Cryptic genetic variation in brain gene expression precedes the evolution of cannibalism in spadefoot toad tadpoles

The origins of novel behaviors are poorly understood, despite behavior’s
hypothesized roles in evolution. One model, “genetic accommodation”,
proposes that selection on ancestral phenotypic plasticity may precede the
evolution of novel traits. A critical assumption of genetic accommodation
is that ancestral lineages possess heritable genetic variation for trait
plasticity that is revealed in novel environments, thereby providing the
raw materials for subsequent refinement of the novel trait in derived
lineages. Here, we use a combination of behavioral and RNA-seq approaches
to test this assumption in the context of a novel tadpole behavior:
predatory cannibalism. Cannibalism evolved in the spadefoot genus Spea,
where an invertebrate diet induces a carnivorous tadpole morph capable of
consuming live conspecific tadpoles. In contrast, closely related
Scaphiopus tadpoles do not induce this carnivorous phenotype. Through
species comparisons, we found that ancestral Spea likely expressed
behavioral plasticity and harbored latent (i.e., “cryptic”) genetic
variation in brain gene expression plasticity associated with
cannibalism-inducing cues. Further, we found this cryptic genetic
variation contains genes specifically associated with a dietary response
and cannibalism in derived Spea. Our results suggest that novel behaviors,
alongside novel morphologies, can evolve via the process of genetic
accommodation. More generally, our results provide key evidence for the
plausibility of genetic accommodation, revealing for the first time that
cryptic genetic variation — the raw material for the evolution of novel
traits — exists in natural populations at the level of gene expression.