The ‘big houses‐big cars dilemma’: How do we reconcile the prevalence of positive correlations among life history traits?

Life history theory assumes that there are negative correlations among different components of the life history—investing more in reproduction now means taking resources away from growth, maintenance or the ability to reproduce in the future. The discovery of positive genetic covariances between life‐history traits usually assumed to trade‐off against each other raises an important question: is life‐history theory misguided or are empirical studies overlooking some crucial information?

We explore the latter possibility with two cases of such paradoxical results—the positive correlations among life history traits described by Ken Spitze for Daphnia pulex and by us for guppies. In each case, we encounter phenotypic correlations that are the opposite of what we would expect if such trade‐offs governed life histories evolution.

For Daphnia , the correlations imply the presence of phenotypes that grow faster, attain larger body sizes and invest more in reproduction than the alternative phenotypes present within the same population at the same time.

For guppies, the evolved differences between populations, as evaluated in a common garden setting, suggest that guppies adapted to high‐predation environments are unconditionally superior to those adapted to low‐predation environments.

What Daphnia and guppies have in common is that the ‘superior’ phenotypes are only superior in resource‐rich environments. The alternative phenotypes emerge as superior in resource poor environments.

Trade‐offs are manifested through these interactions between genotype and environment. For Daphnia , the alternatives are defined by adaptations to predictable seasonal changes in resource availability.

For guppies, the alternatives are adapted to different localities associated with differences in risks of predation, population density, co‐adaptation with other fish species and resource availability. Guppy population density is low and resource availability is high in environments with abundant predators. In the absence of predators, guppy population density is high, they deplete the environment of resources and interactions with the other fish species intensify because of the increased abundance of both species. These conditions favour phenotypes that had appeared to be unconditionally inferior in resource‐rich environments.