Ecological and life history drivers of avian skull evolution

Abstract

One of the most famous examples of adaptive radiation is that of the Galapagos finches, where skull morphology, particularly the beak, varies with feeding ecology. Yet increasingly studies are questioning the strength of this correlation between feeding ecology and morphology in relation to the entire neornithine radiation, suggesting that other factors also significantly affect skull evolution. Here, we broaden this debate to assess the influence of a range of ecological and life history factors, specifically habitat density, migration, and developmental mode, in shaping avian skull evolution. Using 3D geometric morphometric data to robustly quantify skull shape for 354 extant species spanning avian diversity, we fitted flexible phylogenetic regressions and estimated evolutionary rates for each of these factors across the full dataset. The results support a highly significant relationship between skull shape and both habitat density and migration, but not developmental mode. We further found heterogenous rates of evolution between different character states within habitat density, migration, and developmental mode, with rapid skull evolution in species which occupy dense habitats, are migratory, or are precocial. These patterns demonstrate that diverse factors impact the tempo and mode of avian phenotypic evolution, and that skull evolution in birds is not simply a reflection of feeding ecology. Impact summaryAlmost 200 years ago, Darwin found that the beaks of Galapagos finches were different shapes in birds with different diets. Nowadays, it is well established that phylogeny, allometry, and ecology can also be key factors in shaping skulls. Yet, the influence of specific aspects of ecology, as well as life history, on morphological evolution remain poorly constrained. Here, we examined whether three novel factors also influence the shape of bird skulls and rates of evolution: habitat density, migration, or developmental mode. To do so, we combine high resolution 3D quantification of skull shape with dense taxonomic sampling across living birds. Our analyses revealed that skull shape varies in birds based on the density of vegetation in their habitats and on the extent to which they migrate. However, how independent birds are when they are born does not appear to influence overall skull shape. Despite these differences in how much they influence the shape of the skull, habitat density, migration and life history all influence the rate at which bird skulls evolve. Birds evolved fastest if they live in densely vegetated habitats, migrate long distances, or are precocial. These results add to the growing body of evidence that skull evolution in birds is impacted by a diverse range of factors, and suggests that habitat density, migration and life history should be considered in future analyses on drivers of phenotypic evolution.