Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism.
Identifieur interne : 002546 ( Main/Corpus ); précédent : 002545; suivant : 002547Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism.
Auteurs : Todd M. Palmer ; Daniel F. Doak ; Maureen L. Stanton ; Judith L. Bronstein ; E Toby Kiers ; Truman P. Young ; Jacob R. Goheen ; Robert M. PringleSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2010.
English descriptors
- KwdEn :
- MESH :
- physiology : Acacia, Ants, Symbiosis.
- Animals, Biological Evolution, Ecosystem, Genetic Fitness, Host-Parasite Interactions, Survival Rate.
Abstract
Understanding cooperation is a central challenge in biology, because natural selection should favor "free-loaders" that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a "sterilization parasite" that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these "parasites" enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.
DOI: 10.1073/pnas.1006872107
PubMed: 20855614
PubMed Central: PMC2951420
Links to Exploration step
pubmed:20855614Le document en format XML
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Bronstein</name></author><author><name sortKey="Kiers, E Toby" sort="Kiers, E Toby" uniqKey="Kiers E" first="E Toby" last="Kiers">E Toby Kiers</name></author><author><name sortKey="Young, Truman P" sort="Young, Truman P" uniqKey="Young T" first="Truman P" last="Young">Truman P. Young</name></author><author><name sortKey="Goheen, Jacob R" sort="Goheen, Jacob R" uniqKey="Goheen J" first="Jacob R" last="Goheen">Jacob R. Goheen</name></author><author><name sortKey="Pringle, Robert M" sort="Pringle, Robert M" uniqKey="Pringle R" first="Robert M" last="Pringle">Robert M. 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Palmer</name><affiliation><nlm:affiliation>Department of Biology, University of Florida, Gainesville, FL 32611, USA. tmp@ufl.edu</nlm:affiliation></affiliation></author><author><name sortKey="Doak, Daniel F" sort="Doak, Daniel F" uniqKey="Doak D" first="Daniel F" last="Doak">Daniel F. Doak</name></author><author><name sortKey="Stanton, Maureen L" sort="Stanton, Maureen L" uniqKey="Stanton M" first="Maureen L" last="Stanton">Maureen L. Stanton</name></author><author><name sortKey="Bronstein, Judith L" sort="Bronstein, Judith L" uniqKey="Bronstein J" first="Judith L" last="Bronstein">Judith L. Bronstein</name></author><author><name sortKey="Kiers, E Toby" sort="Kiers, E Toby" uniqKey="Kiers E" first="E Toby" last="Kiers">E Toby Kiers</name></author><author><name sortKey="Young, Truman P" sort="Young, Truman P" uniqKey="Young T" first="Truman P" last="Young">Truman P. Young</name></author><author><name sortKey="Goheen, Jacob R" sort="Goheen, Jacob R" uniqKey="Goheen J" first="Jacob R" last="Goheen">Jacob R. Goheen</name></author><author><name sortKey="Pringle, Robert M" sort="Pringle, Robert M" uniqKey="Pringle R" first="Robert M" last="Pringle">Robert M. Pringle</name></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="eISSN">1091-6490</idno><imprint><date when="2010" type="published">2010</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Acacia (physiology)</term><term>Animals (MeSH)</term><term>Ants (physiology)</term><term>Biological Evolution (MeSH)</term><term>Ecosystem (MeSH)</term><term>Genetic Fitness (MeSH)</term><term>Host-Parasite Interactions (MeSH)</term><term>Survival Rate (MeSH)</term><term>Symbiosis (physiology)</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Acacia</term><term>Ants</term><term>Symbiosis</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Biological Evolution</term><term>Ecosystem</term><term>Genetic Fitness</term><term>Host-Parasite Interactions</term><term>Survival Rate</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Understanding cooperation is a central challenge in biology, because natural selection should favor "free-loaders" that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a "sterilization parasite" that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these "parasites" enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">20855614</PMID><DateCompleted><Year>2010</Year><Month>11</Month><Day>16</Day></DateCompleted><DateRevised><Year>2019</Year><Month>01</Month><Day>08</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN><JournalIssue CitedMedium="Internet"><Volume>107</Volume><Issue>40</Issue><PubDate><Year>2010</Year><Month>Oct</Month><Day>05</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation></Journal><ArticleTitle>Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism.</ArticleTitle><Pagination><MedlinePgn>17234-9</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1006872107</ELocationID><Abstract><AbstractText>Understanding cooperation is a central challenge in biology, because natural selection should favor "free-loaders" that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a "sterilization parasite" that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these "parasites" enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Palmer</LastName><ForeName>Todd M</ForeName><Initials>TM</Initials><AffiliationInfo><Affiliation>Department of Biology, University of Florida, Gainesville, FL 32611, USA. tmp@ufl.edu</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Doak</LastName><ForeName>Daniel F</ForeName><Initials>DF</Initials></Author><Author ValidYN="Y"><LastName>Stanton</LastName><ForeName>Maureen L</ForeName><Initials>ML</Initials></Author><Author ValidYN="Y"><LastName>Bronstein</LastName><ForeName>Judith L</ForeName><Initials>JL</Initials></Author><Author ValidYN="Y"><LastName>Kiers</LastName><ForeName>E Toby</ForeName><Initials>ET</Initials></Author><Author ValidYN="Y"><LastName>Young</LastName><ForeName>Truman P</ForeName><Initials>TP</Initials></Author><Author ValidYN="Y"><LastName>Goheen</LastName><ForeName>Jacob R</ForeName><Initials>JR</Initials></Author><Author ValidYN="Y"><LastName>Pringle</LastName><ForeName>Robert M</ForeName><Initials>RM</Initials></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2010</Year><Month>09</Month><Day>20</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Proc Natl Acad Sci U S A</MedlineTA><NlmUniqueID>7505876</NlmUniqueID><ISSNLinking>0027-8424</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000045" MajorTopicYN="N">Acacia</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001000" MajorTopicYN="N">Ants</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005075" MajorTopicYN="N">Biological Evolution</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017753" MajorTopicYN="N">Ecosystem</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D056084" MajorTopicYN="Y">Genetic Fitness</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006790" MajorTopicYN="N">Host-Parasite Interactions</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015996" MajorTopicYN="N">Survival Rate</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2010</Year><Month>9</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2010</Year><Month>9</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2010</Year><Month>11</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">20855614</ArticleId><ArticleId IdType="pii">1006872107</ArticleId><ArticleId IdType="doi">10.1073/pnas.1006872107</ArticleId><ArticleId 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