The Joy of Sets: For Ants and Trees, Multiple Partners Are a Boon
ScienceDaily (Sep. 26, 2010) — In the complex world of ant-plant partnerships, serial monogamy can help trees maximize their evolutionary fitness, a new University of Florida study shows.
Coral reef near Borneo. When you snorkel on a coral reef, you're hovering over an animal -- the coral -- that relies heavily on the algae it cooperates with for photosynthesis. (Credit: iStockphoto/Olga Khoroshunova)
Trees that sequentially partner with multi-species sets of ants produce more offspring than trees that maintain a lifelong association with any single ant -- even when those sets include ant species that appear to harm the tree, said Todd Palmer, a UF biology professor.
The study has broad implications because many of the world's ecosystems rely on cooperative partnerships between species, Palmer said.
"When you snorkel on a coral reef, you're hovering over an animal -- the coral -- that relies heavily on the algae it cooperates with for photosynthesis, just as when you eat an apple, you're reaping the benefits of a tree that was pollinated by an insect," he said.
According to Palmer, many prior studies of cooperation in nature, or mutualism, have focused on the "cheater problem": How can cooperation persist when both sides have an incentive to reap benefits without contributing to the common good? Ecological studies tend to be short-term, with species labeled as "cooperators" or "freeloaders," depending on cost-benefit ratios calculated over just a few years.
Palmer and his team took a different approach, looking at a common African tree and its relationships with four specialized ant partners over the tree's lifetime.
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Todd M. Palmer a,b,1, Daniel F. Doak b,c, Maureen L. Stanton b,d, Judith L. Bronstein e, E. Toby Kiers f, Truman P. Young b,d,g, Jacob R. Goheen b,c,h, and Robert M. Pringle b,i,j
+Author Affiliations
aDepartment of Biology, University of Florida, Gainesville, FL 32611;
bMpala Research Centre, Nanyuki, Kenya 10400;
cDepartment of Zoology, University of Wyoming, Laramie, WY 82072;
Departments of dEvolution and Ecology and
gPlant Sciences, University of California, Davis, CA 95616;
eDepartment of Ecology and Evolutionary Biology, University of Arizona, Tuscon, AZ 85721;
fInstitute of Ecological Science, Faculty of Earth and Life Sciences, Vrije Universiteit, 1081 HV, Amsterdam, The Netherlands;
hDepartment of Zoology, University of British Columbia, Vancouver, BC, Canada V6T1Z4;
iDepartment of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544; and
jSociety of Fellows, Harvard University, Cambridge, MA 02138
Edited* by Paul R. Ehrlich, Stanford University, Stanford, CA, and approved August 17, 2010 (received for review May 17, 2010)
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.
Acacia drepanolobium, cooperation, plant defense, life history theory, ant-plant
Footnotes
1To whom correspondence should be addressed. E-mail: tmp@ufl.edu.
Author contributions: T.M.P. and D.F.D. designed research; T.M.P., D.F.D., M.L.S., T.P.Y., and J.R.G. performed research; T.M.P. and D.F.D. analyzed data; and T.M.P., D.F.D., M.L.S., J.L.B., E.T.K., J.R.G., and R.M.P. wrote the paper.
The authors declare no conflict of interest.
↵*This Direct Submission article had a prearranged editor.
This article contains supporting information online at
Freely available online through the PNAS open access option.
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