Tom Wenseleers

Worker reproduction and policing in insect societies: an ESS analysis

Insect societies are vulnerable to exploitation by workers who reproduce selfishly rather than help to rear the queens offspring. In most species, however, only a small proportion of the workers reproduce. Here, we develop an evolutionarily stable strategy (ESS) model to investigate factors that could explain these observed low levels of reproductive exploitation. Two key factors are identified: relatedness and policing. Relatedness affects the ESS proportion of reproductive workers because laying workers generally work less, leading to greater inclusive fitness costs when within‐colony relatedness is higher. The second key factor is policing. In many species, worker‐laid eggs are selectively removed or ‘policed’ by other workers or the queen. We show that policing not only prevents the rearing of worker‐laid eggs but can also make it unprofitable for workers to lay eggs in the first place. This can explain why almost no workers reproduce in species with efficient policing, such as honeybees, Apis, and the common wasp, Vespula vulgaris, despite relatively low relatedness caused by multiple mating of the mother queen. Although our analyses focus on social insects, the conclusion that both relatedness and policing can reduce the incentive for cheating applies to other biological systems as well.

Enforced altruism in insect societies

Cooperation among workers and their seeming altruism result from strict policing by nestmates.

Caste fate conflict in swarm-founding social Hymenoptera: an inclusive fitness analysis

A caste system in which females develop into morphologically distinct queens or workers has evolved independently in ants, wasps and bees. Although such reproductive division of labour may benefit the colony it is also a source of conflict because individual immature females can benefit from developing into a queen in order to gain greater direct reproduction. Here we present a formal inclusive fitness analysis of caste fate conflict appropriate for swarm‐founding social Hymenoptera. Three major conclusions are reached: (1) when caste is self‐determined, many females should selfishly choose to become queens and the resulting depletion of the workforce can substantially reduce colony productivity; (2) greater relatedness among colony members reduces this excess queen production; (3) if workers can prevent excess queen production at low cost by controlled feeding, a transition to nutritional caste determination should occur. These predictions generalize results derived earlier using an allele‐frequency model [Behav. Ecol. Sociobiol. (2001) 50: 467] and are supported by observed levels of queen production in various taxa, especially stingless bees, where caste can be either individually or nutritionally controlled.

Cuticular Hydrocarbons Provide Reliable Cues of Fertility in the Ant Gnamptogenys striatula

In ca. 150 species of queenless ants, a specialized queen caste is rare or absent, and mated workers take over the role of the queen in some or all of the colonies. Previously, it has been shown that reproduction in queenless ants is regulated by a combination of dominance behavior and chemical fertility signaling. It is unknown, however, whether chemical signals alone can sufficiently regulate reproduction. To investigate this possibility, we studied reproductive regulation in the facultatively queenless ant Gnamptogenys striatula, a species where dominance behavior is rare or absent. Active egg layers and infertile workers showed qualitative and quantitative differences in their cuticular hydrocarbon profile. Five long-chain methyl alkanes, 3,13- and 3,15-dimethyl pentriacontane, 3,13- and 3,15-dimethyl heptentriacontane, and 3,11,15-trimethyl heptentriacontane occurred only on the cuticles of virgin and mated egg layers. Pronounced quantitative differences were found in a further 27 alkenes; alkanes; and mono-, di-, and trimethyl alkanes. Workers that had recently stopped laying eggs had profiles similar to infertile workers, and mating status did not affect this chemical pattern. We conclude that the cuticular hydrocarbon profiles of G. striatula workers provide reliable information about their current fertility. In the interest of colony productivity, this allows reproduction to be regulated without the use of aggression.

The queen is dead—long live the workers: intraspecific parasitism by workers in the stingless bee Melipona scutellaris

Insect societies are well known for their high degree of cooperation, but their colonies can potentially be exploited by reproductive workers who lay unfertilized, male eggs, rather than work for the good of the colony. Recently, it has also been discovered that workers in bumblebees and Asian honeybees can succeed in entering and parasitizing unrelated colonies to produce their own male offspring. The aim of this study was to investigate whether such intraspecific worker parasitism might also occur in stingless bees, another group of highly social bees. Based on a large‐scale genetic study of the species Melipona scutellaris, and the genotyping of nearly 600 males from 45 colonies, we show that ∼20% of all males are workers’ sons, but that around 80% of these had genotypes that were incompatible with them being the sons of workers of the resident queen. By tracking colonies over multiple generations, we show that these males were not produced by drifted workers, but rather by workers that were the offspring of a previous, superseded queen. This means that uniquely, workers reproductively parasitize the next‐generation workforce. Our results are surprising given that most colonies were sampled many months after the previous queen had died and that workers normally only have a life expectancy of ∼30u2003days. It also implies that reproductive workers greatly outlive all other workers. We explain our results in the context of kin selection theory, and the fact that it pays workers more from exploiting the colony if costs are carried by less related individuals.

Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp

Inclusive fitness theory predicts that in colonies of social Hymenoptera headed by a multiple‐mated queen, workers should benefit from policing eggs laid by other workers. Foster & Ratnieks provided evidence that in the vespine wasp Dolichovespula saxonica, workers police other workers’ eggs only in colonies headed by a multiple‐mated queen, but not in those headed by a single‐mated one. This conclusion, however, was based on a relatively small sample size, and the original study did not control for possible confounding variables such as the seasonal colony progression of the nests. Our aim, therefore, was to reinvestigate whether or not facultative worker policing occurs in D. saxonica. Remarkably, our data show that in the studied Danish population, there was no correlation between worker–worker relatedness and the percentage of worker‐derived males. In addition, we show that variability in cuticular hydrocarbon profiles among the workers did not significantly correlate with relatedness and that workers therefore probably did not have sufficient information on queen mating frequency from the workers’ cuticular hydrocarbon profiles. Hence, there was no evidence that workers facultatively policed other workers’ eggs in response to queen mating frequency. Nevertheless, our data do show that the seasonal progression of the nest and the location in which the males were reared both explain the patterns of worker reproduction found. Overall, our results suggest that the earlier evidence for facultative worker policing in D. saxonica may have been caused by accidental correlations with certain confounding variables, or, alternatively, that there are large interpopulation differences in the expression of worker policing.

Modelling social evolution: the relative merits and limitations of a Hamilton's rule-based approach

Lehmann & Keller (2006) convincingly argue that cooperation or altruism can evolve only when at least one of the following conditions are met: (i) cooperation has direct personal benefits, (ii) individuals are genetically related, (iii) individuals have information on the likely behaviour of others or (iv) individuals recognize other cooperators through a phenotypic label (green beard recognition). The first condition is quite obvious. The three others are also intuitive, given that they provide various conditions under which interacting individuals are positively related, meaning more likely than chance to interact with fellow cooperators (Frank, 1998; Pepper & Smuts, 2002; Foster & Wenseleers, 2006; Foster et al., 2006). By focusing on costs and benefits and relatedness, Lehmann and Keller (2006) are adopting an inclusive fitness or Hamilton’s rule-based approach to classify social evolution models (Hamilton, 1964). Personally, I believe a Hamiltonian perspective is indeed a very intuitive one, and should be adopted more widely. This is true particularly in the area of game theory, where currently little effort is made to interpret results this way, and models are frequently simulation-based, making general, intuitive interpretation of results difficult. In fact, in my own work, Hamilton’s rule has always taken a central place in the derivation and interpretation of model results (e.g. Wenseleers et al., 2003, 2004a, b; Ratnieks et al., 2006). At the same time, however, one may also wonder whether it is possible to translate every single social evolution model into the form of Hamilton’s rule. Here, I am skeptical, the reason being that Hamilton’s rule has well-known limitations. In particular, Hamilton’s rule only works correctly under weak selection and additive gene action (Cavalli-Sforza & Feldman, 1978; Michod, 1982; Grafen, 1985; Bulmer, 1994; Hamilton, 1964, 1995; Frank, 1997; Roze & Rousset, 2003; Rousset, 2004). In addition, evolution is normally assumed to be close to equilibrium, with most of the population fixed for a single type (Frank, 1998). Finally, with Hamilton’s rule being a deterministic equation, it entirely neglects stochasticity, and thus ignores the possibility for deleterious altruistic genotypes to go to fixation as a result of drift (Frank, 1997), which models have shown to be quite possible in small populations (Eshel, 1972; Rousset, 2004). In the section below I will give two worked-out examples where some of these limitations come into play and where, due to violations of assumptions, Hamilton’s rule does not correctly predict evolutionary change. The implication is that partitioning selection into direct and indirect fitness components is not always as straightforward as Lehmann and Keller make out. In many cases, the conditions under which a cooperative genotype would spread relative to a noncooperative one simply cannot be written in the form of Hamilton’s rule. In such situations, the inclusive fitness framework of Lehmann and Keller cannot be used to accurately classify models.

Territorial Marking in the Desert Ant Cataglyphis niger: Does It Pay to Play Bourgeois?

Here we report on territorial behavior in the desert ant Cataglyphis niger. We show that, similar to the “bourgeois strategy,” contests are settled quickly through nonescalating fights, with the owner of the territory usually being placed in the winning role. The chemical cue that advertises ownership is shown to come from pheromones secreted by the cloacal gland. Differences in size did not influence the outcome of the experimental contests, but resource value did. The observed results fit in well with the biology of Cataglyphis, where, due to the harsh semidesert environment, fighting costs (C) are expected to be high relative to the value of the contested resources (V). A situation where V < C is exactly that in which bourgeois behavior is expected to be seen.

Successful maintenance of a stingless bee population despite a severe genetic bottleneck

Stingless bees play an important ecological role as pollinators of many wild plant species in the tropics and have significant potential for the pollination of agricultural crops. Nevertheless, conservation efforts as well as commercial breeding programmes require better guidelines on the amount of genetic variation that is needed to maintain viable populations. In this context, we carried out a long-term genetic study on the stingless bee Melipona scutellaris to evaluate the population viability consequences of prolonged breeding from a small number of founder colonies. In particular, it was artificially imposed a genetic bottleneck by setting up a population starting from only two founder colonies, and continued breeding from it for a period of over 10xa0years in a location outside its natural area of occurrence. We show that despite a great reduction in the number of alleles present at both neutral microsatellite loci and the sex-determining locus relative to its natural source population, and an increased frequency in the production of sterile diploid males, the genetically impoverished population could be successfully bred and maintained for at least 10xa0years. This shows that in stingless bees, breeding from a small stock of colonies may have less severe consequences than previously suspected. In addition, we provide a simulation model to determine the number of colonies that are needed to maintain a certain number of sex alleles in a population, thereby providing useful guidelines for stingless bee breeding and conservation efforts.

Knowing your enemies: seasonal dynamics of host–social parasite recognition

Despite its evolutionary significance, behavioural flexibility of social response has rarely been investigated in insects. We studied a host–social parasite system: the slave-making ant Polyergus rufescens and its host Formica rufibarbis. Free-living host workers from parasitized and from unparasitized areas were compared in their level of aggression against the parasite and alien conspecifics. We expected that a seasonal change would occur in the acceptance threshold of F. rufibarbis workers from a parasitized area towards the parasite, whereas F. rufibarbis workers from an unparasitized area would not show substantial changes connected with the parasite’s peak in activity (raiding and colony-founding season). The results showed a significant adaptive behavioural flexibility of host species workers and are consistent with the acceptance threshold model’s (Reeve 1989) prediction that recognition systems are not fixed but context-dependent. In particular, host workers from the unparasitized area were highly aggressive towards the parasite regardless of the season, whereas host workers from the parasitized area significantly increased their aggression towards the parasite during its raiding and colony-founding season. Being able to detect and possibly kill a Polyergus scout searching for host nests can be an effective strategy for a Formica colony to avoid being raided or usurped by a parasite queen.