David M Shuker

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

Are you David M Shuker?

Claim your profile

Publications (98)494.5 Total impact

  • Source
    [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.
    G3-Genes Genomes Genetics 10/2015; DOI:10.1534/g3.115.021220 · 3.20 Impact Factor
  • Source
    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.
    European Journal of Entomology 09/2015; 112(4). DOI:10.14411/eje.2015.098 · 0.98 Impact Factor
  • David M. Shuker ·

  • Source
    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.
    08/2015; 186(4):p. 000. DOI:10.1086/682950
  • 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.
    Biological Journal of the Linnean Society 08/2015; 116(4). DOI:10.1111/bij.12639 · 2.26 Impact Factor
  • Source

  • Source
    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.
    Behavioral Ecology 07/2015; 26(5):arv103. DOI:10.1093/beheco/arv103 · 3.18 Impact Factor
  • Source
    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.
    Current Biology 06/2015; 25(13-13):R534-R536. DOI:10.1016/j.cub.2015.02.058 · 9.57 Impact Factor
  • 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.
    Journal of Evolutionary Biology 06/2015; 28(8). DOI:10.1111/jeb.12678 · 3.23 Impact Factor
  • Source
    [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.
    Proceedings of the Royal Society B: Biological Sciences 05/2015; 282(1808). DOI:10.1098/rspb.2015.0724 · 5.05 Impact Factor
  • Source
    [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.
    Proceedings of the Royal Society of London. Series B, Containing papers of a Biological character. Royal Society (Great Britain) 04/2015; 282(1807):20150389. DOI:10.1098/rspb.2015.0389
  • Source
    David M. Shuker · Niall Currie · Tara Hoole · Emily R. Burdfield-Steel ·
    [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.
    Population Ecology 04/2015; 57(2). DOI:10.1007/s10144-014-0470-1 · 1.57 Impact Factor
  • Source
    Rebecca A Boulton · David M Shuker ·
    [Show abstract] [Hide abstract]
    ABSTRACT: The taxonomically widespread nature of polyandry remains a puzzle. Much of the empirical work regarding the costs and benefits of multiple mating to females has, for obvious reasons, relied on species that are already highly polyandrous. However, this makes it difficult to separate the processes that maintain the current level of polyandry from the processes that facilitate its expression and initiated its evolution. Here we consider the costs and benefits of polyandry in Nasonia vitripennis, a species of parasitoid wasp that is "mostly monandrous" in the wild, but which evolves polyandry under laboratory culture conditions. In a series of six experiments, we show that females gain a direct fecundity and longevity benefit from mating multiply with virgin males. Conversely, mating multiply with previously mated males actually results in a fecundity cost. Sexual harassment may also represent a significant cost of reproduction. Harassment was, however, only costly during oviposition, resulting in reduced fecundity, longevity and disrupted sex allocation. Our results show that ecological changes, in our case associated with differences in the local mating structure in the laboratory can alter the costs and benefits of mating and harassment and potentially lead to shifts in mating patterns. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Evolution 03/2015; DOI:10.1111/evo.12636 · 4.61 Impact Factor
  • Source
    Fhionna R Moore · David M Shuker · Liam R Dougherty ·

    Behavioral Ecology 01/2015; DOI:10.1093/beheco/arv195 · 3.18 Impact Factor
  • Source
    Nicola Cook · David M Shuker ·
    [Show abstract] [Hide abstract]
    ABSTRACT: A study in spider mites confirms predictions that males and females come into conflict over optimal sex allocation when local mate competition affects sex allocation in haplodiploid species.
    Current Biology 12/2014; 24(13):pR1135-1137. DOI:10.1016/j.cub.2014.10.068 · 9.57 Impact Factor
  • Source
    Emily R. Burdfield-Steel · David M. Shuker ·
    [Show abstract] [Hide abstract]
    ABSTRACT: Mating strategy is often informed by social context. However, information on social environment may be sensitive to interference by nearby heterospecifics, a process known as reproductive interference (RI). When heterospecific individuals are present in the environment, failures in species discrimination can lead to sub-optimal mating behaviours, such as misplaced courtship, misplaced rivalry behaviours, or heterospecific copulation attempts. All aspects of mating behaviour that are influenced by social context may be prone to RI, including copulatory behaviours associated with mate-guarding in the presence of possible competitors. Here we investigate the effect of three heterospecifics on the mate-guarding behaviour of male Lygaeus equestris seed bugs. We find that, despite previously reported heterospecific mating harassment amongst these species of lygaeid bug, male L. equestris are able to effectively distinguish rival conspecific males from heterospecifics. Thus, heterospecific mating attempts in this group may reflect selection on males to mate opportunistically, rather than a failure of species discrimination.
    Evolutionary Ecology 11/2014; 28(6):1031-1042. DOI:10.1007/s10682-014-9726-7 · 2.52 Impact Factor
  • Source
    Liam R Dougherty · David M. Shuker ·

  • Source
    Liam R Dougherty · David M. Shuker ·
    [Show abstract] [Hide abstract]
    ABSTRACT: Quantifying the shape and strength of mating preferences is a vital component of the study of sexual selection and reproductive isolation, but the influence of experimental design on these estimates is unclear. Mating preferences may be tested using either no-choice or choice designs, and these tests may result in different estimates of preference strength. However, previous studies testing for this difference have given mixed results. To quantify the difference in the strength of mating preferences obtained using the 2 designs, we performed a meta-analysis of 38 studies on 40 species in which both experimental designs were used to test for preferences in a single species/trait/sex combination. We found that mating preferences were significantly stronger when tested using a choice design compared with a no-choice design. We suggest that this difference is due to the increased cost of rejecting partners in no-choice tests; if individuals perceive they are unlikely to remate in a no-choice situation they will be more likely to mate randomly. Importantly the use of choice tests in species in which mates are primarily encountered sequentially in the wild may lead to mating preferences being significantly overestimated. Furthermore, this pattern was seen for female mate choice but not for male mate choice, and for intraspecific choice but not for interspecies or interpopulation mate discrimination. Our study thus highlights the fact that the strength of mating preferences, and thus sexual selection, can vary significantly between experimental designs and across different social and ecological contexts.
    Behavioral Ecology 08/2014; 26(2). DOI:10.1093/beheco/aru125 · 3.18 Impact Factor
  • Source
    Rebecca A Boulton · Laura A Collins · David M Shuker ·
    [Show abstract] [Hide abstract]
    ABSTRACT: Despite the diverse array of mating systems and life histories which characterise the parasitic Hymenoptera, sexual selection and sexual conflict in this taxon have been somewhat overlooked. For instance, parasitoid mating systems have typically been studied in terms of how mating structure affects sex allocation. In the past decade, however, some studies have sought to address sexual selection in the parasitoid wasps more explicitly and found that, despite the lack of obvious secondary sexual traits, sexual selection has the potential to shape a range of aspects of parasitoid reproductive behaviour and ecology. Moreover, various characteristics fundamental to the parasitoid way of life may provide innovative new ways to investigate different processes of sexual selection. The overall aim of this review therefore is to re-examine parasitoid biology with sexual selection in mind, for both parasitoid biologists and also researchers interested in sexual selection and the evolution of mating systems more generally. We will consider aspects of particular relevance that have already been well studied including local mating structure, sex allocation and sperm depletion. We go on to review what we already know about sexual selection in the parasitoid wasps and highlight areas which may prove fruitful for further investigation. In particular, sperm depletion and the costs of inbreeding under chromosomal sex determination provide novel opportunities for testing the role of direct and indirect benefits for the evolution of mate choice.
    Biological reviews of the Cambridge Philosophical Society 07/2014; 90(2). DOI:10.1111/brv.12126 · 9.67 Impact Factor
  • Article: NO title

Publication Stats

2k Citations
494.50 Total Impact Points


  • 2009-2015
    • University of St Andrews
      • School of Biology
      Saint Andrews, Scotland, United Kingdom
  • 2010
    • University of Groningen
      • Centre for Ecological and Evolutionary Studies (CEES)
      Groningen, Groningen, Netherlands
  • 2003-2010
    • The University of Edinburgh
      • • Institute of Evolutionary Biology
      • • School of Biological Sciences
      • • Institute of Cell Biology
      Edinburgh, Scotland, United Kingdom
  • 2008
    • University of Cambridge
      • Department of Zoology
      Cambridge, England, United Kingdom
    • Manchester Metropolitan University
      Manchester, England, United Kingdom
  • 2006
    • University of Exeter
      Exeter, England, United Kingdom
  • 2005
    • University of Chicago
      Chicago, Illinois, United States
  • 2001-2002
    • University of Nottingham
      Nottigham, England, United Kingdom