Journal of Animal Ecology 2008, 77 , 616–623 doi: 10.1111/j.1365-2656.2008.01359.x © 2008 The Authors. Journal compilation © 2008 British Ecological Society Blackwell Publishing Ltd Trade-off between reciprocal mutualists: local resource availability-oriented interaction in fig/fig wasp mutualism Rui Wu Wang 1* , Lei Shi 2 , Shi Meng Ai 1,3 and Qi Zheng 1,4 1 Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, 650223, China; 2 Statistics and Mathematics College, Yunnan University of Finance and Economics, Kunming, Yunnan 650221, China; 3 Department of Mathematics, Yunnan Agricultural University, Yunnan 650201, China; and 4 Graduate School of Kunming Medical College, Kunming, Yunnan 650031, China Summary 1. The mechanisms that prevent competition (conflict) between the recipient and co-operativeactor in co-operative systems remain one of the greatest problems for evolutionary biology. Previoushypotheses suggest that self-restraint, dispersal or spatial constraints can prevent direct competitionfor local resources or any other common resources, thereby maintaining stable co-operation inter-actions. In this study, we use the obligate fig–fig-wasp mutualism to examine whether the abovemechanisms can maintain stable co-operation sufficiently between figs and fig wasps. 2. Our data on obligate co-operation between figs ( Ficus racemosa Linn.) and fig wasps ( Ceratoslenfusciceps Mayr) show that the number of viable seeds of figs is positively correlated with the numberof pollinator offspring when the number of vacant female flowers is high while the foundress numberis low (two foundresses). Meanwhile, they are negatively correlated when the number of vacantfemale flowers is low and the number of foundresses is increased manually (eight foundresses). Thecorrelation coefficient between viable seeds and wasp offspring (galls) depends on vacant femaleflower availability. 3. Our data suggest that the interaction between figs and fig wasps is conditional, and that theyco-operate when local resource availability is plentiful but are in conflict when local resourceavailability is limited. The self-restraint, dispersal and spatial heterogeneity previously hypothesizedin maintaining stable co-operation cannot sufficiently prevent the symbionts from utilizing morelocal resources at the expense of the recipients. The conflict, which can disrupt the co-operationinteraction, exists after the local resource is saturated with symbionts. The repression of symbiontincrease, therefore repressing the utilization of local resources in the conflict period, is crucial in themaintenance and evolution of co-operation. Key-words: conflict, co-operation, fig, mutualism, repression, trade-off Introduction In interspecific mutualistic systems, symbionts (co-operativeindividuals) provide services or goods for the recipients. Thesegoods and services are costly in some systems, while therecipients reward the symbionts with direct or indirect benefits.Therefore in co-operation systems, both species will bilater-ally increase their fitness. However, the conflict for localresources (or any other common resources) can be increasedthrough augmentation of the symbiont if the available resourceis limited, potentially disrupting the co-operation system(Williams 1966; Taylor 1992; Wilson, Pollock & Dugatkin 1992;West, Pen & Griffin 2002a). What mechanisms preventco-operative partners from over-utilizing local resources atthe expense of the recipient, and therefore maintain a stableco-operation interaction, remains a heated argument in thescientific community (Clutton-Brock 2002; West et al . 2002b).Classical co-operation theories emphasize that the geneticrelatedness resulting from viscosity of the individuals involvedcan increase the inclusive or direct fitness of involved partners(Hamilton 1972; Mitteldorf & Wilson 2000). However, thecost of co-operative behaviour can cancel out the benefitswith increasing numbers of actors (co-operative individuals),because the benefits received from the recipient may decreasedisproportionately with the augmentation of actors, while thecost of co-operative behaviour is a relatively constant value *Correspondence author. E-mail: [email protected] between reciprocal mutualists 617 © 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Animal Ecology , 77 , 616–623 (Williams 1966; Taylor 1992; Wilson et al . 1992). Geneticrelatedness (between the original donor and recipient) inreciprocity selection, or kin relatedness in kin selection(Hamilton 1964; Frank 1994), will be unimportant in theevolution of co-operation (Williams 1966), and the co-operationinteraction should proceed to extinction with the augmenta-tion of actors if there is no mechanism that can sufficientlyprevent the competition resulting from an augmentation ofactors (Hamilton 1972; Taylor 1992; Wilson et al . 1992).Spatial models of the evolution of altruism hypothesizedthat self-restraint (Hamilton 1972; Axelrod & Hamilton 1981),dispersal of the altruists (Greenwood-Lee & Taylor 2001), orspatial constraints (Nowak, Bonhoeffer & May 1994; Doebeli& Knowlton 1998) might play a role in preventing extra actorsor cheating individuals from over-exploiting the commons atthe expense of the recipient, and therefore might maintainstable co-operation. However, the above mechanisms cannotexplain sufficiently why the cheating or less co-operativeindividuals do not invade the co-operation system, especiallyin cases where individuals cannot disperse to another colonyor cannot live alone (for a critique of self-restraint mechanismsthrough recognition see Doebeli & Knowlton 1998; Clutton-Brock 2002; for a critique of spatial constraints see Hauert &Doebeli 2004).Essentially, the evolution of co-operation is determined bywhether a positive correlation coefficient of inclusive or directfitness between the recipient and co-operative actors can becreated (Price 1970; Hamilton 1972; Queller 1992a). If thespatial structure created by genetic restraint can maintainthe stable co-operation sufficiently, a positive correlationcoefficient should be observed, because the cheating indi-vidual of co-operative actors or extra co-operative actors cannotutilize the commons at the expense of the recipient (Price 1971;Hamilton 1972; Doebeli & Knowlton 1998), and the directconflict (the negative correlation