Light enough to travel or wise enough to stay? Brain size evolution and migratory behavior in birds

Abstract

Brain size relative to body size is smaller in migratory than in nonmigratory birds. Two mutually nonexclusive hypotheses had been proposed to explain this association. On the one hand, the "energetic trade-off hypothesis" claims that migratory species were selected to have smaller brains because of the interplay between neural tissue volume and migratory flight. On the other hand, the "behavioral flexibility hypothesis" argues that resident species are selected to have higher cognitive capacities, and therefore larger brains, to enable survival in harsh winters, or to deal with environmental seasonality. Here, I test the validity and setting of these two hypotheses using 1466 globally distributed bird species. First, I show that the negative association between migration distance and relative brain size is very robust across species and phylogeny. Second, I provide strong support for the energetic trade-off hypothesis, by showing the validity of the trade-off among long-distance migratory species alone. Third, using resident and short-distance migratory species, I demonstrate that environmental harshness is associated with enlarged relative brain size, therefore arguably better cognition. My study provides the strongest comparative support to date for both the energetic trade-off and the behavioral flexibility hypotheses, and highlights that both mechanisms contribute to brain size evolution, but on different ends of the migratory spectrum.

Environmental variation and the evolution of large brains in birds

“…This finding is consistent with the view that a relatively larger brain is useful not only in harsh regions (for example, high latitudes with cold winters)3233, but also in more benign regions that exhibit substantial year-to-year variation in environmental conditions11. Although the model explains over 87% of variation in absolute brain size, only 4% of this variation can be attributed to the environmental variation axes.…”

“…4c, Supplementary Table 15). In addition, long distance migrants have a smaller brain optimum compared with residents, further confirming previous evidence2433, and exhibit lower variation around this optimum perhaps reflecting a trade-off between brain size and the costs of locomotion44.…”

A model for brain life history evolution

“…For instance, increasingly challenging environments favor large brains up to a point, so that exceedingly challenging environments disfavor large brains. Thus, on the low end of environmental difficulty, the prediction that increasingly challenging environments favor large brains is consistent with ecological challenge hypotheses [45, 46, 111]; yet, on the high end of environmental difficulty, the prediction that increasingly challenging environments disfavor large brains is consistent with constraint hypotheses according to which facilitation of environmental challenge favors larger brains [46, 112–114]. Counter-intuitively on first encounter, the finding that moderately effective skills are most conducive to a large brain and high skill is a consequence of the need of higher skill when skill effectiveness decreases (Fig 6B).…”

Large-brained frogs mature later and live longer

“…; Sayol et al. ; Vincze ). Indeed large‐brained birds and mammals survive better in novel environments (Sol et al., , ), which supports the brain size longevity correlation hypothesis in mammals (Allman et al.…”