David M Shuker

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

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Publications (85)452.87 Total impact

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    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 · 5.29 Impact Factor
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    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
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    Rebecca A Boulton, David M Shuker
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    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 · 4.66 Impact Factor
  • Population Ecology 01/2015; DOI:10.1007/s10144-014-0470-1 · 1.70 Impact Factor
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    Nicola Cook, David M Shuker
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    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 · 9.92 Impact Factor
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    Liam R Dougherty, David M. Shuker
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    Liam R Dougherty, David M. Shuker
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    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 · 3.16 Impact Factor
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    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 · 6.63 Impact Factor
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    Emily R. Burdfield‐Steel, David M. Shuker
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    ABSTRACT: The Lygaeidae (sensu lato) are a highly successful family of true bugs found worldwide, yet many aspects of their ecology and evolution remain obscure or unknown. While a few species have attracted considerable attention as model species for the study of insect physiology, it is only relatively recently that biologists have begun to explore aspects of their behavior, life history evolution, and patterns of intra- and interspecific ecological interactions across more species. As a result though, a range of new phenotypes and opportunities for addressing current questions in evolutionary ecology has been uncovered. For example, researchers have revealed hitherto unexpectedly rich patterns of bacterial symbiosis, begun to explore the evolutionary function of the family's complex genitalia, and also found evidence of parthenogenesis. Here we review our current understanding of the biology and ecology of the group as a whole, focusing on several of the best-studied characteristics of the group, including aposematism (i.e., the evolution of warning coloration), chemical communication, sexual selection (especially, postcopulatory sexual selection), sexual conflict, and patterns of host-endosymbiont coevolution. Importantly, many of these aspects of lygaeid biology are likely to interact, offering new avenues for research, for instance into how the evolution of aposematism influences sexual selection. With the growing availability of genomic tools for previously “non-model” organisms, combined with the relative ease of keeping many of the polyphagous species in the laboratory, we argue that these bugs offer many opportunities for behavioral and evolutionary ecologists.
    Ecology and Evolution 05/2014; DOI:10.1002/ece3.1093 · 1.66 Impact Factor
  • David M Shuker
    Trends in Ecology & Evolution 04/2014; 29(6). DOI:10.1016/j.tree.2014.03.012 · 15.35 Impact Factor
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    Liam R. Dougherty, David M. Shuker
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    ABSTRACT: Mate choice has long been appreciated as a key component of sexual selection. However, how we measure mate choice, both in the field and in the laboratory, remains problematic. Mating preferences may be tested using either no-choice or choice tests, but explicit comparisons between these two experimental paradigms remain limited. It has been suggested that preferences may be stronger in choice tests as they allow simultaneous comparison, and some studies have indeed found stronger mating preferences in choice tests compared to no-choice tests. Here we explicitly tested the effect of experimental choice paradigm on the measurement of sexual selection on male and female morphology in the promiscuous seed bug Lygaeus equestris (Heteroptera, Lygaeidae). We performed mating trials in which we varied the amount of choice presented to each sex, giving four choice treatments: no-choice, male choice, female choice and mutual choice. Overall we found evidence for significant positive directional selection on female body length and stabilizing selection on an overall measure of male body size. However, we found no significant effect of choice paradigm on the patterns of sexual selection for males or females. We suggest this may be because of the method of mate assessment in L. equestris, which appears to be primarily via contact cues, which may limit simultaneous comparison between options.
    Animal Behaviour 03/2014; 89:207–214. DOI:10.1016/j.anbehav.2014.01.005 · 3.07 Impact Factor
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    Emily R. Burdfield-Steel, David M. Shuker
    Evolutionary Ecology 01/2014; 28(6):1031-1042. · 2.37 Impact Factor
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    Article: Polyandry.
    Rebecca A Boulton, David M Shuker
    Current biology: CB 12/2013; 23(24):R1080-1. DOI:10.1016/j.cub.2013.09.042 · 9.92 Impact Factor
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    ABSTRACT: Niche construction refers to the activities of organisms that bring about changes in their environments, many of which are evolutionarily and ecologically consequential. Advocates of niche construction theory (NCT) believe that standard evolutionary theory fails to recognize the full importance of niche construction, and consequently propose a novel view of evolution, in which niche construction and its legacy over time (ecological inheritance) are described as evolutionary processes, equivalent in importance to natural selection. Here, we subject NCT to critical evaluation, in the form of a collaboration between one prominent advocate of NCT, and a team of skeptics. We discuss whether niche construction is an evolutionary process, whether NCT obscures or clarifies how natural selection leads to organismal adaptation, and whether niche construction and natural selection are of equivalent explanatory importance. We also consider whether the literature that promotes NCT overstates the significance of niche construction, whether it is internally coherent, and whether it accurately portrays standard evolutionary theory. Our disagreements reflect a wider dispute within evolutionary theory over whether the neo-Darwinian synthesis is in need of reformulation, as well as different usages of some key terms (e.g. evolutionary process). This article is protected by copyright. All rights reserved.
    Evolution 12/2013; DOI:10.1111/evo.12332 · 4.66 Impact Factor
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    ABSTRACT: The ability of animals to remember the what, where and when of a unique past event is used as an animal equivalent to human episodic memory. We currently view episodic memory as reconstructive, with an event being remembered in the context in which it took place. Importantly, this means that the components of a what, where, when memory task should be dissociable (e.g. what would be remembered to a different degree than when). We tested this hypothesis by training hummingbirds to a memory task, where the location of a reward was specified according to colour (what), location (where), and order and time of day (when). Although hummingbirds remembered these three pieces of information together more often than expected, there was a hierarchy as to how they were remembered. When seemed to be the hardest to remember, while errors relating to what were more easily corrected. Furthermore, when appears to have been encoded as a combination of time of day and sequence information. As hummingbirds solved this task using reconstruction of different memory components (what, where and when), we suggest that similar deconstructive approaches may offer a useful way to compare episodic and episodic-like memories.
    Proceedings of the Royal Society B: Biological Sciences 10/2013; 280(1772):20132194. DOI:10.1098/rspb.2013.2194 · 5.29 Impact Factor
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    ABSTRACT: Linking behavioural phenotypes to their underlying genotypes is crucial for uncovering the mechanisms that underpin behaviour and for understanding the origins and maintenance of genetic variation in behaviour. Recently, interest has begun to focus on the transcriptome as a route for identifying genes and gene pathways associated with behaviour. For many behavioural traits studied at the phenotypic level, we have little or no idea of where to start searching for "candidate" genes: the transcriptome provides such a starting point. Here we consider transcriptomic changes associated with oviposition in the parasitoid wasp Nasonia vitripennis. Oviposition is a key behaviour for parasitoids, as females are faced with a variety of decisions that will impact offspring fitness. These include choosing between hosts of differing quality, as well as making decisions regarding clutch size and offspring sex ratio. We compared the whole-body transcriptomes of resting or ovipositing female Nasonia using a "DeepSAGE" gene expression approach on the Illumina sequencing platform. We identified 332 tags that were significantly differentially expressed between the two treatments, with 77% of the changes associated with greater expression in resting females. Oviposition therefore appears to focus gene expression away from a number of physiological processes, with gene ontologies suggesting that aspects of metabolism may be down-regulated during egg-laying. Nine of the most abundant differentially expressed tags showed greater expression in ovipositing females though, including the genes purity-of-essence (associated with behavioural phenotypes in Drosophila) and glucose dehydrogenase (GLD). The GLD protein has been implicated in sperm storage and release in Drosophila and so provides a possible candidate for the control of sex allocation by female Nasonia during oviposition. Oviposition in Nasonia therefore clearly modifies the transcriptome, providing a starting point for the genetic dissection of oviposition.
    PLoS ONE 07/2013; 8(7):e68608. DOI:10.1371/journal.pone.0068608 · 3.53 Impact Factor
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    ABSTRACT: Understanding variation in social behaviour both within and among species continues to be a challenge. Evolutionary or ecological theory typically predicts the optimal behaviour for an animal under a given set of circumstances, yet the real world presents much greater variation in behaviour than predicted. This variation is apparent in many social and sexual interactions, including mate choice, and has led to a renewed focus on individual variation in behaviour. Here we explore within and among species variation in social behaviour in four species of aposematic seed bug (Lygaeidae: Hemiptera). These species are Müllerian mimics, with characteristic warning colouration advertising their chemical toxicity. We examine the role of diet in generating variation in two key behaviours: social aggregation of nymphs and mate choice. We test how behaviour varies with exposure to either milkweed (a source of defensive compounds) or sunflower (that provides no defence). We show that although the four species vary in their food preferences, and diet influences their life-history (as highlighted by body size), social aggregation and mate choice is relatively unaffected by diet. We discuss our findings in terms of the evolution of aposematism, the importance of automimicry, and the role of diet in generating behavioural variation.
    Behavioural processes 06/2013; 99. DOI:10.1016/j.beproc.2013.06.006 · 1.46 Impact Factor
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    ABSTRACT: Host-parasite interactions are a key paradigm for understanding the process of coevolution. Central to coevolution is how genetic variation in interacting species allows parasites to evolve manipulative strategies. However, genetic variation in the parasite may also be associated with host phenotype changes, thereby changing the selection on both species. For instance, parasites often induce changes in the behaviour of their host to maximize their own fitness, yet the quantitative genetic basis for behavioural manipulation has not been fully demonstrated. Here, we show that the genotype of the parasitoid wasp Aphidius ervi has a significant effect on where its aphid host Acyrthosiphon pisum moves to die following parasitism, including the likelihood that the aphid abandons the plant. These results provide a clear example of an interspecific indirect genetic effect whereby the genetics of one species influences the expression of a specific behavioural trait in another.
    Biology letters 03/2013; 9(3):20121151. DOI:10.1098/rsbl.2012.1151 · 3.43 Impact Factor
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    ABSTRACT: There is a long-standing debate within the field of sexual selection regarding the potential projection of stereotypical sex roles onto animals by researchers. It has been argued that this anthropomorphic view may be hampering research in this area, for example by prioritizing the study of male sexual adaptations over female ones. We investigated how males and females are described in the sexual cannibalism literature. Sexual cannibalism is a specific form of sexual conflict and is highly gendered, with females generally cannibalizing males. We found that females were more likely to be described using active words and males with reactive words. This is contrary to recent results from a survey of the sexual conflict literature. While this reversed gender bias may arise from the nature of sexual cannibalism, our results nevertheless indicate an alternative form of sexual stereotyping. A number of the words used to describe cannibalistic females were highly loaded and suggestive of a negative stereotype of sexually aggressive females. To make progress we suggest first that animal behaviour researchers recognize both the costs and benefits of looking for general patterns as part of the scientific method. Although necessary, the search for general patterns may validate existing stereotypes or provide the basis for new ones. Additionally, we suggest that the field of sexual behaviour research is neither wholly bad nor good in terms of language use but that we should work towards a consensus of how and when we use particular terms to describe sexual behaviour.
    Animal Behaviour 02/2013; 85(2):313-322. DOI:10.1016/j.anbehav.2012.12.008 · 3.07 Impact Factor
  • European Journal of Entomology 01/2013; 110(1):87-93. DOI:10.14411/eje.2013.011 · 1.08 Impact Factor

Publication Stats

2k Citations
452.87 Total Impact Points

Institutions

  • 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
    • University of Leeds
      • School of Biology
      Leeds, England, United Kingdom
  • 2005
    • University of Chicago
      Chicago, Illinois, United States
  • 2001–2002
    • University of Nottingham
      Nottigham, England, United Kingdom