Economic contract theory tests models of mutualism

Abstract

Although mutualisms are common in all ecological communities and have played key roles in the diversification of life, our current understanding of the evolution of cooperation applies mostly to social behavior within a species. A central question is whether mutualisms persist because hosts have evolved costly punishment of cheaters. Here, we use the economic theory of employment contracts to formulate and distinguish between two mechanisms that have been proposed to prevent cheating in host-symbiont mutualisms, partner fidelity feedback (PFF) and host sanctions (HS). Under PFF, positive feedback between host fitness and symbiont fitness is sufficient to prevent cheating; in contrast, HS posits the necessity of costly punishment to maintain mutualism. A coevolutionary model of mutualism finds that HS are unlikely to evolve de novo, and published data on legume-rhizobia and yucca-moth mutualisms are consistent with PFF and not with HS. Thus, in systems considered to be textbook cases of HS, we find poor support for the theory that hosts have evolved to punish cheating symbionts; instead, we show that even horizontally transmitted mutualisms can be stabilized via PFF. PFF theory may place previously underappreciated constraints on the evolution of mutualism and explain why punishment is far from ubiquitous in nature.evolution of cooperation | punishment | symbiosis | partner fidelity feedback | host sanctions

Standing genetic variation in host preference for mutualist microbial symbionts

“…The mere existence of a harmful yet compatible exploiter strain, combined with the fact that bacteria can reproduce (and hence respond to selection) much more quickly than their host, suggests that there will probably be strong selective pressure for the host to reduce post-infection feedback benefits by aborting or inactivating nodules [64]. Post-infection stabilizing mechanisms, such as host sanction mechanisms (as defined by Denison [8]) and partner fidelity feedbacks (as defined by Weyl et al [22]) will probably play a key role in reducing infection by exploitative or inefficient rhizobia partners that possess compatible traits to invade and form root nodules. Since coevolutionary responses on post-infection traits are currently intensely debated [20,22,24,25,59], more data on genetic variation in symbiosisrelated traits (e.g.…”

“…Post-infection stabilizing mechanisms, such as host sanction mechanisms (as defined by Denison [8]) and partner fidelity feedbacks (as defined by Weyl et al [22]) will probably play a key role in reducing infection by exploitative or inefficient rhizobia partners that possess compatible traits to invade and form root nodules. Since coevolutionary responses on post-infection traits are currently intensely debated [20,22,24,25,59], more data on genetic variation in symbiosisrelated traits (e.g. nodule size [65], energy storage in rhizobia [66]) and post-infection stabilizing traits, as well as the strength of natural selection acting on them, would clarify their role in stabilizing or destabilizing mutualisms [19].…”

“…While there is debate on the origin and the maintenance of these mechanisms [20 -23], their viability as an evolutionary stable state [15][16][17]24], and how we can distinguish between them in natural systems [20,22,25], all three mechanisms share a common outcome: the host increases the relative fitness of more beneficial partners and/or decreases the relative fitness of less beneficial or exploitative partners. Given the recurrent observation of exploitative partners [4,8,26], selection on stabilizing mechanisms is predicted to be strong because exploitative symbionts are assumed to have negative effects on host fitness [13,16,[27][28][29][30] (but see [31]).…”

The Direct and Ecological Costs of an Ant-Plant Symbiosis

“…Mechanisms that maintain cooperation and prevent cheating have been heavily emphasized in the mutualism literature (e.g., Pierce 1987;Sachs et al 2004;Foster and Kokko 2006;Douglas 2008;Weyl et al 2010). Although individuals may reap net benefits through cooperation, they may do even better by cheating and taking the benefits of cooperation without paying the costs of reciprocation.…”

Bet hedging based cooperation can limit kin selection and form a basis for mutualism

“…in ecology, and intraspecific mutualism, which is important in e.g. the human economy (Trivers, 1971, Herre, 1999Clutton-Brock, 2002;Bergstrom and Lachmann, 2003;Ferriere et al, 2002;Sachs et al, 2004;Foster and Wenseleers, 2006;Bronstein, 2009;Weyl et al, 2010). A general characteristic of mutualism is that the partners are mutually dependent because they are specialized.…”