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

Persistent Link:
http://hdl.handle.net/10150/610267
Title:
Tradeoff between robustness and elaboration in carotenoid networks produces cycles of avian color diversification
Author:
Badyaev, Alexander V.; Morrison, Erin S.; Belloni, Virginia; Sanderson, Michael J.
Affiliation:
Department of Ecology and Evolutionary Biology, University of Arizona
Issue Date:
2015
Publisher:
Springer
Citation:
Badyaev et al. Biology Direct (2015) 10:45 DOI 10.1186/s13062-015-0073-6
Journal:
Biology Direct
Rights:
© 2015 Badyaev et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/)
Collection Information:
This item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.
Abstract:
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. REVIEWERS: This article was reviewed by Junhyong Kim, Eugene Koonin, and Fyodor Kondrashov. For complete reports, see the Reviewers' reports section.
EISSN:
1745-6150
DOI:
10.1186/s13062-015-0073-6
Keywords:
Metabolic networks; Robustness; Metabolic distance; Diversification
Version:
Final published version
Additional Links:
http://www.biologydirect.com/content/10/1/45

Full metadata record

DC FieldValue Language
dc.contributor.authorBadyaev, Alexander V.en
dc.contributor.authorMorrison, Erin S.en
dc.contributor.authorBelloni, Virginiaen
dc.contributor.authorSanderson, Michael J.en
dc.date.accessioned2016-05-20T09:02:41Z-
dc.date.available2016-05-20T09:02:41Z-
dc.date.issued2015en
dc.identifier.citationBadyaev et al. Biology Direct (2015) 10:45 DOI 10.1186/s13062-015-0073-6en
dc.identifier.doi10.1186/s13062-015-0073-6en
dc.identifier.urihttp://hdl.handle.net/10150/610267-
dc.description.abstractBACKGROUND: 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. REVIEWERS: This article was reviewed by Junhyong Kim, Eugene Koonin, and Fyodor Kondrashov. For complete reports, see the Reviewers' reports section.en
dc.language.isoenen
dc.publisherSpringeren
dc.relation.urlhttp://www.biologydirect.com/content/10/1/45en
dc.rights© 2015 Badyaev et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/)en
dc.subjectMetabolic networksen
dc.subjectRobustnessen
dc.subjectMetabolic distanceen
dc.subjectDiversificationen
dc.titleTradeoff between robustness and elaboration in carotenoid networks produces cycles of avian color diversificationen
dc.typeArticleen
dc.identifier.eissn1745-6150en
dc.contributor.departmentDepartment of Ecology and Evolutionary Biology, University of Arizonaen
dc.identifier.journalBiology Directen
dc.description.collectioninformationThis item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
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