Rapid evolution of robustness following colonization of a new environment

Cameron Ghalambor
Université de Trondheim, Norvège
The relationship between patterns of phenotypic plasticity observed within a generation and adaptive
evolutionary change observed across generations has long been of interest to evolutionary biologists. For
example, concepts such as the Baldwin Effect, genetic assimilation, and genetic accommodation seek to provide
a general framework for how natural selection acts on plasticity and leads to adaptive evolution. However, a core
issue that arises is whether the direction of plastic responses are largely aligned (adaptive) or misaligned (nonadaptive)
with adaptive evolutionary trajectories. Evidence for both relationships have been observed, leading to
debate over whether a generalized role for plasticity can be inferred during adaptive evolution. Here I argue that
the relationship between plasticity is dependent on 1) the time scale over which evolutionary divergence is
examined, and 2) whether the traits being examined ultimately function to buffer environmental variation (i.e.
resist change) or track environmental variation (i.e. embrace change). I will present results showing how patterns
of gene expression evolve across generations by following experimental introductions of Trinidadian guppies
that were transplanted from a site with predators to sites without major predators. After three generations in the
new environment, we find replicated evidence for a misaligned response between the direction of ancestral
plasticity and evolution in a subset of genes thought to be under strong selection, suggesting non-adaptive
plasticity results in strong directional selection. However, this pattern is transient and over longer time periods is
reversed, such that introduced populations evolve patterns of gene expression that become more similar to their
ancestral state and less plastic. These results are more consistent with the evolution of robustness in the gene
regulatory network and a return to the initial homeostatic conditions that buffers environmental conditions. Such
results suggest that the relationship between plasticity and evolutionary divergence will change as populations
becoming locally adapted to new environments and that it is important to distinguish between traits and
functions that buffer versus track environmental variation when interpreting the relationship between plasticity
and adaptive evolution.