Date Published: September 24, 2004
Publisher: Public Library of Science
Author(s): Robert L Hammond, Laurent Keller
Abstract: Mutual policing is an important mechanism that maintains social harmony in group-living organisms by suppressing the selfish behavior of individuals. In social insects, workers police one another (worker-policing) by preventing individual workers from laying eggs that would otherwise develop into males. Within the framework of Hamilton’s rule there are two explanations for worker-policing behavior. First, if worker reproduction is cost-free, worker-policing should occur only where workers are more closely related to queen- than to worker-produced male eggs (relatedness hypothesis). Second, if there are substantial costs to unchecked worker reproduction, worker-policing may occur to counteract these costs and increase colony efficiency (efficiency hypothesis). The first explanation predicts that patterns of the parentage of males (male parentage) are associated with relatedness, whereas the latter does not. We have investigated how male parentage varies with colony kin structure and colony size in 50 species of ants, bees, and wasps in a phylogenetically controlled comparative analysis. Our survey revealed that queens produced the majority of males in most of the species and that workers produced more than half of the males in less than 10% of species. Moreover, we show that male parentage does not vary with relatedness as predicted by the relatedness hypothesis. This indicates that intra- and interspecific variation in male parentage cannot be accounted for by the relatedness hypothesis alone and that increased colony efficiency is an important factor responsible for the evolution of worker-policing. Our study reveals greater harmony and more complex regulation of reproduction in social insect colonies than that expected from simple theoretical expectations based on relatedness only.
Partial Text: Major evolutionary transitions (Maynard-Smith and Szathmáry 1995) require the evolution of mechanisms that moderate within-group conflict (Keller 1999; Queller 2000; Michod and Roze 2001). One such mechanism is mutual policing, where members of a group collectively prevent individuals from acting in their own selfish interests (Frank 1995). The best example of mutual policing behavior in nature is found in social insects, where workers police worker reproduction (worker-policing) by selectively removing worker-laid eggs that would otherwise develop into males (Ratnieks and Visscher 1989; Foster and Ratnieks 2000, 2001a; Halling et al. 2001; Oldroyd et al. 2001), or by directing aggression toward workers with developing ovaries (Monnin and Ratnieks 2001; Iwanishi et al. 2003). Selection for worker-policing depends upon two variables: the relative relatedness of workers to queen- and worker-produced males (relatedness hypothesis) and the colony-level cost of workers reproducing (efficiency hypothesis). Worker-policing theory (Starr 1984; Woyciechowski and Lomnicki 1987; Ratnieks 1988), an extension of kin selection theory (Hamilton 1964), has typically highlighted relatedness as the all-important variable that explains when workers should lay male-destined eggs and when they should police one another’s reproduction. In contrast, the costs of worker reproduction (Ratnieks 1988) have been largely ignored or given low prominence in the literature, with the effect that the relatedness hypothesis has become widely accepted as the explanation for worker-policing (Whitfield 2002).
We found data for 50 species: 16 ants, 20 bees, and 14 wasps (Table 1; Figure 1). WPM varied considerably (0%–85%), but in most species, queens produced the majority of males, with less than 10% of males being worker-produced in 72% of species surveyed. In only 10% of species were more than 50% of males worker-produced. There was great variation in the number of males (nm = 13–1,426) and likewise in the number of assignable males (na = 10–677, where na is the sample size corrected for the probability of nondetection [Foster et al. 2001]) that were used to estimate the WPM. However, in those species for which we had relevant data, there was no significant correlation of nm or na with WPM (Spearman’s rank correlation: nm versus WPM: ρ = 0.17, n = 45, p = 0.27; na versus WPM: ρ = 0.11, n = 27, p = 0.59), suggesting that there was no systematic bias in our dataset.
Our survey revealed that queens produced the majority of males in most of the species, and in less than 10% of the species did workers produce more than half of the males, in line with earlier surveys based largely on behavioral data (Bourke 1988; Choe 1988). Since workers of all the species included in our survey have functional ovaries, this demonstrates that self-restraint and worker-policing are widespread and powerful mechanisms that regulate reproduction in colonies of social Hymenoptera.