Mating system evolution and worker caste diversity in Pheidole ants.

The efficiency of social groups is generally optimized by a division of labour, achieved through behavioural or morphological diversity of members. In social insects, colonies may increase the morphological diversity of workers by recruiting standing genetic variance for size and shape via multiply mated queens (polyandry) or multiple-breeding queens (polygyny). However, greater worker diversity in multi-lineage species may also have evolved due to mutual worker policing if there is worker reproduction. Such policing reduces the pressure on workers to maintain reproductive morphologies, allowing the evolution of greater developmental plasticity and the maintenance of more genetic variance for worker size and shape in populations. Pheidole ants vary greatly in the diversity of worker castes. Also, their workers lack ovaries and are thus invariably sterile regardless of the queen mating frequency and numbers of queens per colony. This allowed us to perform an across-species study examining the genetic effects of recruiting more patrilines on the developmental diversity of workers in the absence of confounding effects from worker policing. Using highly variable microsatellite markers, we found that the effective mating frequency of the soldier-polymorphic P. rhea (avg. meN = 2.65) was significantly higher than that of the dimorphic P. spadonia (avg. meN = 1.06), despite a significant paternity skew in P. rhea (avg. B = 0.10). Our findings support the idea that mating strategies of queens may co-evolve with selection to increase the diversity of workers. We also detected patriline bias in the production of different worker sizes, which provides direct evidence for a genetic component to worker polymorphism.

Cooperative social clusters are not destroyed by dispersal in a ciliate.

BACKGROUND: The evolution of social cooperation is favored by aggregative behavior to facilitate stable social structure and proximity among kin. High dispersal rates reduce group stability and kin cohesion, so it is generally assumed that there is a fundamental trade-off between cooperation and dispersal. However, empirical tests of this relationship are rare. We tested this assumption experimentally using ten genetically isolated strains of a ciliate, Tetrahymena thermophila. RESULTS: The propensity for social aggregation was greater in strains with reduced cell quality and lower growth performance. While we found a trade-off between costly aggregation and local dispersal in phenotypic analyses, aggregative strains showed a dispersal polymorphism by producing either highly sedentary or long-distance dispersive cells, in contrast to less aggregative strains whose cells were monomorphic local dispersers. CONCLUSION: High dispersal among aggregative strains may not destroy group stability in T. thermophila because the dispersal polymorphism allows social strains to more readily escape kin groups than less aggregative strains, yet still benefit from stable group membership among sedentary morphs. Such dispersal polymorphisms should be common in other social organisms, serving to alter the nature of the negative impact of dispersal on social evolution.

Evolution of dispersal and life history strategies--Tetrahymena ciliates.

BACKGROUND: Considerable attention has focused on how selection on dispersal and other core life-history strategies (reproductive effort, survival ability, colonization capacity) may lead to so-called dispersal syndromes. Studies on genetic variation in these syndromes within species could importantly increase our understanding of their evolution, by revealing whether traits co-vary across genetic lineages in the manner predicted by theoretical models, and by stimulating further hypotheses for experimental testing. Yet such studies remain scarce. Here we studied the ciliated protist Tetrahymena thermophila, a particularly interesting organism due to cells being able to transform into morphs differing dramatically in swim-speed. We investigated dispersal, morphological responses, reproductive performance, and survival in ten different clonal strains. Then, we examined whether life history traits co-varied in the manner classically predicted for ruderal species, examined the investment of different strains into short- and putative long-distance dispersal, while considering also the likely impact of semi-sociality (cell aggregation, secretion of 'growth factors') on dispersal strategies. RESULTS: Very significant among-strain differences were found with regard to dispersal rate, morphological commitment and plasticity, and almost all core life-history traits (e.g. survival, growth performance and strategy), with most of these traits being significantly intercorrelated. Some strains showed high short-distance dispersal rates, high colonization capacity, bigger cell size, elevated growth performance, and good survival abilities. These well performing strains, however, produced fewer fast-swimming dispersal morphs when subjected to environmental degradation than did philopatric strains performing poorly under normal conditions. CONCLUSION: Strong evidence was found for a genetic covariation between dispersal strategies and core life history traits in T. thermophila, with a fair fit of observed trait associations with classic colonizer models. However, the well performing strains with high colonization success and short-distance dispersal likely suffered under a long-distance dispersal disadvantage, due to producing fewer fast-swimming dispersal morphs than did philopatric strains. The smaller cell size at carrying capacity of the latter strains and their poor capacity to colonize as individual cells suggest that they may be adapted to greater levels of dependency on clone-mates (stronger sociality). In summary, differential exposure to selection on competitive and cooperative abilities, in conjunction with selective factors targeting specifically dispersal distance, likely contributed importantly to shaping T. thermophila dispersal and life history evolution.

The evolution of worker caste diversity in social insects.

Morphological diversification of workers is predicted to improve the division of labor within social insect colonies, yet many species have monomorphic workers. Individual-level selection on the reproductive capacities of workers may counter colony-level selection for diversification, and life-history differences between species (timing of caste determination, colony size, genetic variation available) may mediate the strength of this selection. We tested this through phylogenetically independent contrast analyses on a new data set for 35 ant species. Evidence was found that early divergence of queen-worker developmental pathways may facilitate the evolution of worker diversity because queen-worker dimorphism was strongly positively associated with diversity. By contrast, risks for colonies that invest in specialized workers and colony size effects on costs of worker reproduction seem unlikely to strongly affect the evolution of worker diversity because there was no significant association between colony size and diversity when controlling statistically for queen-worker dimorphism. Finally, worker diversity was greater in species with multiple lineages per colony, and it was negatively associated with relatedness in monogynous species. This could be due to high intracolonial genetic variance favoring the expression and evolution of great worker diversity or to diversity evolving more easily when there is selection for repression of worker reproduction (worker policing).

Control of body size of Lasius niger ant sexuals--worker interests, genes and environment.

In most animals, the survival and reproductive success of males and females is linked to their size. The ability of individuals to control environmental influences on size will therefore have consequences for their fitness. In eusocial insects, individual males and reproductive females do not have to forage for themselves or control their local environment. Instead, they are reared by nonreproductive siblings (workers) inside colonies. Workers should benefit from controlling the size of sexuals because these sexuals are usually the only means for workers to transmit their genes to future generations. Nevertheless, considerable intraspecific variation exists around mean sexual size in social hymenopterans, even in species with monomorphic sexuals. This variation could result from genetic influences on sexual size, for instance sexuals may be selected to not agree to worker interests, or be due to strong, unpredictable environmental conditions constraining the efforts of workers to control sexual size. In a study that is the first of its kind I investigated genetic and environmental components of sexual body size variation in the ant Lasius niger, examining sexuals from wild colonies with one or several fathers (paternity levels established through microsatellite DNA offspring analysis). Evidence was found for a genetic component of size (broad-sense heritability of up to 42%) but strong common-colony effects (among-colony variation in food availability or in worker capacities to restrain sexual selfishness) also increased the size differences among colonies. Workers thus seem to only have partial-control over sexual size, but may be doing the best of a bad job.

Relationships between phenotype, mating behavior, and fitness of queens in the ant Lasius niger.

Considerable attention has focused on why females of many species mate with several males. For social hymenopteran insects, efforts have primarily concentrated on determining whether multiple mating increases colony performance due to the increased genetic diversity. Most of these studies are correlative because it is difficult or impossible to experimentally mate queens in most species. Thus, the positive associations found between multiple paternity and colony fitness in some cases may not be due to direct effects of genetic diversity but could, in theory, arise from high-quality queens having more mates. Here we show that in the ant Lasius niger variation in the number of matings covaries with queen phenotype. Young queens that were heavier at the time of the mating flight were significantly more likely to mate with several males. As a result, heavier queens stored more sperm. The initial weight of queens was significantly associated with the probability of surviving mating flights during the two years of the study, with queens of intermediate weight having the highest across-year survival. Queen initial weight was also significantly and positively associated with the quantity of brood at the time of the first worker eclosion as well as colony productivity at the time of hibernation. By contrast, there was little evidence for a positive effect of the number of matings on colony performance when the effect of mate number and queen initial weight were considered simultaneously.

Why do some social insect queens mate with several males? Testing the sex-ratio manipulation hypothesis in Lasius niger.

Although multiple mating most likely increases mortality risk for social insect queens and lowers the kin benefits for nonreproductive workers, a significant proportion of hymenopteran queens mate with several males. It has been suggested that queens may mate multiply as a means to manipulate sex ratios to their advantage. Multiple paternity reduces the extreme relatedness value of females for workers, selecting for workers to invest more in males. In populations with female-biased sex ratios, queens heading such male-producing colonies would achieve a higher fitness. We tested this hypothesis in a Swiss and a Swedish population of the ant Lasius niger. There was substantial and consistent variation in queen mating frequency and colony sex allocation within and among populations, but no evidence that workers regulated sex allocation in response to queen mating frequency; the investment in females did not differ among paternity classes. Moreover, population-mean sex ratios were consistently less female biased than expected under worker control and were close to the queen optimum. Queens therefore had no incentive to manipulate sex ratios because their fitness did not depend on the sex ratio of their colony. Thus, we found no evidence that the sex-ratio manipulation theory can explain the evolution and maintenance of multiple mating in L. niger.