.
    Full-text · Article · Apr 2015 · Population Ecology
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    Liam R. Dougherty · David M Shuker
    Full-text · Article · Mar 2015 · Behavioral Ecology

Publication Stats

2k Citations
531.23 Total Impact Points

Institutions

  • 2009-2015
    • University of St Andrews
      • School of Biology
      Saint Andrews, Scotland, United Kingdom
  • 2003-2010
    • The University of Edinburgh
      • • Institute of Evolutionary Biology
      • • Institute of Cell Biology
      Edinburgh, Scotland, United Kingdom
  • 2008
    • Manchester Metropolitan University
      Manchester, England, United Kingdom
  • 2004
    • University of Stirling
      • Department of Biological and Environmental Sciences
      Stirling, Scotland, United Kingdom
  • 2001
    • University of Nottingham
      Nottigham, England, United Kingdom