Joan E. Strassmann

Microsatellites and kinship

Many evolutionary studies, particularly kinship studies, have been limited by the availability of segregating genetic marker loci. Microsatellites promise to alleviate these problems. Microsatellite loci are segments of DNA with very short sequence motifs repeated in tandem; their often numerous alleles differ in the number of these repeat units. They are very common in eukaryotic DNA and can be amplified by the polymerase chain reaction, which allows the use of minute or degraded DNA samples. The alleles can be scored consistently and compared unambiguously, even across different gels.

KIN SELECTION AND SOCIAL INSECTS

Social insects so dominate many terrestrial habitats (Wilson 1990) that they can hardly escape the attention of biologists, but even if they were rare, they would still attract special interest because of the intricate cooperation within their societies. William Morton Wheeler (1911) described the social insect colony as an organism (or as a higher-level organism or superorganism) because of the degree to which individuals appear to operate as a unit that is dedicated to the perpetuation and reproduction of the colony as a whole. The reinvention of the organism at a higher level has occurred at a number of crucial junctures in the history of life (Maynard Smith and Szathmary 1995). For example, the eukaryotic cell arose from several prokaryotic ancestors (Margulis 1970), and multicellular plants, animals, and fungi arose from single-celled ancestors (Buss 1987). Because insect societies are macroscopic, and because they span the entire range from solitary individuals to essentially superorganismal colonies, they offer an accessible model for how such transitions can happen.

The rarity of multiple mating by females in the social Hymenoptera

Summary: Interest in how often female social insects mate is particularly intense because of its impact on sociality and because of the well-known extreme multiple mating in honeybees. With multiple mating, worker to brood relatedness decreases but worker versus queen interests often converge. The overwhelming majority of species of social ants, bees, and wasps mate only once. Even those species where some females mate multiply typically have effective mate numbers close to one. Ants have effective mate numbers of 1.43, which drops to 1.15 if the advanced fungus growers (2.14) and harvester ants (6.76) are excluded. Honeybees have effective mate numbers of 12.48. Stingless bees and bumblebees have effective mate numbers of only 1.06 and 1.02 respectively. Polistine wasps have effective mate numbers of 1.01. Vespine wasps have effective mate numbers of 1.12 excluding only Vespula which has effective mate numbers of 3.68. Favoring the very low mate numbers we observe for nearly all female social insects is the narrow time window for mating, lack of material gain from males, lack of male ability to harass females (who must move their sting aside to mate in most species), and lack of paternal care. Single mating may be further favored by the apparent lack of any post-copulatory sperm discrimination mechanisms. Leks and male territories, which are common in social insects, make it easier for females to choose the single best mate, further contributing to low mate numbers. Multiple mating is a rare, derived trait in a generally single-mating group. Single mating may have facilitated the origins of sociality in the Hymenoptera because it confers higher relatedness among potential workers and the brood they care for. The rare exceptions to low mate numbers all come from highly social species with single queens, morphological castes, and many workers. Multiple mating might be stable in highly social species because their highly specialized workers have few selfish responses to lowered relatedness. The unusual cases of multiple mating are most likely to be selected for because they increase genetic diversity in the brood, though empirical support for specific genetic diversity hypotheses has proved to be elusive. What is clear is that single mating is predominant in this large, evolutionarily and ecologically successful group.

Unrelated helpers in a social insect

High-resolution genetic markers have revolutionized our understanding of vertebrate mating systems, but have so far yielded few comparable surprises about kinship in social insects. Here we use microsatellite markers to reveal an unexpected and unique social system in what is probably the best-studied social wasp, Polistes dominulus. Social insect colonies are nearly always composed of close relatives; therefore, non-reproductive helping behaviour can be favoured by kin selection, because the helpers aid reproductives who share their genes. In P. dominulus, however, 35% of foundress nestmates are unrelated and gain no such advantage. The P. dominulus system is unlike all other cases of unrelated social insects, because one individual has nearly complete reproductive dominance over subordinates who could have chosen other reproductive options. The only significant advantage that subordinates obtain is a chance at later reproduction, particularly if the queen dies. Thus, P. dominulus societies are functionally unlike other social insects, but similar to certain vertebrate societies, in which the unrelated helpers gain through inheritance of a territory or a mate.

Pleiotropy as a mechanism to stabilize cooperation

Most genes affect many traits. This phenomenon, known as pleiotropy, is a major constraint on evolution because adaptive change in one trait may be prevented because it would compromise other traits affected by the same genes. Here we show that pleiotropy can have an unexpected effect and benefit one of the most enigmatic of adaptations—cooperation. A spectacular act of cooperation occurs in the social amoeba Dictyostelium discoideum, in which some cells die to form a stalk that holds the other cells aloft as reproductive spores. We have identified a gene, dimA, in D. discoideum that has two contrasting effects. It is required to receive the signalling molecule DIF-1 that causes differentiation into prestalk cells. Ignoring DIF-1 and not becoming prestalk should allow cells to cheat by avoiding the stalk. However, we find that in aggregations containing the wild-type cells, lack of the dimA gene results in exclusion from spores. This pleiotropic linkage of stalk and spore formation limits the potential for cheating in D. discoideum because defecting on prestalk cell production results in an even greater reduction in spores. We propose that the evolution of pleiotropic links between cheating and personal costs can stabilize cooperative adaptations.

Beyond society: the evolution of organismality

The evolution of organismality is a social process. All organisms originated from groups of simpler units that now show high cooperation among the parts and are nearly free of conflicts. We suggest that this near-unanimous cooperation be taken as the defining trait of organisms. Consistency then requires that we accept some unconventional organisms, including some social insect colonies, some microbial groups and viruses, a few sexual partnerships and a number of mutualistic associations. Whether we call these organisms or not, a major task is to explain such cooperative entities, and our survey suggests that many of the traits commonly used to define organisms are not essential. These non-essential traits include physical contiguity, indivisibility, clonality or high relatedness, development from a single cell, short-term and long-term genetic cotransmission, germ–soma separation and membership in the same species.

High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants

The control of cheating is important for understanding major transitions in evolution, from the simplest genes to the most complex societies. Cooperative systems can be ruined if cheaters that lower group productivity are able to spread. Kin-selection theory predicts that high genetic relatedness can limit cheating, because separation of cheaters and cooperators limits opportunities to cheat and promotes selection against low-fitness groups of cheaters. Here, we confirm this prediction for the social amoeba Dictyostelium discoideum; relatedness in natural wild groups is so high that socially destructive cheaters should not spread. We illustrate in the laboratory how high relatedness can control a mutant that would destroy cooperation at low relatedness. Finally, we demonstrate that, as predicted, mutant cheaters do not normally harm cooperation in a natural population. Our findings show how altruism is preserved from the disruptive effects of such mutant cheaters and how exceptionally high relatedness among cells is important in promoting the cooperation that underlies multicellular development.

Cooperation among unrelated individuals: the ant foundress case

Ant foundress associations are an example of cooperation among non-kin. Across a dozen genera, queens able to found a colony alone often join unrelated queens, thereby enhancing worker production and colony survivorship. The benefits of joining other queens vary with group size and ecological conditions. However, after the first workers mature, the queens fight until only one survives. The presence of cofoundresses, and their relative fighting ability, also affects the extent of cooperative investment before worker emergence. This reveals previously overlooked early conflicts among queens, which reduce the mutualistic benefits of cooperation.

Mate number, kin selection and social conflicts in stingless bees and honeybees

Microsatellite genotyping of workers from 13 species (ten genera) of stingless bees shows that genetic relatedness is very high. Workers are usually daughters of a single, singly mated queen. This observation, coupled with the multiple mating of honeybee queens, permits kin selection theory to account for many differences in the social biology of the two taxa. First, in contrast to honeybees, where workers are predicted to and do police each others male production, stingless bee workers are predicted to compete directly with the queen for rights to produce males. This leads to behavioural and reproductive conflict during oviposition. Second, the risk that a daughter queen will attack the mother queen is higher in honeybees, as is the cost of such an attack to workers. This explains why stingless bees commonly have virgin queens in the nest, but honeybees do not. It also explains why in honeybees the mother queen leaves to found a new nest, while in stingless bees it is the daughter queen who leaves.

Unicolonial ants: where do they come from, what are they and where are they going?

Unicolonial ant populations are the most extensive cooperative units known in nature, forming networks of interconnected nests extending sometimes hundreds of kilometers. Within such a supercolony, worker altruistic behavior might be maladaptive, because it seems to aid random members of the population instead of relatives. However, recent genetic and behavioral data show that, viewed on a sufficiently large scale, unicolonial ants do have colony boundaries that define very large kin groups. It seems likely that they are family groups that continue to express their kin-selected behavior as they grow to extreme sizes. However, at extreme sizes, kin selection theory predicts that these behaviors are maladapted and evolutionarily unstable, a prediction that is supported by their twiggy phylogenetic distribution.