Division of labour and social insect colony performance in relation to task and mating number under two alternative response threshold models

Gove, Robert; Hayworth, Miranda; Chhetri, Maya; Rueppell, Olav

doi:10.1007/s00040-009-0028-y

Cited by 44 publications

(36 citation statements)

References 79 publications

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“…Our results on the strong effect of multiple mating on intra- and inter-colonial genotypic variance conforms well with previous theoretical work [51], computer simulations of colony task performance [9], and empirical studies showing benefits of multiple mating for behavioral organization [14], disease resistance [17], and colony performance [16]. In concordance with previous studies the main benefit of multiple mating for genetic diversity is gained when mating numbers are low and the increase in variance becomes marginal for mating number above 20, irrespective of the number of contributing loci or other modifications of the genetic architecture.…”

Section: Discussionsupporting

confidence: 91%

Multiple Mating But Not Recombination Causes Quantitative Increase in Offspring Genetic Diversity for Varying Genetic Architectures

2012

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Explaining the evolution of sex and recombination is particularly intriguing for some species of eusocial insects because they display exceptionally high mating frequencies and genomic recombination rates. Explanations for both phenomena are based on the notion that both increase colony genetic diversity, with demonstrated benefits for colony disease resistance and division of labor. However, the relative contributions of mating number and recombination rate to colony genetic diversity have never been simultaneously assessed. Our study simulates colonies, assuming different mating numbers, recombination rates, and genetic architectures, to assess their worker genotypic diversity. The number of loci has a strong negative effect on genotypic diversity when the allelic effects are inversely scaled to locus number. In contrast, dominance, epistasis, lethal effects, or limiting the allelic diversity at each locus does not significantly affect the model outcomes. Mating number increases colony genotypic variance and lowers variation among colonies with quickly diminishing returns. Genomic recombination rate does not affect intra- and inter-colonial genotypic variance, regardless of mating frequency and genetic architecture. Recombination slightly increases the genotypic range of colonies and more strongly the number of workers with unique allele combinations across all loci. Overall, our study contradicts the argument that the exceptionally high recombination rates cause a quantitative increase in offspring genotypic diversity across one generation. Alternative explanations for the evolution of high recombination rates in social insects are therefore needed. Short-term benefits are central to most explanations of the evolution of multiple mating and high recombination rates in social insects but our results also apply to other species.

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Section: Discussionsupporting

confidence: 91%

Multiple Mating But Not Recombination Causes Quantitative Increase in Offspring Genetic Diversity for Varying Genetic Architectures

2012

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“…Theoretical work has investigated the role of interindividual variability and genetic architecture on colony performance (e.g. Page & Mitchell, ; Bertram, Gorelick & Fewell, ; Myerscough & Oldroyd, ; Jeanson et al , ; Gove et al , ; Tarapore, Floreano & Keller, ). Despite variations in model structures, these studies generally showed that interindividual variability is beneficial to colonies.…”

Section: Ultimate Consequences: How Does Variability Affect the Colony?mentioning

confidence: 99%

Interindividual variability in social insects – proximate causes and ultimate consequences

2013

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Individuals within social groups often show consistent differences in behaviour across time and context. Such interindividual differences and the evolutionary challenge they present have recently generated considerable interest. Social insects provide some of the most familiar and spectacular examples of social groups with large interindividual differences. Investigating these within-group differences has a long research tradition, and behavioural variability among the workers of a colony is increasingly regarded as fundamental for a key feature of social insects: division of labour. The goal of this review is to illustrate what we know about both the proximate mechanisms underlying behavioural variability among the workers of a colony and its ultimate consequences; and to highlight the many open questions in this research field. We begin by reviewing the literature on mechanisms that potentially introduce, maintain, and adjust the behavioural differentiation among workers. We highlight the fact that so far, most studies have focused on behavioural variability based on genetic variability, provided by e.g. multiple mating of the queen, while other mechanisms that may be responsible for the behavioural differentiation among workers have been largely neglected. These include maturational, nutritional and environmental influences. We further discuss how feedback provided by the social environment and learning and experience of adult workers provides potent and little-explored sources of differentiation. In a second part, we address what is known about the potential benefits and costs of increased behavioural variability within the workers of a colony. We argue that all studies documenting a benefit of variability so far have done so by manipulating genetic variability, and that a direct test of the effect of behavioural variability on colony productivity has yet to be provided. We emphasize that the costs associated with interindividual variability have been largely overlooked, and that a better knowledge of the cost/benefit balance of behavioural variability is crucial for our understanding of the evolution of the mechanisms underlying the social organization of insect societies. We conclude by highlighting what we believe to be promising but little-explored avenues for future research on how within-colony variability has evolved and is maintained. We emphasize the need for comparative studies and point out that, so far, most studies on interindividual variability have focused on variability in individual response thresholds, while the significance of variability in other parameters of individual response, such as probability and intensity of the response, has been largely overlooked. We propose that these parameters have important consequences for the colony response. Much more research is needed to understand if and how interindividual variability is modulated in order to benefit division of labour, homeostasis and ultimately colony fitness in social insects.

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“…These benefits could arise because there is a genetic basis to worker castes (e.g. Hughes et al , 2003; Hughes & Boomsma, 2007; Jaffe et al , 2007) such that colonies founded by polygamous queens are more efficient in their division of labour (review: Smith et al , 2008; theoretical models: Gove et al , 2009; Tarapore, Floreano & Keller, 2010). There is also good evidence that patrilines differ in their susceptibility to certain diseases, so that a more genetically diverse colony workforce reduces the spread of disease and/or parasites, and lowers the mean level of worker mortality (e.g.…”

Section: Introductionmentioning

confidence: 99%

Estimating genetic benefits of polyandry from experimental studies: a meta‐analysis

et al. 2011

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The consequences of polyandry for female fitness are controversial. Sexual conflict studies and a meta-analysis of mating rates in insects suggest that there is a longevity cost when females mate repeatedly. Even so, compensatory material benefits can elevate egg production and fertility, partly because polyandry ensures an adequate sperm supply. Polyandry can therefore confer direct benefits. The main controversy surrounds genetic benefits. The argument is analogous to that surrounding the evolution of conventional female mate choice, except that with polyandry it is post-copulatory mechanisms that might bias paternity towards males with higher breeding values for fitness. Recent meta-analyses of extra-pair copulations in birds have cast doubt on whether detectable genetic benefits exist. By contrast, another meta-analysis showed that polyandry elevates egg hatching success (possibly due to a fertilization bias towards sperm with paternal genes that elevate embryo survival) in insects. A detailed summary of whether polyandry elevates other components of offspring performance is lacking. Here we present a comprehensive meta-analysis of 232 effect sizes from 46 experimental studies. These experiments were specifically designed to try to quantify the potential genetic benefits of polyandry by controlling fully for the number of matings by females assigned to monandry and polyandry treatments. The bias-corrected 95% confidence intervals for egg hatching success (d = -0.01 to 0.61), clutch production (d = 0.07 to 0.45) and fertility (d = 0.04 to 0.40) all suggest that polyandry has a beneficial effect (although P values from parametric tests were marginally non-significant at P = 0.075, 0.052 and 0.058, respectively). Polyandry was not significantly beneficial for any single offspring performance trait (e.g. growth rate, survival, adult size), but the test power was low due to small sample sizes (suggesting that many more studies are still needed). We then calculated a composite effect size that provides an index of general offspring performance. Depending on the model assumptions, the mean effect of polyandry was either significantly positive or marginally non-significant. A possible role for publication bias is discussed. The magnitude of the reported potential genetic benefits (d = 0.07 to 0.19) are larger than those from two recent meta-analyses comparing offspring sired by social and extra-pair mates in birds (d = 0.02 to 0.04). This difference raises the intriguing possibility that cryptic, post-copulatory female choice might be more likely to generate 'good gene' or 'compatible gene' benefits than female choice of mates based on the expression of secondary sexual traits.

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Division of labour and social insect colony performance in relation to task and mating number under two alternative response threshold models

Cited by 44 publications

References 79 publications

Multiple Mating But Not Recombination Causes Quantitative Increase in Offspring Genetic Diversity for Varying Genetic Architectures

Multiple Mating But Not Recombination Causes Quantitative Increase in Offspring Genetic Diversity for Varying Genetic Architectures

Interindividual variability in social insects – proximate causes and ultimate consequences

Estimating genetic benefits of polyandry from experimental studies: a meta‐analysis

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