Tradeoff between robustness and elaboration in carotenoid networks produces cycles of avian color diversification.
BACKGROUND
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. 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.


RESULTS
We 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.


CONCLUSIONS
The 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.
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA. abadyaev@email.arizona.edu.
Alexander V
AV
Badyaev
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA. esmorr@email.arizona.edu.
Erin S
ES
Morrison
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA. belloniua@gmail.com.
Virginia
V
Belloni
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA. sanderm@email.arizona.edu.
Michael J
MJ
Sanderson
D000818:Animals; D005075:Biological Evolution; D001717:Birds / Q000235:genetics* / Q000378:metabolism; D002338:Carotenoids / Q000235:genetics* / Q000378:metabolism; D003116:Color; D010802:Phylogeny; D010858:Pigmentation; D013045:Species Specificity
D002338:Carotenoids