Abstract
BackgroundResolution of the link between micro- and macroevolution calls for comparing both processes on the same deterministic landscape, such as genomic, metabolic or fitness networks. We apply this perspective to the evolution of carotenoid pigmentation that produces spectacular diversity in avian colors and show that basic structural properties of the underlying carotenoid metabolic network are reflected in global patterns of elaboration and diversification in color displays. Birds color themselves by consuming and metabolizing several dietary carotenoids from the environment. Such fundamental dependency on the most upstream external compounds should intrinsically constrain sustained evolutionary elongation of multi-step metabolic pathways needed for color elaboration unless the metabolic network gains robustness – the ability to synthesize the same carotenoid from an additional dietary starting point.ResultsWe found that gains and losses of metabolic robustness were associated with evolutionary cycles of elaboration and stasis in expressed carotenoids in birds. Lack of metabolic robustness constrained lineage’s metabolic explorations to the immediate biochemical vicinity of their ecologically distinct dietary carotenoids, whereas gains of robustness repeatedly resulted in sustained elongation of metabolic pathways on evolutionary time scales and corresponding color elaboration.ConclusionsThe structural link between length and robustness in metabolic pathways may explain periodic convergence of phylogenetically distant and ecologically distinct species in expressed carotenoid pigmentation; account for stasis in carotenoid colors in some ecological lineages; and show how the connectivity of the underlying metabolic network provides a mechanistic link between microevolutionary elaboration and macroevolutionary diversification.ReviewersThis article was reviewed by Junhyong Kim, Eugene Koonin, and Fyodor Kondrashov. For complete reports, see the Reviewers’ reports section.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-015-0073-6) contains supplementary material, which is available to authorized users.
Highlights
Resolution of the link between micro- and macroevolution calls for comparing both processes on the same deterministic landscape, such as genomic, metabolic or fitness networks
We found that diversification in expressed carotenoids was the greatest in recently diverged species
Rapid metabolic diversification had led to highly distinct plumage carotenoids between recently diverged and ecologically similar taxa, such as bullfinches Pyrrhula pyrrhula and P. aurantiaca that have diverged less than 5 million years ago or cotingas Rupicola rupicola and R. peruviana that have diverged less than 4 million years ago, with neither sister groups sharing the expressed carotenoids (Additional file 3: Appendix S2 and references therein)
Summary
Resolution of the link between micro- and macroevolution calls for comparing both processes on the same deterministic landscape, such as genomic, metabolic or fitness networks. We apply this perspective to the evolution of carotenoid pigmentation that produces spectacular diversity in avian colors and show that basic structural properties of the underlying carotenoid metabolic network are reflected in global patterns of elaboration and diversification in color displays. We hypothesized that the evolutionary diversification in carotenoid-based coloration in these taxa should be a reflection of the structure and patterns of enzymatic connectivity of the underlying “global network” of carotenoid biosynthesis
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