Causes and consequences of brain size evolution : a global analysis on birds

Why some vertebrate lineages, including humans, evolved large brains is one of the main puzzles in evolutionary biology. Of the many hypotheses that have been launched to try to resolve this puzzle, environmental variability stands out as a major cause of relative brain size variation. More formally, the cognitive buffer hypothesis (CBH) postulates that relatively large brains evolved to facilitate behavioural adjustments to enhance survival under changing conditions. The rationale of the CBH is that advanced cognition can increase fitness in varying environments by enhancing information gathering and learning, facilitating for instance shifts between different feeding sites or food types to alleviate periods of food scarcity. While the CBH has received ample empirical support in recent years, some authors have questioned its relevance to account for the evolution of enlarged brains on the grounds that maintaining the brain during periods of food scarcity may be excessively costly, so environmental variability should constrain rather than favour the evolution of large brains. The present PhD thesis explores the causes and consequences of the CBH, validating its assumptions, testing its predictions and assessing its evolutionary implications. It takes advantage of a large database on brain size comprising more than 1900 extant bird species in combination with recently developed phylogenetic comparative methods to elucidate the origins of brain size variation in the most diverse vertebrate class. As a first objective, the thesis validates the extent to which relative brain size is a good proxy of the brain structures involved in the capacity to construct behavioural responses to new challenges. Chapter 1 thus shows that the associative areas of the brain, classically related with general intelligence, are disproportionally larger in large brained species and accurately predict variation in the whole brain, therefore validating its use in broader comparative analyses. According to the CBH, species living in regions with higher environmental variation should be selected for larger brains, unless they have adaptive specialisations to avoid drops in resource availability. Chapter 2 shows that birds living in highly seasonal and unpredictable environments, like high-latitude regions, possess relatively large brains than residents from other regions, supporting the CBH in birds. Additional support for the hypothesis is found in Chapter 3, where birds colonizing oceanic islands seem to evolve relatively larger brains than their continental relatives. These changes seem to be in part caused by the increased uncertainty in resource availability that characterizes islands, which together with limited chances to disperse and a trend toward slower life-history strategies can facilitate the evolution of enlarged brains. Finally, Chapter 4 explores the active role of brain size on evolution. As predicted by the behavioral drive hypothesis, frequent behavioral changes as a response to environmental challenges should expose individuals to new sets of selective pressures, thereby favouring evolutionary divergence from the ancestors. Chapter 4 provides evidence for the behavioural drive hypothesis, showing that avian lineages with relatively large brained have experienced higher diversification rates than those with smaller brains. This finding is in line with the view that animals are not passive agents of selection, but by actively modifying its relationship with their environment also influence their own pace of evolution. Overall, the findings of the present thesis provide empirical support for the CBH, showing that a relatively large brain functions, and hence may have evolved, to cope with environmental changes, and that the evolution of enlarged brains may subsequently influence the evolutionary diversification of the lineage.