Eusociality through conflict dissolution

Eusociality, where largely unreproductive offspring help their mothers reproduce, is a major form of social organization in social insects and other animals. An increasingly documented feature of eusociality is that mothers induce their offspring to help by means of hormones, pheromones, or behavioral displays, with evidence often indicating that offspring help voluntarily. The co-occurrence of widespread maternal influence and voluntary offspring help may be explained by what we call the converted helping hypothesis, whereby helping originally arising from maternal manipulation subsequently becomes voluntary. This hypothesis requires that parent-offspring conflict is eventually dissolved—for instance, if the benefit of helping increases sufficiently over evolutionary time. Here we show that maternal manipulation of offspring help enables the mother to increase her fertility to such extent that parent-offspring conflict is transformed into parent-offspring agreement. Such conflict dissolution mechanism requires that helpers alleviate the total percent life-history trade-off limiting maternal fertility, and results in reproductive division of labor, high queen fertility, and honest queen signaling suppressing worker reproduction, thus exceptionally recovering diverse features of eusociality. This mechanism is widely applicable, thus suggesting a general explanation for the origin of eusociality, the prevalence of maternal influence, and the offspring’s willingness to help. Overall, our results explain how a major evolutionary transition can happen from ancestral conflict.

Maternal Effects and Parent-Offspring Conflict

Maternal effects can provide offspring with reliable information about the environment they are likely to experience, but also offer scope for maternal manipulation of young when interests diverge between parents and offspring. To predict the impact and outcome of parent-offspring conflict, we model the evolution of maternal effects on local adaptation of young. We find that parent-offspring conflict strongly influences the stability of maternal effects; moreover, the nature of the disagreement between parents and young predicts how conflict is resolved: when mothers favour less extreme mixtures of phenotypes relative to offspring (i.e., when mothers stand to gain by hedging their bets), mothers win the conflict by providing offspring with only limited amounts of information. When offspring favour overproduction of one and the same phenotype across all environments compared to mothers (e.g., when offspring favour a larger body size), neither side wins the conflict and signaling breaks down. Only when offspring favour less extreme mixtures relative to their mothers (the case we consider least likely), offspring win the conflict and obtain full information about the state of the environment. We conclude that a partial or complete breakdown of informative maternal effects will be the norm rather than the exception in the presence of parent-offspring conflict.

Cryptic male choice: experimental evidence of sperm sex ratio and seminal fluid adjustment in relation to coital rate

The differential allocation hypothesis suggests that a mother should adjust the sex of offspring in relation to her mate’s attractiveness, thereby increasing future reproductive fitness when her sons inherit the attractive traits. More attractive males have been shown to sire more sons, but it is possible that the sex ratio skew could be a result of paternal rather than maternal manipulation, which would be a more parsimonious explanation. We manipulated coital rate (an indicator of attractiveness) in laboratory mice and showed that males that mate more often have higher levels of glucose in their semen despite lower blood glucose levels. Since peri-conceptual glucose levels in utero increase male conceptus survival, this could result in male-biased sex ratios. The males that mated most also had more remaining X-chromosome-bearing-spermatozoa, suggesting depletion of Y-chromosome-bearing-spermatozoa during mating. We hypothesise that males may alter both seminal fluids and X : Y ratios in an ejaculate to influence subsequent sex ratios. Our results further support a paternal role in sex allocation.

Stable eusociality via maternal manipulation when resistance is costless

In many eusocial species, queens use pheromones to influence offspring to express worker phenotypes. While evidence suggests that queen pheromones are honest signals of the queen's reproductive health, here I show that queen's honest signaling can result from ancestral maternal manipulation. I develop a mathematical model to study the coevolution of maternal manipulation, offspring resistance to manipulation, and maternal resource allocation. I assume that (1) maternal manipulation causes offspring to be workers against offspring's interests; (2) offspring can resist at no direct cost, as is thought to be the case with pheromonal manipulation; and (3) the mother chooses how much resource to allocate to fertility and maternal care. In the coevolution of these traits, I find that maternal care decreases, thereby increasing the benefit that offspring obtain from help, which in the long run eliminates selection for resistance. Consequently, ancestral maternal manipulation yields stable eusociality despite costless resistance. Additionally, ancestral manipulation in the long run becomes honest signaling that induces offspring to help. These results indicate that both eusociality and its commonly associated queen honest signaling can be likely to originate from ancestral manipulation.