Alan A. Cohen, Christophe Coste, Xiang-Yi Li, Salomé Bourg and Samuel Pavard
Why do we age? Since a given cell contains all the DNA necessary to manufacture an entire organism, why not just keep going indefinitely to reproduce more and maximize fitness? The currently accepted answer to that question largely relies on the idea of trade-offs: that by accepting some aging, we can increase reproduction or other aspects of function while young, and thereby maximize total fitness. While there is substantial support for this idea in the literature, there are also many emerging reasons to think it’s not the whole story, notably some species that don’t age, or that age in unusual ways. In this review, we look at empirical studies that have supported – or failed to support – the idea that trade-offs underlie the evolution of aging. We look at theoretical reasons why trade-offs are likely to be weaker than generally thought. And we look at what we know about mechanisms of aging, showing that while some mechanisms lend themselves easily to evolutionary adjustment via trade-offs, others appear much harder to modulate, and are thus what we call constraints. For example, tooth wear is an aging mechanism that cannot be adjusted by changing our reproductive rates; other molecular aging mechanisms are similarly insulated from adjustment via trade-offs. Putting all this together, we propose a new way to understand aging and how it evolves across species. Trade-offs and constraints interact to determine aging rate, but their relative importance varies greatly depending on the group of species in question. In birds and mammals, trade-offs appear to predominate, but among reptiles and fish, for example, constraints might be more important. This new framework is important for several reasons. First, it explains why we don’t always detect trade-offs when we look for them, and suggests that we will need to make much more nuanced predictions. Second, it implies that the evolutionary mechanisms underlying aging are multiple and vary across the tree of life. Third, it suggests that we should start to consider aging mechanisms in light of how they might evolve, in order to understand aging in the species they affect.