This blog post has been provided by Mike Moore, a post-doctoral fellow with the Living Earth Collaborative in St. Louis, USA. It tells the #StoryBehindThePaper for “On the evolution of carry-over effects”, a review that was short-listed for the Sidnie Manton Award. 

Simply put, the things that animals need to do in one part of the life cycle are almost always different from the things they need to do in other parts. Sometimes, these shifting demands accompany transitions between different habitats (think frogs or migratory birds). Other times, the shifting demands arise merely from the fact that juveniles must grow and survive to maturity whereas adults need to acquire mates and reproduce. Of course, these differing pressures would not pose a problem if animals could just reset their development between life-cycle stages. However, the last twenty years has borne witness to an explosion of research that documents how the conditions faced early in life often affect the traits that an animal produces later in life—even in organisms with extreme life-cycle transitions like frogs and butterflies. Thus, much like F. Scott Fitzgerald once famously remarked about life in America, there seems to be no second acts in the lives of animals either.

The life cycle of a dragonfly. Despite the dramatic transformation undertaken between life-cycle stages, the environment experienced during the larval stage often affects key traits produced in the adult stage (e.g. Moore et al. 2018; Lis et al. In Press). Photo credits: M. Moore (left and centre); I. Gherghel (right).

“Carry-over effects” occur when the environmental conditions of an earlier life-cycle stage affect traits in later stages, and researchers are increasingly recognizing them as a fundamental feature of development. Often manifesting as a cost of developing beneficial traits early in the life cycle, carry-over effects have recently captivated animal biologists because such trade-offs could resolve longstanding problems in ecology and evolution, including why some animals don’t adapt in the same way to the same environment, and why some traits fail to evolve even over tens of millions of years. Nonetheless, despite the surge in interest, no one had ever really considered the evolution of carry-over effects. As my collaborator, Ryan Martin, and I became interested in carry-over effects and trade-offs between life-cycle stages more generally, we felt that three questions needed answers. How do carry-over effects evolve? How does natural selection act on carry-over effects? What are the broader evolutionary consequences of selection on carry-over effects?

Our review of the literature uncovered two non-mutually exclusive ways that carry-over effects evolve. To start, imagine a situation where the juvenile environment causes an animal to produce traits that end up harming adult survival. First, the carry-over effect could evolve by the adult trait decoupling its development from processes that begin in the juvenile stage. Second, the carry-over effect could evolve such that environmentally sensitive feature of development simply becomes less sensitive to the environment altogether. Beyond detailing evidence for these two evolutionary outcomes, as well as means to test them, we make specific predictions for what kinds of organisms and traits are likely to evolve in each way.

Because carry-over effects span multiple life stages, it was also necessary to consider how “episodes” of natural selection in each life stage combine and interact. Here, theory from population ecology and life histories came in handy. An important, sometimes overlooked, insight from researchers working in these spheres is that life stages are not all equally important. Consequently, episodes of selection that are apparently equal in strength are actually unlikely to be equally influential. As a result, the evolution of a carry-over effect will be governed by the strength of selection in each life stage and how much each life stage contributes to population-mean fitness. Although the latter component is often studied by population ecologists, evolutionary ecologists rarely consider it, and we therefore provide a hypothetical example with frogs of how to go about estimating and integrating these parameters.

Measuring the strength and direction of natural selection on a carry-over effect. Here, when the environment induces longer development times in the tadpole stage, it results in adult frogs with longer legs. B is the relationship between each trait and each component of fitness (juvenile or adult survival) and e is the elasticity, one measure of the relationship between a vital rate and population-mean fitness. From Figure 4, Moore & Martin (2019).

In terms of the broader evolutionary consequences of selection acting on carry-over effects, we think our framework reveals two particularly exciting hypotheses. First, cases of very strong selection in one life stage may not have a huge impact on evolution if that life stage does not contribute much to population-mean fitness. This scenario may occur quite frequently, as evolutionary ecologists find that sexual selection is often the strongest form of selection, but population ecologists find that variation in survival typically contributes the most to population-mean fitness. Second, carry-over effects that result in large fitness costs for one stage might actually be adaptive if another life stage is more important. Although this idea is commonly invoked to explain the evolution of animal senescence, our framework illustrates how fitness costs should be deferred to less important life stages more generally.

Moving forward, Ryan and I hope our article fosters more attempts to evaluate how carry-over effects evolve and invites a deeper consideration about how they influence evolution in other ways. As noted by West-Eberhard (2003) in her treatise on evolution, evolutionary biology is sometimes criticized as a “theory of adults” for its common focus on adaptation in a single (usually adult) life stage at a time. Given the widespread importance of carry-over effects, the need to take a more integrative view of the entire life cycle seems more vital than ever, and the framework that we provide in this article hopefully makes addressing this topic more attainable.

More Info:

Crone 2001. Is survivorship a better fitness surrogate than fecundity? Evolution 55: 2611-2614.

Kingsolver et al. 2012. Synthetic analyses of phenotypic selection in natural populations: Lessons, limitations, and future directions. Evolutionary Ecology 26: 1101-1118.

Lis et al. In Press. Warm developmental temperatures induce non-adaptive plasticity in the intrasexually selected colouration of a dragonfly. Ecological Entomology

Mojica & Kelly 2010. Viability selection prior to trait expression is an essential component of natural selection. Proceedings of the Royal Society of London B: Biological Sciences 277: 2945-2950.

Moore et al. 2018. Immune deployment increases larval vulnerability to predators and inhibits adult life-history traits in a dragonfly. Journal of Evolutionary Biology 31, 1365-1376.

Moore & Martin 2019. On the evolution of carry-over effects. Journal of Animal Ecology 88, 1832-1844.

van Tienderen 2000. Elasticities and the link between demographic and evolutionary dynamics. Ecology 81: 666-679.

Waller & Svensson 2017. Body size evolution in an old insect order: no evidence for Cope’s Rule in spite of fitness benefits of large size. Evolution 71: 2178-2193.

West-Eberhard 2003. Developmental plasticity and evolution. Oxford UK: Oxford University Press.

Williams 1957. Pleiotropy, natural selection and the evolution of senescence. Evolution 11: 398-411.