Genetic royal cheats in leaf-cutting ant societies

Abstract

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.caste ͉ polymorphism ͉ social evolution ͉ polyandry ͉ social insect

Lifetime monogamy and the evolution of eusociality

“…Those relevant for domain 1 are reviewed in Burt & Trivers (2006) and those relevant for domain 2 in Buss (1987) and Michod (2005). Threats of domain 3 may include workers that reproduce in the presence of the queen and socially parasitic additional queens that may ultimately give rise to inquiline species (Buschinger 1990) and selfish patrilines (Hughes & Boomsma 2008 . Schematic comparison of the evolutionary transition from unicellularity to multicellularity and the evolution of eusociality in the haplodiploid ants (the same applies to bees and wasps) and diploid termites.…”

Patriline shifting leads to apparent genetic caste determination in harvester ants

“…This z-statistic is the effect size for a particular colony and has the desirable property that the null expectation is a standard normal distribution. From earlier studies of A. echinatior (20,23), E. burchellii (22), P. badius (21,24), F. exsecta, and F. truncorum (62), we calculated the heterogeneity G-statistic and the exact probability, the effect size for each colony in the study, and the 95% confidence interval of the mean effect size (across colonies) for each species. Data for a recent similar study in P. rugosus (29) were not presented in a form that allowed calculation of appropriate statistics.…”

“…A similar phenomenon occurs in hybridizing populations of fire ant species (19). In these species, there is a clear genetic effect.A second set of studies involves species with polyandrous queens that find differences in the distribution of male genotypes between gynes and workers or between workers belonging to different castes (20)(21)(22)(23)(24). The general pattern is to find that in some, but not all, colonies the distribution of male genotypes (patrilines) differs significantly between castes, leading to a significant overall difference when results are pooled across colonies.…”

“…Just as task specialization leads to division of labor and increased efficiency in colonies (e.g., ref. 26), so too could a genetic predisposition to become a major or minor worker enhance colony-level performance (23). Similarly, utilization of high-quality genotypes as gynes could increase colony fitness (27).…”

Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants

“…Even though recent studies revealed genetic influences on caste determination in social insects (reviewed in ref. 26), female caste fate is primarily influenced by environmental factors in most species studied (27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39). In ants, several studies suggested that maternal factors such as temperature or queen age may affect caste determination (40)(41)(42)(43)(44).…”