Liselotte Sundström

Informational constraints on optimal sex allocation in ants

Workers of the ant Formica truncorum specialize in rearing females or males depending on the number of fathers of a colony. These split sex ratios increase inclusive fitness, but it has remained unknown how workers assess the number of patrilines in their colonies and to what extent their reproductive decisions are constrained by lack of information. By analysis of the quantitative variation in cuticular hydrocarbon profiles of workers of multiply mated queens, we show that the heritable component of recognition cues is low and that the extent of sex ratio biasing toward males is correlated with patriline differences in hydrocarbon profiles. Workers are thus able to capitalize on colony-level relatedness asymmetry, but their inclusive fitness is constrained by uninformative recognition cues. These results are consistent with the hypothesis that the occasional expression of nepotistic phenotypes favoring full-sisters over half-sisters maintains selection against informative recognition cues. We evaluate how inclusive fitness theory may be used to predict the number and kind of recognition cues in insect societies of a specific relatedness structure.

Genetic population structure and sociogenetic organisation in Formica truncorum (Hymenoptera; Formicidae)

SummaryThe genetic population structure and the sociogenetic organization of the red wood ant Formica truncorum were compared in two populations with monogynous colonies and two populations with polygynous colonies. The genetic population structure was analysed by measuring allele frequency differences among local subsets of the main study populations. The analysis of sociogenetic organisation included estimates of nestmate queen and nestmate worker relatedness, effective number of queens, effective number of matings per queen, relatedness among male mates of nestmate queens and relatedness between queens and their male mates. The monogynous populations showed no differentiation between subpopulations, whereas there were significant allele frequency differences among the subpopulations in the polygynous population. Workers, queens and males showed the same genetical population structure. The relatedness among nestmate workers and among nestmate queens was identical in the polygynous societies. In three of the four populations there was a significant heterozygote excess among queens. The queens were related to their male mates in the polygynous population analysed, but not in the monogynous ones. The data suggest limited dispersal and partial intranidal mating in the populations with polygynous colonies and outbreeding in the populations having monogynous colonies. Polyandry was common in both population types; about 50% of the females had mated at least twice. The males contributed unequally to the progeny, one male fathering on average 75% of the offspring with double mating and 45–80% with three or more matings.

Diploid males and colony-level selection in Formica ants

It is suggested that the evolution of polyandry by social hymenopteran queens is caused by colony-level selection, either because polyandry affects the distribution of non-functional diploid males in colonies (the load hypothesis) or because it increases the genetic diversity of the worker force (the diversity hypothesis). Diploid males that arise from fertilized eggs thai are homozygous at the sex-determining locus (or loci) are inviable or infertile. Models of the load hypothesis analysed in this study suggest that slow growth and high mortality of colonies with diploid males favour single mating by queens. The longer the period ol colony growth (the period with selective differences) and the heavier the mortality, the stronger is the selection for monandry. The load hypothesis also predicts an association between monogyny and monandry. In contrast, the diversity hypothesis predicts an association between monogyny and polyandry, as multiple mating offers a way by which a monogynous colony could increase...

Sociobiology: Worker nepotism among polygynous ants

Insect societies are a prime example of extreme cooperation, but their social life also entails the pursuit of selfish interests by society members. Here we show that workers of the ant Formica fusca favour their own close kin when rearing eggs and larvae in colonies that are derived from several queens. This nepotistic behaviour indicates that ant workers are able not only to detect kin relationships, but also to pursue their selfish genetic interests if the costs to their colony are not prohibitive.

Queen acceptance and nestmate recognition in monogyne and polygyne colonies of the antFormica truncorum

In ants permanent polygyny (the permanent presence of multiple reproducing queens) commonly arises secondarily through the adoption of daughter queens. Polygyny decreases the relatedness among nestmate workers and consequently the genetic benefits from helping close relatives. Hence, studies on nestmate recognition and queen adoption may shed light on how queen numbers are regulated as well as on causes of variation in queen number. In this study acceptance of nestmate and non-nestmate young queens in monogyne (single queen) and polygyne colonies of the antFormica truncorumwas compared. Queen number varies in this species: in some populations colonies have a single queen (monogyne populations), whereas in others all colonies contain several functional queens (polygyne populations). Young queens introduced into the experimental colonies varied with respect to female origin (nestmate versus non-nestmate), dispersal prospects as reflected by wing status (wingless versus winged) and mating status (mated versus virgin). Monogyne and polygyne colonies differed in one fundamental way in their responses to introduced females. Workers of monogyne colonies, but not those of polygyne colonies, discriminated between nestmate and non-nestmate females. In both monogyne and polygyne colonies mated females were destroyed to a higher extent than virgin ones, largely independently of wing status. None the less, mated females may have a reasonable chance of becoming adopted in their natal colony both in monogyne and polygyne colonies. If so, the single-queen status of monogyne colonies may be retained by a high rate of female dispersal in combination with few intra-nidal mating opportunities. Polygyne colonies are characterized by both a low degree of female rejection and low levels of discrimination between nestmates and non-nestmates. Nevertheless, previous genetic and behavioural data on female dispersal suggest that the majority of new queens adopted into polygyne colonies are their own daughters.

Conflicts and alliances in insect families.

Hamilton’s principle of inclusive fitness implies that reproductive altruism can evolve, because individuals can pass on genes not only through their own offspring, but also through the offspring of their relatives. Social insects are spectacular examples of how some individuals may be selected to forgo reproduction and instead help others reproduce. Social Hymenoptera are also special because relatedness patterns within families can be asymmetrical, so that optimal sex-ratios, preferred male parentage or preferred mating frequencies become objects of reproductive conflict. The now extensive inclusive fitness theory provides precise qualitative predictions with respect to the emergence of such conflicts. Recent advances in the power of genetic markers applied to resolve family structure in insect societies have brought about a series of studies that have tested these predictions. In support of kin selection as a major evolutionary force, the results suggest that workers frequently control sex allocation. However, the very establishment of such worker control has made new conflicts come to light, between mothers and fathers and between adult individuals and brood. Evidence for these conflicts is only just beginning to be gathered. Recent studies tend to include issues such as ‘information’ and ‘power’ (i.e. the ability to perceive signals and the opportunity to act upon this information), and to address selection for selfishness at the individual level with costs of social disruption at the colony level.

Patterns of paternity skew in Formica ants

Reproductive skew among cooperatively breeding animals has recently attracted considerable interest. In social insects reproductive skew has been studied in females but not in males. However, cooperative breeding of males occurs when two males mate with the same queen and father offspring. Here we present the first analysis of comparative data on paternity skew in ants. We show that, across seven species of Formica ants, the average skew in paternity among worker offspring of doubly mated queens is negatively correlated with the population-wide frequency of multiple (mostly double) mating. We also demonstrate that this trend is relatively robust in additional analyses taking phylogenetic relationships between species into account. The observed trend is opposite to the one normally found in non-social insects with second-male precedence through sperm displacement, but agrees with predictions based on queen-male conflict over sperm allocation as a consequence of facultative, worker controlled, sex allocation – an interpretation which assumes first-male precedence. However, alternative (but not mutually exclusive) explanations are possible and further studies will be needed to discriminate between these alternatives.

Seasonal polydomy and unicoloniality in a polygynous population of the red wood ant Formica truncorum

Ant colonies may have a single or several reproductive queens (monogyny and polygyny, respectively). In polygynous colonies, colony reproduction may occur by budding, forming multinest, polydomous colonies. In most cases, budding leads to strong genetic structuring within populations, and positive relatedness among nestmates. However, in a few cases, polydomous populations may be unicolonial, with no structuring and intra-nest relatedness approaching zero. We investigated the spatial organisation and genetic structure of a polygynous, polydomous population of Formica truncorum in Finland. F. truncorum shifts nest sites between hibernation and the reproductive season, which raises the following question: are colonies maintained as genetic entities throughout the seasons, or is the population unicolonial throughout the season? Using nest-specific marking and five microsatellite loci, we found a high degree of mixing between individuals of the population, and no evidence for a biologically significant genetic structuring. The nestmate relatedness was also indistinguishable from zero. Taken together, the results show that the population is unicolonial. In addition, we found that the population has undergone a recent bottleneck, suggesting that the entire population may have been founded by a very limited number of females. The precise causes for unicoloniality in this species remain open, but we discuss the potential influence of intra-specific competition, disintegration of recognition cues and the particular hibernation habits of this species.

Reproductive alliances and posthumous fitness enhancement in male ants.

Ants provide excellent opportunities for studying the evolutionary aspects of reproductive conflict. Relatedness asymmetries owing to the haplodiploid sex determination of Hymenoptera create substantial fitness incentives for gaining control over sex allocation, often at the expense of the fitness interests of nest–mates. Under worker–controlled split sex ratios either the reproductive interests of the mother queen (when workers male bias the sex ratio) or the father (when workers female bias the sex ratio), but never that of both parents simultaneously, are fulfilled. When workers bias sex ratios according to the frequency of queen mating, males which co–sire a colony have a joint interest in manipulating their daughter workers into rearing a more female–biased sex ratio. Here we show that males of the ant Formica truncorum achieve such manipulation by partial sperm clumping, so that the cohort–specific relatedness asymmetry of the workers in colonies with multiple fathers is higher than the cumulative relatedness asymmetry across worker cohorts. This occurs because a single male fathers the majority of the offspring within a cohort. Colonies with higher average cohort–specific relatedness asymmetry produce more female–biased sex ratios. Posthumously expressed male genes are thus able to oppose the reproductive interests of the genes expressed in queens and the latter apparently lack mechanisms for enforcing full control over sperm mixing and sperm allocation.

Worker reproduction in ants — a genetic analysis

Workers of social insects may enhance their inclusive fitness by laying unfertilized eggs that develop into males. In particular, workers may gain from rearing worker-produced males if their average relatedness to them exceeds their relatedness to queen-produced males. These relatedness values depend both on the queen mating frequency and on the number and relatedness of nestmate queens. We examined the occurrence of worker reproduction in field colonies of four ant species of the genera Formica and Myrmica. Based on relatedness arguments alone, worker reproduction was expected in all species because of low queen mating frequency, or low effective queen numbers. Nevertheless, genotype matching of workers and males showed that worker reproduction was absent or rare in two of the three Formica species studied here. In M. ruginodis, queens may have been the sisters of the workers in many cases, which means that workers of this species may regularly rear nephews. In the three species in which worker reproduction was not found, workers bias colony sex ratios to enhance their inclusive fitness. We therefore hypothesize that sex ratio biasing and male production may be mutually exclusive strategies for workers.