Taxonomic overview of all birds sampled from Back in black: melanin-rich skin colour associated with increased net diversification rates in birds

Evolutionary biologists have long been interested in understanding the factors that promote diversification in organisms, often focussing on distinct and/or conspicuous phenotypes with direct effects on natural or sexual selection such as body size and plumage coloration. However, multiple traits that potentially influence net diversification are not conspicuous and/or might be concealed. One such trait, the dark, melanin-rich skin concealed beneath the feathers, evolved more than 100 times during avian evolution, frequently in association with white feathers on the crown and UV-rich environments, suggesting that it is a UV-photoprotective adaptation. Furthermore, multiple species are polymorphic, having both light and dark skin potentially aiding occupation in different UV radiation-environments. As such these polymorphisms are predicted to occur in species with large latitudinal variation in their distribution. Furthermore, by alleviating evolutionary constraints on feather colour, the evolution of dark skin may promote net diversification. Here, using an expanded dataset on bird skin coloration of 3033 species we found that more than 19% of species had dark skin. In contrast to our prediction, dark skinned birds have smaller distribution ranges. Furthermore, both dark skin and polymorphism in skin coloration promote net diversification. These results suggest that even concealed traits can influence large scale evolutionary events such as diversification in birds.

进化生物学家长期以来一直致力于探究推动生物演化多样化（diversification）的核心驱动因素，过往研究多聚焦于对自然选择（natural selection）或性选择（sexual selection）具有直接影响的显著醒目表型（phenotype），例如体型与羽色。然而，诸多可能影响净物种分化（net diversification）的性状并不醒目，甚至可能被隐藏于体表之下。其中一类典型性状便是隐藏于羽毛下方的深色富含黑色素皮肤——该性状在鸟类演化历程中独立起源超过100次，且常与头顶白羽及高紫外线环境相伴出现，提示其为一种紫外线光保护适应性（UV-photoprotective adaptation）特征。此外，诸多鸟类物种存在皮肤颜色多态性（skin color polymorphism），兼具浅色与深色皮肤，这可能有助于它们在不同紫外线辐射环境中占据适宜生态位。据此推测，这类皮肤颜色多态性应出现于分布纬度跨度较大的物种中。另外，深色皮肤的演化可缓解羽色演化所受的进化约束（evolutionary constraints），进而可能推动净物种分化。本研究基于涵盖3033个物种的扩展版鸟类皮肤颜色数据集开展分析，结果显示超过19%的鸟类物种拥有深色皮肤。与此前预测相悖的是，拥有深色皮肤的鸟类其分布范围（distribution ranges）反而更小。此外，深色皮肤与皮肤颜色多态性均能推动净物种分化。本研究结果表明，即便是隐藏的性状，也可对鸟类物种分化这类宏观演化事件产生重要影响。