Genetic royal cheats in leaf-cutting ant societies

Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 05/2008; 105(13):5150-3. DOI: 10.1073/pnas.0710262105
Source: PubMed


Social groups are vulnerable to cheating because the reproductive interests of group members are rarely identical. All cooperative systems are therefore predicted to involve a mix of cooperative and cheating genotypes, with the frequency of the latter being constrained by the suppressive abilities of the former. The most significant potential conflict in social insect colonies is over which individuals become reproductive queens rather than sterile workers. This reproductive division of labor is a defining characteristic of eusocial societies, but individual larvae will maximize their fitness by becoming queens whereas their nestmates will generally maximize fitness by forcing larvae to become workers. However, evolutionary constraints are thought to prevent cheating by removing genetic variation in caste propensity. Here, we show that one-fifth of leaf-cutting ant patrilines cheat their nestmates by biasing their larval development toward becoming queens rather than workers. Two distinct mechanisms appear to be involved, one most probably involving a general tendency to become a larger adult and the other relating specifically to the queen-worker developmental switch. Just as evolutionary theory predicts, these "royal" genotypes are rare both in the population and within individual colonies. The rarity of royal cheats is best explained as an evolutionary strategy to avoid suppression by cooperative genotypes, the efficiency of which is frequency-dependent. The results demonstrate that cheating can be widespread in even the most cooperative of societies and illustrate that identical principles govern social evolution in highly diverse systems.

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Available from: William O H Hughes, Mar 19, 2014
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    • "A genetic predisposition for certain genotypes to develop into certain castes is of considerable importance in eusocial insects as any male carrying genes that increase the chance that his daughters develop into gynes rather than workers will effectively parasitize on colony resources by producing more than his fair share of sexual offspring. Evidence for such selfish patrilines has been found for replacement queen rearing in honeybees (Moritz et al. 2005), emergency queen rearing through thelytokous parthenogenesis by workers in Cataglyphis cursor ants (Ch^ eron et al. 2011), and in gyne production in A. echinatior leaf-cutting ants (Hughes and Boomsma 2008). While Wiernasz and Cole (2010) argued that sperm clumping might be more common than previously considered, the results of our present study make it unlikely that genotypic variation in caste propensity (Hughes et al. 2003; Hughes and Boomsma 2008) can be explained by deviations from random use of stored sperm. "
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    ABSTRACT: The insemination of queens by sperm from multiple males (polyandry) has evolved in a number of eusocial insect lineages despite the likely costs of the behavior. The selective advantages in terms of colony fitness must therefore also be significant and there is now good evidence that polyandry increases genetic variation among workers, thereby improving the efficiency of division of labor, resistance against disease, and diluting the impact of genetically incompatible matings. However, these advantages will only be maximized if the sperm of initially discrete ejaculates are mixed when stored in queen spermathecae and used for egg fertilization in a “fair raffle.” Remarkably, however, very few studies have addressed the level of sperm mixing in social insects. Here we analyzed sperm use over time in the highly polyandrous leaf-cutting ant Acromyrmex echinatior. We genotyped cohorts of workers produced either 2 months apart or up to over a year apart, and batches of eggs laid up to over 2 years apart, and tested whether fluctuations in patriline distributions deviated from random. We show that the representation of father males in both egg and worker cohorts does not change over time, consistent with obligatorily polyandrous queens maximizing their fitness when workers are as genetically diverse as possible.
    Full-text · Article · Sep 2014 · Ecology and Evolution
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    • "Suggested benefits that may explain polyandry include direct benefits, such as sperm provision, nuptial gifts, and paternal care, and indirect genetic benefits, such as trading up, the dilution of genetic incompatibility, and increased offspring genetic diversity (Arnqvist and Nilsson 2000; Jennions and Petrie 2000; Simmons 2005). In contrast to most other animals, monandry (females inseminated by only a single male) is the most common and ancestral state in social insects, with females (queens) in only a third of species exhibiting some level of polyandry (Hughes et al. 2008a, 2008b). However, some of these are notable for having evolved exceptionally high or apparently obligate levels of polyandry. "
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    ABSTRACT: The evolution of polyandry is a general problem in behavioral ecology that has attracted particular interest in the social insects. Most social insects are monandrous (i.e., females are inseminated by a single male), but approximately a third of species have evolved polyandry (i.e., females are inseminated by multiple males), which can reach extreme levels. One of the leading explanations for polyandry is that genetically diverse colonies may have improved division of labor because of genotypic variation in the propensity of workers to engage in particular tasks. Here we investigate whether there may also be genotypic variation in the ability to carry out a task, by examining the effect of genotype, as well as caste and age, on the foraging performance of workers of the leaf-cutting ant Acromyrmex subterraneus. Larger ants cut larger fragments of orange-impregnated parafilm, and did so more quickly than smaller ants, whereas older ants also cut larger fragments but were slower to transport them. Most importantly, we found that patrilines within colonies differed significantly in the size of fragment cut, and the speed of cutting and transporting fragments when controlling for both ant size and fragment size in the analyses. Certain patrilines were better foragers, often in multiple ways, whereas other patrilines were significantly worse at foraging. Genotype can therefore affect the ability of social insect workers to carry out tasks as well as their previously shown propensity to engage in them, providing an additional mechanism by which genetic diversity may be beneficial to social insect colonies.
    Full-text · Article · Oct 2012 · Behavioral Ecology
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    • "In addition, this species is particularly interesting because certain 'royal cheat' patrilines show a greater propensity to develop into gynes, thus cheating their nest-mates out of a fair chance of reproduction (Hughes & Boomsma, 2008). Such patriline variation in caste propensity can be due to the genetic incompatibilities in some ant species (Schwander & Keller, 2008), but the within-colony rarity of royal patrilines in leaf-cutting ants means that it is more likely to result from genotypic variation in the ability to obtain, utilize or respond to key caste-determining environmental cues, and fitness costs selecting for a low frequency of cheats within colonies (Hughes & Boomsma, 2008). "
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    ABSTRACT: Body size and morphology are key fitness-determining traits that can vary genotypically. They are likely to be important in social insect queens, which mate in swarms and found colonies independently, but genetic influences on queen morphology have been little investigated. Here, we show that the body size and morphology of queens are influenced by their genotype in the leaf-cutting ant Acromyrmex echinatior, a species in which certain lineages (patrilines) bias their development towards reproductive queens rather than sterile workers. We found no relationship between the queen-worker skew of patrilines and the size or morphology of queens, but there was a significant relationship with fluctuating asymmetry, which was greater in more queen-biased patrilines. Our results suggest that queen-biased patrilines do not incur a fitness cost in terms of body size, but may face more subtle costs in developmental stability. Such costs may constrain the evolution of royal cheating in social insects.
    Full-text · Article · Mar 2012 · Journal of Evolutionary Biology
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