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Economic Contract Theory Tests Models of Mutualism

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Economic Contract Theory Tests Models of Mutualism Economic contract theory tests models of mutualism E. Glen Weyla, Megan E. Fredericksona,b, Douglas W. Yuc,d,1, and Naomi E. Piercea,e aSociety of Fellows, Harvard University, Cambridge, MA 02138; bDepartment of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3G5; cState Key Laboratory of Genetic Resources and Evolution, Ecology, Conservation, and Environment Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China; dSchool of Biological Sciences, University of East Anglia, Norwich, Norfolk NR47TJ, United Kingdom; and eDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138 Edited by Jose A. Scheinkman, Princeton University, Princeton, NJ, and approved July 27, 2010 (received for review April 18, 2010) Although mutualisms are common in all ecological communities and Under PFF, natural selection favors mutualists rather than have played key roles in the diversification of life, our current cheaters because an individual that fails to cooperate reduces its understanding of the evolution of cooperation applies mostly to own fitness (or loses an opportunity to increase its own fitness); social behavior within a species. A central question is whether no further punishment is necessary. By contrast, HS posits that mutualisms persist because hosts have evolved costly punishment PFF is not sufficient to negate the incentive to cheat, and, thus, of cheaters. Here, we use the economic theory of employment mutualism will persist only if hosts evolve to detect and punish contracts to formulate and distinguish between two mechanisms cheaters (1, 13) (Box 1). that have been proposed to prevent cheating in host–symbiont fi mutualisms, partner delity feedback (PFF) and host sanctions (HS). Box 1. Partner fidelity feedback vs. host sanctions. One way Under PFF, positive feedback between host fitness and symbiont fi fi to contrast PFF and HS is by analogy to the criminal justice tness is suf cient to prevent cheating; in contrast, HS posits the system. PFF is akin to the theory that incarceration should necessity of costly punishment to maintain mutualism. A coevolu- bring about incapacitation and/or rehabilitation, thus pre- tionary model of mutualism finds that HS are unlikely to evolve de , – – venting any prospective (short-term future) harms the criminal novo and published data on legume rhizobia and yucca moth may also cause society and only incidentally punishing mis- mutualisms are consistent with PFF and not with HS. Thus, in systems fi fi behavior. Each case is justi ed individually. By contrast, HS considered to be textbook cases of HS, we nd poor support for the are analogous to theories that emphasize the value of pun- theory that hosts have evolved to punish cheating symbionts; in- ishment as a public deterrent to criminal activity. According to stead, we show that even horizontally transmitted mutualisms can Becker’s economic theory of crime and punishment (45), the be stabilized via PFF. PFF theory may place previously underappreci- least expensive means of deterrence are punishments that are ated constraints on the evolution of mutualism and explain why infrequently administered, widely publicized, and severe, such punishment is far from ubiquitous in nature. as corporal punishment or torture. The prospect of suffering similar punishment is transmitted culturally to the wider popu- evolution of cooperation | punishment | symbiosis | partner fidelity lation and deters misbehavior by others. In a biological context, feedback | host sanctions HS is the theory that host punishment selects for “evolutionary improvement” of the symbiont population. See also analysis in n contrast to the decades-long development of social co- SI Text 1. Ioperation theory (reviews in refs. 1–5), mutualism theory has An example is recent reaction to illegal downloading of only recently begun to be formalized (6–15), and major questions copyrighted media, such as films and music. As in HS, copyright remain open. One of these questions concerns whether mutualists owners have tried to deter such violations by prosecuting indi- evolve to punish cheaters (1, 7–10, 16, 17). The host sanctions viduals who can be shown in court to have shared files illegally (HS) hypothesis suggests that the costly, selective punishment of and widely publicizing these cases. However, recent years have cheating symbionts can evolve de novo in host species (i.e., in shown that socially acceptable levels of punishment (typically, response to symbiont behaviors). As an alternative, partner small fines) are too low to be an effective deterrent. Alterna- fidelity feedback (PFF) suggests that punishment is only apparent tively, simple nonretributive policies may help reduce violations and is instead an epiphenomenon of the fact that concordant life at low social cost. Illegal downloads consume substantial band- histories cause two species to be bound together for an “extended width, so some have argued that establishing an automatic sys- ” fi tem of graduated charges for bandwidth consumption would series of exchanges (1), thereby linking their tnesses. There has fi fi been, to date, no sharp way to distinguish these very different signi cantly reduce such violations. Such policies are ef cient even if illegal downloading is not taking place, as they help ensure explanations for the maintenance of mutualism, and this has ob- efficient use of scarce bandwidth. Thus, as with PFF, natural scured our understanding of the factors that promote or constrain incentives without any retributive motive may be sufficient to the evolution of cooperation between species. deter antisocial behavior. PFF occurs when the benefits provided by a donor individual to a recipient individual automatically feed back to the donor (1, 9, 18, 19). The harder the donor works to assist the recipient, the Although both concepts (PFF and HS) have been discussed in ’ better off the recipient is and the more benefits it, in turn, provides some form in the literature at least since Trivers seminal paper back to the donor. For example, a symbiont that provides a nu- trient to a host improves the host’s vigor, which can indirectly, but automatically, benefit the symbiont by decreasing the risk of host Author contributions: E.G.W., M.E.F., D.W.Y., and N.E.P. designed research; E.G.W., M.E.F., D.W.Y., and N.E.P. performed research; E.G.W. contributed new reagents/analytic tools; mortality. Analogously, if a donor harms the recipient, such as by E.G.W., M.E.F., D.W.Y., and N.E.P. analyzed data; and E.G.W., M.E.F., D.W.Y., and N.E.P. failing to provide a valuable nutrient, the harm to the recipient wrote the paper. also feeds back automatically to the donor. Note that PFF is The authors declare no conflict of interest. possible only when partners associate long enough that the short- This article is a PNAS Direct Submission. term costs of helping can be recuperated by the helper. The most Freely available online through the PNAS open access option. straightforward example of PFF thus involves vertical trans- 1To whom correspondence should be addressed. E-mail: [email protected]. mission of symbionts, because partners are associated for multiple This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. generations (20, 21). 1073/pnas.1005294107/-/DCSupplemental. 15712–15716 | PNAS | September 7, 2010 | vol. 107 | no. 36 www.pnas.org/cgi/doi/10.1073/pnas.1005294107 Downloaded by guest on October 2, 2021 À Á À Á Â Ã in 1971 (22), it was Bull and Rice (23) who coined the term A ; π S P ; π − π [1.1] “partner fidelity” in 1991, which they distinguished from partner U a ¼ u a þ fU s choice. Today, partner choice is often used interchangeably with By the definition of actions a and a being short-term profitable HS, but Bull and Rice originally defined partner choice to mean 1 2 actions, we assume that uSða Þ; uSða Þ > uSðaÃÞ; that is, cheating interactions in which individuals “differentially reward coopera- 1 2 improves A’s short-term fitness. Importantly, because nature is tive vs. un-cooperative partners in advance of any possible exploi- tation” (italics added) (ref. 23, p 63), whereas both PFF and HS stochastic, any single action a could result in any one of N signals are differential rewards or punishments implemented after ex- (outcomes) s, albeit with different probabilities for different ploitation is possible. Here, we argue that a failure to clearly actions. For instance, a symbiont might not protect its host from define the differences between PFF and HS has led to their parasites, which increases the probability of but does not doom the conflation, with the result that experiments demonstrating what host to parasitism, or a symbiont might engage in protective 1.1 appears to be the punishment of cheating in a wide range of behaviors but still fail to prevent parasitism. Eq. is therefore fi mutualisms, including those between yucca plants and yucca expressed generally as an expected tness across a distribution of moths (24), legumes and nitrogen-fixing bacteria (25, 26), ants possible signals, given a particular action: and plants (27), plants and mycorrhizal fungi (28), and figs and fi N À Á g wasps (29), have been generally accepted as evidence for HS A ; π · ≡ S ∑ P ; π − π : [1.2] – U ða ½ Þ u ðaÞþ fU ðsi ½siÞ ½si pðsijaÞ (1, 9, 13, 26 29), whereas PFF is the more likely explanation. i Model This model allows us to differentiate PFF and HS once we have To formally differentiate PFF from HS, we use a general principal– made an important, if common, assumption: Subject to the con- agent (host–symbiont) model that includes the possibility of costly straints imposed by the theories, both A and P maximize their punishment.
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