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Study: It's not cheating unless a species gets hurt

Ecological review finds little proof of cheating among cooperating species

Rice University

HOUSTON -- (Sept. 21, 2015) -- A review of dozens of key ecological studies has found very little evidence to support one of the field's commonly held beliefs: Cheating is widespread among 'mutualists,' species that cooperate with one another for mutual benefit.

"We find that although there are numerous observations of low-quality partners, there is currently very little support ... that any of these meet our criteria to be considered cheaters," according to the study published online this week in Ecology Letters.

Rice University evolutionary ecologist Emily Jones, the study's co-lead author, said a 14-member research team working under the auspices of the National Center for Ecological Analysis and Synthesis at the University of California, Santa Barbara, found that cheating has never had a common definition in ecology. Thus, although hundreds of studies have reportedly examined mutualistic "cheating," most were actually examining only limited aspects of it.

"By definition, a behavior is only cheating if it provides one partner with an advantage and also imposes a disadvantage on the other partner," said Jones, a Huxley Fellow in BioSciences at Rice. "We found that most previous definitions were focused on just one side of the interaction. People have tended to be narrowly focused on whether one partner was either giving less of a resource or taking more from the other partner, but neither of those qualifies as cheating unless the other partner is harmed."

Interspecies cooperation is a fixture of the natural world. Among the hundreds of documented examples are nitrogen-fixing bacteria that help plants obtain nutrients, honeybees that pollinate as they gather nectar and gut bacteria that help humans digest food. But mutualisms also present evolutionary biologists with a conundrum: Why should species cooperate at all, given that Darwinian selection demands that each organism act in its own self-interest?

"One of my advisers from graduate school, Judie Bronstein, liked to describe mutualism as 'mutual exploitation,'" said Jones. "Each species is actually exploiting the other, and each one benefits more from the mutual arrangement than they are harmed by it."

Even so, the self-interest of each partner sets the stage for cheating because each partner is driven by selective pressure to extract the most it can from the relationship.

Michigan State University plant biologist Maren Friesen, the study's other co-lead author, said mutualistic interactions are theoretically interesting to evolutionary biologists because of the self-interest of the partners.

"The selective pressure to cheat challenges the 'persistence of cooperation,' and there is a healthy theoretical debate about the conditions that underlie and promote stable mutualistic relationships," she said.

The idea that natural selection pushes species to cheat has motivated hundreds of ecological studies. For example, the authors found that since 2010, more than 100 studies per year have examined concepts related to mutualistic cheating. For its study, the team reviewed dozens of studies and focused closely on those related to mutualisms in which cheating has been suspected to be important.

Friesen and Jones are careful to point out that the team's findings do not preclude the possibility that cheating is widespread among mutualists.

"It is possible that cheating is widespread," Friesen said. "But it is clear that previous studies have not proved that widespread cheating is taking place."

To help with future studies, Friesen, Jones and their co-authors have provided a rigorous scientific definition of cheating that ecologists can use to unequivocally determine whether one species is cheating its mutualist partner.

"In order to qualify as cheating, a behavior must increase the fitness of the cheating partner above the average fitness of individuals in its own population, and it must decrease the fitness of the partner below the average fitness of individuals in the partner's population," Friesen said.

Jones said the definition could help scientists overcome another problem that has likely plagued the discipline.

"The word 'cheating' implies that something unfair is taking place, but it is very difficult to make judgments about fairness when species are trading and contributing different resources," Jones said. "We considered suggesting that people avoid using the term 'cheating' altogether, but we decided that was impractical. The best course of action was to clearly define it instead."

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Study co-authors include Michelle Afkhami and Megan Frederickson, both of the University of Toronto; Erol Akçay of the University of Pennsylvania; Judith Bronstein of the University of Arizona; Redouan Bshary of the University of Neuchâtel in Switzerland; Katy Heath of the University of Illinois; Jason D. Hoeksema of the University of Mississippi; Joshua Ness of Skidmore College; Sabrina Pankey of the University of New Hampshire; Joel Sachs of the University of California, Riverside; Stephanie Porter, formerly of the University of California, Riverside, and currently of Washington State University; and Klara Scharnagl of Michigan State University.

This research was supported by the National Science Foundation; the Natural Sciences and Engineering Research Council of Canada; the University of California, Santa Barbara; and the state of California.

High-resolution IMAGES are available for download at:

http://news.rice.edu/wp-content/uploads/2015/09/0921-CHEATERS-Fish-lg.jpg
CAPTION: Two Labroides bicolor cleaner fish with their 'client' partner. L. bicolor helps its client by feeding on parasites, but it also takes an occasional bite of client flesh. A review of current literature found the behavior could not be called cheating because it was unclear whether client fish are harmed by the biting or whether the occasional bite of client flesh provides a measureable 'fitness increase' for L. biocolor.
CREDIT: R. Bshary/University of Neuchâtel

http://news.rice.edu/wp-content/uploads/2015/09/0921-CHEATERS-nods-lg.jpg
CAPTION: The Chamaecrista plant obtains nitrogen from rhizobial bacteria and each cooperates to form root nodules where the bacteria live. While some rhizobial strains withhold nitrogen, plants have the ability to reward more generous partners. A review of current literature found no unequivocal examples of rhizobial cheaters that increase their fitness by fixing less nitrogen for their partners.
CREDIT: K. Heath/University of Illinois at Urbana-Champaign

http://news.rice.edu/wp-content/uploads/2015/09/0921-CHEATERS-Jones-lg.jpg
CAPTION: Emily Jones
CREDIT: Rice University

http://news.rice.edu/wp-content/uploads/2015/09/0921-CHEATERS-Friesen-lg.jpg
CAPTION: Maren Friesen
CREDIT: Michigan State University

A copy of the Ecology Letters paper is available at: http://onlinelibrary.wiley.com/doi/10.1111/ele.12507/abstract

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