Luck can explain the positive link between fecundity and longevity: the Matthew effect in social insects and beyond

The universality of the trade-off between fecundity and longevity in life-history theory is sometimes contested. Social insects present the arguably strongest challenge, as (i) queens not only monopolize reproduction, but also live much longer than workers, and (ii) within a caste, those individuals that lay more eggs are also observed to live longer. Positive fecundity-longevity relationships can appear in observational data even though an underlying trade-off exists, as individual variation in resource acquisition (e.g., variation in habitat quality) can mask the trade-off. Here, we demonstrate theoretically that the fecundity-longevity trade-off in social insects can be easily masked even without differences in individual quality. Demographic stochasticity, caused by variable worker lifespans, leads to self-reinforcing dynamics (equivalent to the well-known Matthew effect), where "lucky" colonies exhibit healthy growth and long-lived, productive queens, while "unlucky" colonies show the opposite combination of traits. Allocation variation between individual queens, if present, can unmask the trade-off in principle, but the trade-off remains commonly concealed not only when measuring fecundity as a cumulative total (a strongly confounded measure as longer-lived queens have more time to produce eggs), but also when measuring fecundity as a rate. Our results help align superorganismal fitness components with general life-history principles, and highlight the necessity of experimental manipulations when making statements regarding trade-offs or the lack thereof.