Cooperation among unrelated ant queens provides persistent growth and survival benefits during colony ontogeny

The fitness consequences of cooperation can vary across an organism’s lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-queen colonies of the primary polygynous harvester ant, Pogonomyrmex californicus, from founding through the first ten months of colony growth, when groups face high mortality risks. We found that colonies founded by multiple, unrelated queens experienced significant survival and growth advantages that outlasted the colony founding period. Multi-queen colonies experienced lower mortality than single-queen colonies, and queens in groups experienced lower mortality than solitary queens. Further, multi-queen colonies produced workers at a faster rate than did single-queen colonies, even while experiencing lower per-queen worker production costs. Additionally, we characterized ontogenetic changes in the organization of labor, and observed increasing and decreasing task performance diversity by workers and queens, respectively, as colonies grew. This dynamic task allocation likely reflects a response to the changing role of queens as they are increasingly able to delegate risky and costly tasks to an expanding workforce. Faster worker production in multi-queen colonies may beneficially accelerate this behavioral transition from a vulnerable parent–offspring group to a stable, growing colony. These combined benefits of cooperation may facilitate the retention of multiple unrelated queens in mature colonies despite direct fitness costs, providing insight into the evolutionary drivers of stable associations between unrelated individuals.

Sex allocation conflict and sexual selection throughout the lifespan of eusocial colonies

Models of sex allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen-worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, male-biased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex-allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.

Termite colony ontogeny: supplemental data in the long-term assessment of reproductive lifespan, female neotenic production and colony size in Reticulitermes flavipes (Isoptera: Rhinotermitidae)

Reticulitermes flavipes (Kollar) colonies established by field-collected alates were reared in the laboratory for 11 years. Weights of members of each caste and full-colony censuses were performed regularly; the most recent 2003–2004 data are reported. Colonies averaged 11623.5±910 individuals, and with the exception of primary queens from one genetic lineage, mean weights for all castes had increased since 2001. Female replacement reproductives, or neotenics, developed to replace dead queens in clusters of either few, large individuals or many, small individuals. Regardless of cluster size, female neotenics comprised more reproductive biomass per colony than primary queens. The number and size of female neotenics was independent of colony size or time elapsed since a founding queen's death.

Termite colony ontogeny: a long-term assessment of reproductive lifespan, caste ratios and colony size in Reticulitermes flavipes (Isoptera: Rhinotermitidae)

Thirty Reticulitermes flavipes (Kollar) colonies established by alates collected from two separate field sites were raised in the laboratory for eight years. Twenty-one of the colonies were founded by alates from one field source and nine from another, providing demographic data from two unrelated parental lineages. Colony totals ranged from 3620 to 11641 individuals, with no significant difference in size between lineages. Soldier caste proportion of the colony total and mean wet weights for workers, soldiers and kings were significantly different between the two lineages. This suggests that at least a portion of the variability observed in caste ratios and body size may be heritable. One founding reproductive had died in five of the colonies (17%); none lost both parents. The queenless colonies contained exclusively female replacement reproductives (neotenics); the kingless colony contained a female-skewed mixture of male and female neotenics. All the nests that lost a founding parent contained significantly more pre-alate nymphs than the nests with both a king and a queen. Comparisons with published reports of ontogenetic patterns in other termites and social insects are discussed.