Competition Drives Group Formation and Reduces Within Nest Relatedness in a Facultatively Social Carpenter Bee

Animals respond to competition among kin for critical breeding resources in two ways: avoidance of direct fitness costs via dispersal of siblings to breed separately, and formation of kin-based societies in which subordinates offset direct fitness costs of breeding competition via altruism and increased indirect fitness. In the facultatively social eastern carpenter bee, nests are a critical breeding resource in perpetually short supply, leading to strong competition among females. Observations of individually marked and genotyped females in conditions of high and low resource competition demonstrate that competition leads to resource sharing and group nesting. However, in contrast to almost all known animal societies, females avoid nesting with relatives, and disperse from their natal nests to join social groups of non-relatives. This is the first example of a structured insect society with cooperation nestmates, the majority of which are unrelated; thus cooperation is more likely based on selection for direct, rather than indirect fitness. By forming social groups of non-kin, females avoid the indirect fitness costs of kin competition among sisters, yet increase their chances of successful reproduction, and thus direct fitness, when forming colonies of non-relatives.

Nutrition induced direct fitness for workers in a primitively eusocial wasp

Eusocial insects are characterised by a reproductive caste differentiation such that egg-laying is restricted to a small number of queens. The majority of the colony members function as non-reproducing workers and gain indirect fitness by rearing the offspring of the reproductives. In primitively eusocial species, some workers can also get direct fitness by sneaking in some eggs in the presence of the queens, replacing the queens and becoming new queens, or initiating new nests. Here we aimed to understand the factors that permit some workers to gain direct fitness and alter the number of workers doing so, using the primitively eusocial wasp Ropalidia marginata. We transplanted 12 naturally occurring colonies into large laboratory cages where there was adequate space for the workers to leave their natal nests and initiate new colonies. We compared six control colonies that we provided with ad libitum food placed near the nest to six test colonies in which we hand-fed the wasps in addition to the ad libitum food. Wasps in test colonies consumed more food, showed more aggression, replaced their queens, and initiated new nests significantly more often than those in control colonies. When considering all 12 colonies, the rates of queen replacement and nest foundation were significantly positively correlated with food consumption rates. The additional nutrition gained by hand-fed wasps appears to help workers in test colonies to develop their ovaries and lay eggs, implying that they are nutritionally castrated in control colonies.

Lifetime reproductive benefits of cooperative polygamy vary for males and females in the acorn woodpecker ( Melanerpes formicivorus )

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers ( Melanerpes formicivorus ), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.

Aggression towards neonates and possible infanticide in the boto, or Amazon river dolphin (Inia geoffrensis)

Recent observed attacks by male Amazon river dolphins on conspecific calves, together with post-mortem examinations, indicate that infanticide occurs in this species but that not all attacked calves are killed. If mortality occurs, it might therefore be an inadvertent consequence of the behaviour rather than the motive for it. Our observations suggest that males who commit infanticide are unlikely to gain direct fitness benefits. Evidence does not fit the sexual selection hypothesis. Aggression towards calves usually ‘drew a crowd’ and may represent socio-sexual display or simply be a form of social pathology, as found in other infanticidal mammals.

An evolutionary perspective on kin care directed up the generations

Within evolutionary sciences, care towards younger kin is well understood from an inclusive fitness framework, but why adults would care for older relatives has been less well researched. One existing model has argued that care directed towards elderly parents might be adaptive because of their benefits as carers themselves, with their help freeing up the middle generations’ energy which can then be invested into direct reproduction. However, in this model, elder care is more beneficial to fitness if the carer is fecund. To offer an initial test of this hypothesis, we look at caring behaviour relative to fecundity status in a contemporary dataset from the United Kingdom. If elder care is contingent on possible direct fitness benefits, we would expect women who are still menstruating to care more for their parents than women who can no longer reproduce. Based on this, we also predict that women who are physiologically post-reproductive would invest more in their grandchildren, through whom they can increase their inclusive fitness. After controlling for age and other relevant factors, we find that women who are still menstruating spend more time caring for their parents than those who are not, and the reverse is true when looking at time spent caring for grandchildren. These findings demonstrate that potential inclusive fitness outcomes influence how women allocate care up and down the generations.

Cell-growth gene expression reveals a direct fitness cost of grazer-induced toxin production in red tide dinoflagellate prey

Induced prey defences against consumers are conspicuous in microbes, plants and animals. In toxigenic prey, a defence fitness cost should result in a trade-off between defence expression and individual growth. Yet, previous experimental work has failed to detect such induced defence cost in toxigenic phytoplankton. We measured a potential direct fitness cost of grazer-induced toxin production in a red tide dinoflagellate prey using relative gene expression (RGE) of a mitotic cyclin gene ( cyc ), a marker that correlates to cell growth. This approach disentangles the reduction in cell growth from the defence cost from the mortality by consumers. Treatments where the dinoflagellate Alexandrium catenella were exposed to copepod grazers significantly increased toxin production while decreasing RGE of cyc , indicating a defence-growth trade-off. The defence fitness cost represents a mean decrease of the cell growth rate of 32%. Simultaneously, we estimate that the traditional method to measure mortality loss by consumers is overestimated by 29%. The defence appears adaptive as the prey population persists in quasi steady state after the defence is induced. Our approach provides a novel framework to incorporate the fitness cost of defence in toxigenic prey–consumer interaction models.

Oxidative costs of cooperation in cooperatively breeding Damaraland mole-rats

Within cooperatively breeding societies, individuals adjust cooperative contributions to maximize indirect fitness and minimize direct fitness costs. Yet, little is known about the physiological costs of cooperation, which may be detrimental to direct fitness. Oxidative stress, the imbalance between reactive oxygen species (by-products of energy production) and antioxidant protection, may represent such a cost when cooperative behaviours are energetically demanding. Oxidative stress can lead to the accumulation of cellular damage, compromising survival and reproduction, thus mediating the trade-off between these competing life-history traits. Here, we experimentally increased energetically demanding cooperative contributions in captive Damaraland mole-rats ( Fukomys damarensis ). We quantified oxidative stress-related effects of increased cooperation on somatic and germline tissues, and the trade-off between them. Increased cooperative contributions induced oxidative stress in females and males, without increasing somatic damage. Males accumulated oxidative damage in their germline despite an increase in antioxidant defences. Finally, oxidative damage accumulation became biased towards the germline, while antioxidant protection remained biased towards the soma, suggesting that males favour the maintenance of somatic tissues (i.e. survival over reproduction). Our results show that heightened cooperative contributions can ultimately affect direct fitness through oxidative stress costs, which may represent a key selective pressure for the evolution of cooperation.