- Email: [email protected]
Animal Behaviour: Friendship Enhances Trust in Chimpanzees
Current Biology
Dispatches balancing selection on patterns of genetic variation will surely continue. REFERENCES 1. Darwin, C. (1859). The Origin of Species by Means of Natural Selection, or the Preservation of Favored Races in the Struggle for Life (London: John Murray). 2. Cutter, A.D., Jovelin, R., and Dey, A. (2013). Molecular hyperdiversity and evolution in very large populations. Mol. Ecol. 22, 2074–2095. 3. Chakraborty, M., and Fry, J.D. (2016). Evidence that environmental heterogeneity maintains a detoxifying enzyme polymorphism in Drosophila melanogaster. Curr. Biol. 26, 219–223. 4. Dobzhansky, T. (1951). Genetics and the Origin of Species (Columbia University Press). 5. Levene, H. (1953). Genetic equilibrium when more than one ecological niche is available. Am. Nat. 87, 331–333. 6. Dempster, E.R. (1955). Maintenance of genetic heterogeneity. Cold Spring Harbor Symp. Quant. Biol. 20, 25–32. 7. Hedrick, P.W. (2006). Genetic polymorphism in heterogeneous environments: the age of genomics. Annu. Rev. Ecol. Evol. Syst. 37, 67–93. 8. Gillespie, J.H., and Turelli, M. (1989). Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121, 129–138. 9. Allison, A.C. (1954). Protection afforded by sickle-cell trait against subtertian malarial infection. Br. Med. J. 1, 290–294. 10. Lewontin, R.C., and Hubby, J.L. (1966). A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54, 595–609. 11. Gillespie, J.H., and Langley, C.H. (1974). A general model to account for enzyme variation in natural populations. Genetics 76, 837–848. 12. Kimura, M. (1968). Evolutionary rate at the molecular level. Nature 217, 624–626. 13. Lande, R. (1976). The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet. Res. 26, 221–235. 14. Christiansen, F.B. (1975). Hard and soft selection in a subdivided population. Am. Nat. 109, 11–16. 15. Hughes, A.L., and Nei, M. (1988). Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170. 16. Fumagalli, M., Sironi, M., Pozzoli, U., Ferrer-Admettla, A., Pattini, L., and Nielsen, R. (2011). Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7, e1002355.
17. Bergland, A.O., Behrman, E.L., O’Brien, K.R., Schmidt, P.S., and Petrov, D.A. (2014). Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. e1004775. 18. Huang, Y., Wright, S.I., and Agrawal, A.F. (2014). Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genet. 10, e1004527.
19. Charlesworth, B. (2015). Causes of natural variation in fitness: evidence from studies of Drosophila populations. Proc. Natl. Acad. Sci. USA 112, 1662–1669. 20. Pujolar, J.M., Jacobsen, M.W., Als, T.D., Frydenberg, J., Munch, K., Jonsson, B., Jian, J.B., Cheng, L., Maes, G.E., Bernatchez, L., and Hansen, M.M. (2014). Genome-wide single-generation signatures of local selection in the panmictic European eel. Mol. Ecol. 23, 2514–2528.
Animal Behaviour: Friendship Enhances Trust in Chimpanzees Joan Silk School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287-2402, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.11.030
Individuals that participate in exchanges with delayed rewards can be exploited if their partners don’t reciprocate. In humans, friendships are built on trust, and trust enhances cooperation. New evidence suggests that close social bonds also enhance trust in chimpanzees. Ronald Reagan was responsible for popularizing a Russian proverb ‘‘trust, but verify’’. This proverb captures the dilemma that confronts individuals (or countries) when they venture into cooperative agreements, but are uncertain about the intentions of their partners. If there is some risk of being exploited, each side will need some guarantee that their partners will behave as promised. Formal institutions, like contracts, treaties, and international monitoring agencies, serve this purpose. But in informal interactions, we rely on knowledge of our partners’ past behavior and reputation to determine who we can trust. Trust is a key element of close social bonds, like friendship [1], and friendship enhances cooperation [2–4]. In this issue of Current Biology, Engelmann and Hermann [5] provide evidence that close social bonds may function in a similar way in chimpanzees. Economists define trust as an expectation about future cooperation in contexts in which there is some incentive
R76 Current Biology 26, R60–R82, January 25, 2016 ª2016 Elsevier Ltd All rights reserved
for partners to cheat [6]. This definition is operationalized in the trust game [7]. In this game, two players are given endowments: Player 1 can send any amount of her endowment to Player 2; the experimenter will triple the allocation, and the full amount will be delivered to Player 2. Then, Player 2 is given the opportunity to make an allocation to Player 1. To avoid the possibility that subjects will be influenced by concerns about their own reputation or future benefits, strangers are paired in anonymous one-shot games. If Player 1 thinks that Player 2 will treat her fairly, then it is best to send Player 2 the whole endowment; however, if Player 1 expects Player 2 to be selfish and keep all the money, then it is best to send nothing. The majority of people who take the role of Player 2 do send back money, and the amount that they send is proportional to the amount that they have received [8]. Engelmann et al. [9] developed an alternative version of the trust game for chimpanzees, who cannot multiply and do not tolerate strangers at close
Current Biology
Dispatches quarters. In the chimpanzee version of the game, Player 1 is given two options: she can choose a small reward for herself, or send two larger sets of rewards to Player 2. Player 2 obtains one set of the rewards, and can send the other set back to Player 1 or do nothing. This version of the game departs in some important ways from the trust game. First, Player 2 cannot keep the second set of rewards for herself, so she has much less incentive to defect than players in the human version of the game. Second, the game is repeated across several trials, so there are opportunities for direct reciprocity. Finally, the two players are not strangers, they are members of the same group with a long history of previous interactions. Nonetheless, Player 1’s best strategy still depends on the behavior of her partner: sending rewards to Player 2 only pays off if Player 2 actually sends food back; otherwise, Player 1 should choose the smaller reward. The results reported by Engelmann and Hermann [5] demonstrate that chimpanzees are fairly likely to send rewards to their partners initially, but adjust their behavior as they gain more information about their partners’ likelihood of returning food to them. They become more likely to send food to partners that reciprocate and less likely to send food to partners who do not. In an intriguing follow-up experiment, Engelmann and Hermann [5] asked whether close social bonds generate trust. To assess this, they compared chimpanzees’ behavior in the game when they were paired with animals with whom they had strong social bonds outside the confines of the experiment (friends) and animals with whom they had weak social bonds (nonfriends). Eleven of the 14 chimpanzees that they tested were more likely to send food to friends than to nonfriends, and on average chimpanzees sent food to friends about twice as often as they sent food to nonfriends. Engelmann and Hermann [5] conclude that ‘‘.chimpanzees, like humans, evolved robust forms of trust toward their close social partners, which might allow them to forge cooperative relationships even in contexts where threats of defection by cheaters loom large.’’
It is only profitable for individuals to base cooperation on trust if trust is linked to trustworthiness [10]. In this experiment, however, the rate of defection was actually very low, and nonfriends were just as likely to reciprocate as friends. This mismatch had material consequences for the chimpanzees because their reluctance to send rewards to nonfriends cost them opportunities to obtain higher payoffs. There are several possible explanations for the mismatch between trust and trustworthiness. It is possible that the chimpanzees’ decisions about whether to send food to friends and nonfriends were based on their knowledge of their partners’ behavior outside the context of the experiment. If the chimpanzees were uncertain about the behavior of those with whom they do not interact often (nonfriends) and they are averse to losses [11], then taking the small reward when paired with nonfriends might be a more attractive option than risking the loss of a larger reward. An alternative possible explanation is that chimpanzees do not practice strict tit-for-tat reciprocity. A number of studies of monkeys demonstrate that services, such as grooming, are reciprocated over extended time periods [12], and this may be true for chimpanzees as well. Thus, chimpanzees’ decisions about whether to send food to their partners may be based on their long-term history of interactions, not their expectation of immediate returns. A third possibility is that chimpanzees are motivated by generosity toward their friends, not their expectations about reciprocity. This interpretation would imply that chimpanzees would be willing to give up small rewards for themselves in order to provide larger rewards to friends. Engelmann and Hermann [5] are skeptical of this possibility. They cite evidence from a set of previous experiments in which one chimpanzee is offered a choice between one option that provides one reward to the actor and an identical reward to its partner (1/1) and another option that provides one reward to the actor and nothing to its partner (1/0) [13]. If chimpanzees prefer outcomes that benefit others, they are expected to choose the 1/1 option more often when a partner is present to receive rewards
than when they are alone. This has come to be known as the prosocial game. Even though chimpanzees can deliver rewards to others at no cost to themselves, they are no more likely to choose the 1/1 option when another chimpanzee is present than when they are alone. However, it is not clear how chimpanzees would behave in the prosocial game if they were paired with friends. Additional experiments could provide insight about the relative importance of generosity and expectations of reciprocity on chimpanzees’ behavior in the trust game. If chimpanzees are motivated mainly by generosity to friends, then we would expect them to choose the 1/1 option in the prosocial game more often when paired with friends than nonfriends. In Engelmann and Hermann’s [5] experiment, however, the chimpanzees had to give up rewards in order to deliver rewards to their partners. Thus, we also need to know how chimpanzees would behave when there was a conflict between self-interest and generosity. In the Costly Sharing game, the actor is given the choice between 1/1 and 2/0. This means the actor must make a sacrifice to provide rewards to its partner. If chimpanzees consistently choose 1/1 when paired with friends, then generosity is a plausible motivation for the behavior in Engelmann and Hermann’s [5] experiment. If they do not, then trust is a more compelling explanation for the results. I suspect that no one will run the costly sharing game with chimpanzees because they expect the results to be negative, even when chimpanzees are paired with friends. Negative results are hard to publish [14,15] and easy to dismiss [16]. But positive or negative results in the costly sharing game would be interesting because we know that children often behave altruistically in this game when they are randomly paired with classmates [17,18] or anonymous recipients [19]. While positive results in experiments like the chimpanzee trust game suggest similarities between humans and other primates, negative results in experiments can help us to define the differences. We need both kinds of data if we want to understand the origins of cooperation in the human species.
Current Biology 26, R60–R82, January 25, 2016 ª2016 Elsevier Ltd All rights reserved R77
Current Biology
Dispatches REFERENCES 1. Hruschka, D. (2010). Friendship: Development, Ecology and Evolution of a Relationship (Berkeley: University of California Press). 2. Majolo, B., Ames, K., Brumpton, R., Garratt, R., Hall, K., and Wilson, N. (2006). Human friendship favours cooperation in the Iterated Prisoner’s Dilemma. Behaviour 143, 1383– 1395.
7. Berg, J., Dickhaut, J., and McCabe, K. (1995). Trust, reciprocity, and social history. Games Econ. Behav. 10, 122–142. 8. Johnson, N.D., and Mislin, A.A. (2011). Trust games: a meta-analysis. J. Econ. Psychol. 32, 865–889. 9. Engelmann, J.M., Herrmann, E., and Tomasello, M. (2015). Chimpanzees trust conspecifics to engage in low-cost reciprocity. Proc. R. Soc. Lond. B 282, 20142803.
3. Harrison, F., Sciberras, J., and James, R. (2011). Strength of social tie predicts cooperative investment in a human social network. PLoS One 6, e18338.
10. Braynov, S., and Sandholm, T. (2002). Contracting with uncertain level of trust. Comp. Intel. 18, 501–514.
4. Xue, M., and Silk, J.B. (2012). The role of tracking and tolerance in relationships among friends. Evol. Hum. Behav. 33, 17–25.
11. Krupenye, C., Rosati, A.G., and Hare, B. (2015). Bonobos and chimpanzees exhibit human-like framing effects. Biol. Lett. 11, 20140527.
5. Engelmann, J.M., and Hermann, E. (2016). Chimpanzees trust their friends. Curr. Biol. 26, 252–256. 6. Burt, R.S., and Knez, M. (1996). Trust and third-party gossip. In Trust in Organizations: Frontiers of Theory and Research, R.M. Kramer, and T.R. Tyler, eds. (Thousand Oaks: Sage Publications), pp. 68–89.
12. Seyfarth, R.M., and Cheney, D.L. (2012). The evolutionary origins of friendship. Annu. Rev. Psychol. 63, 153–177. 13. Silk, J.B., and House, B.R. (2015). The evolution of altruistic social preferences in human groups. Phil. Trans. R. Soc. B, 20150097.
14. Matosin, N., Frank, E., Engel, M., Lum, J.S., and Newell, K.A. (2014). Negativity towards negative results: a discussion of the disconnect between scientific worth and scientific culture. Dis. Model Mech. 7, 171–173. 15. Fanelli, D. (2011). Negative results are disappearing from most disciplines and countries. Scientometrics 90, 891–904. 16. De Waal, F.B.M. (2009). The Age of Empathy (New York: Harmony Books). 17. House, B.R., Henrich, J., Brosnan, S.F., and Silk, J.B. (2012). The ontogeny of human prosociality: behavioral experiments with children aged 3 to 8. Evol. Hum. Behav. 33, 291–308. 18. House, B.R., Silk, J.B., Henrich, J., Barrett, H.C., Scelza, B., Boyette, A., Hewlett, B., and Laurence, S. (2013). The ontogeny of prosocial behavior across diverse cultures. Proc. Natl. Acad. Sci. USA 110, 14586–14591. 19. Fehr, E., Bernhard, H., and Rockenbach, B. (2008). Egalitarianism in young children. Nature 454, 1079–1083.
Signal Evolution: ‘Shaky’ Evidence for Sensory Bias Sonia Pascoal, Peter Moran, and Nathan W. Bailey* Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, UK *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.11.045
A study of tropical crickets suggests that a twitchy response to ultrasonic bat calls has been co-opted for mate location. The neuroethological approach picks apart some surprising evolutionary steps that could inform the widespread occurrence of complex duetting behaviour. What accounts for the impressive complexity and behavioural coordination of mate signaling in so many species? One idea that researchers have come to appreciate in recent decades is that pre-existing biases in sensory mechanisms can provide a ready-made substrate for sexual selection to exploit in the context of mate attraction [1]. It would seem logical that mating signals evolving in such circumstances should mimic or overlap with cues that provoke positive responses in potential mates, such as colouration or movement associated with tasty food items [2,3]. However, male courtship signals can also evolve to exploit aversive stimuli, such as predator cues.
Examples of the latter are less common, but classic research on sensory exploitation in moths has shown that males in some species produce an ultrasonic signal mimicking predatory bat calls that cause females to freeze, which facilitates mating [4–6]. A recent study by ter Hofstede et al. [7] in Current Biology proposes that a similar mechanism of sensory exploitation may have driven the evolution of a complex, multi-modal mating duet in a group of tropical crickets — the Lebinthini (Figure 1). Their study coincides with a recent publication by Rajamaran et al. [8] on a bushcricket, Onomarchus uninotatus, which displays a similarly complex duet
R78 Current Biology 26, R60–R82, January 25, 2016 ª2016 Elsevier Ltd All rights reserved
involving the same two modalities: acoustic song and vibration [8]. Sexual duetting is a well-established phenomenon in many insect taxa [9]. However, both the field cricket and bushcricket present tricky evolutionary puzzles to crack, because sexual communication in each species involves more than one set of signals and responses whose smooth functioning depend on one another [7,8]. If a sexual signal arose through sensory exploitation, the response to the signal should predate the appearance of the signal itself [10]. To peel apart the co-evolutionary steps that might be involved, ter Hofstede et al. [7] took a phylogenetically-informed approach, and
Dispatches balancing selection on patterns of genetic variation will surely continue. REFERENCES 1. Darwin, C. (1859). The Origin of Species by Means of Natural Selection, or the Preservation of Favored Races in the Struggle for Life (London: John Murray). 2. Cutter, A.D., Jovelin, R., and Dey, A. (2013). Molecular hyperdiversity and evolution in very large populations. Mol. Ecol. 22, 2074–2095. 3. Chakraborty, M., and Fry, J.D. (2016). Evidence that environmental heterogeneity maintains a detoxifying enzyme polymorphism in Drosophila melanogaster. Curr. Biol. 26, 219–223. 4. Dobzhansky, T. (1951). Genetics and the Origin of Species (Columbia University Press). 5. Levene, H. (1953). Genetic equilibrium when more than one ecological niche is available. Am. Nat. 87, 331–333. 6. Dempster, E.R. (1955). Maintenance of genetic heterogeneity. Cold Spring Harbor Symp. Quant. Biol. 20, 25–32. 7. Hedrick, P.W. (2006). Genetic polymorphism in heterogeneous environments: the age of genomics. Annu. Rev. Ecol. Evol. Syst. 37, 67–93. 8. Gillespie, J.H., and Turelli, M. (1989). Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121, 129–138. 9. Allison, A.C. (1954). Protection afforded by sickle-cell trait against subtertian malarial infection. Br. Med. J. 1, 290–294. 10. Lewontin, R.C., and Hubby, J.L. (1966). A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54, 595–609. 11. Gillespie, J.H., and Langley, C.H. (1974). A general model to account for enzyme variation in natural populations. Genetics 76, 837–848. 12. Kimura, M. (1968). Evolutionary rate at the molecular level. Nature 217, 624–626. 13. Lande, R. (1976). The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet. Res. 26, 221–235. 14. Christiansen, F.B. (1975). Hard and soft selection in a subdivided population. Am. Nat. 109, 11–16. 15. Hughes, A.L., and Nei, M. (1988). Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170. 16. Fumagalli, M., Sironi, M., Pozzoli, U., Ferrer-Admettla, A., Pattini, L., and Nielsen, R. (2011). Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7, e1002355.
17. Bergland, A.O., Behrman, E.L., O’Brien, K.R., Schmidt, P.S., and Petrov, D.A. (2014). Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. e1004775. 18. Huang, Y., Wright, S.I., and Agrawal, A.F. (2014). Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genet. 10, e1004527.
19. Charlesworth, B. (2015). Causes of natural variation in fitness: evidence from studies of Drosophila populations. Proc. Natl. Acad. Sci. USA 112, 1662–1669. 20. Pujolar, J.M., Jacobsen, M.W., Als, T.D., Frydenberg, J., Munch, K., Jonsson, B., Jian, J.B., Cheng, L., Maes, G.E., Bernatchez, L., and Hansen, M.M. (2014). Genome-wide single-generation signatures of local selection in the panmictic European eel. Mol. Ecol. 23, 2514–2528.
Animal Behaviour: Friendship Enhances Trust in Chimpanzees Joan Silk School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287-2402, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.11.030
Individuals that participate in exchanges with delayed rewards can be exploited if their partners don’t reciprocate. In humans, friendships are built on trust, and trust enhances cooperation. New evidence suggests that close social bonds also enhance trust in chimpanzees. Ronald Reagan was responsible for popularizing a Russian proverb ‘‘trust, but verify’’. This proverb captures the dilemma that confronts individuals (or countries) when they venture into cooperative agreements, but are uncertain about the intentions of their partners. If there is some risk of being exploited, each side will need some guarantee that their partners will behave as promised. Formal institutions, like contracts, treaties, and international monitoring agencies, serve this purpose. But in informal interactions, we rely on knowledge of our partners’ past behavior and reputation to determine who we can trust. Trust is a key element of close social bonds, like friendship [1], and friendship enhances cooperation [2–4]. In this issue of Current Biology, Engelmann and Hermann [5] provide evidence that close social bonds may function in a similar way in chimpanzees. Economists define trust as an expectation about future cooperation in contexts in which there is some incentive
R76 Current Biology 26, R60–R82, January 25, 2016 ª2016 Elsevier Ltd All rights reserved
for partners to cheat [6]. This definition is operationalized in the trust game [7]. In this game, two players are given endowments: Player 1 can send any amount of her endowment to Player 2; the experimenter will triple the allocation, and the full amount will be delivered to Player 2. Then, Player 2 is given the opportunity to make an allocation to Player 1. To avoid the possibility that subjects will be influenced by concerns about their own reputation or future benefits, strangers are paired in anonymous one-shot games. If Player 1 thinks that Player 2 will treat her fairly, then it is best to send Player 2 the whole endowment; however, if Player 1 expects Player 2 to be selfish and keep all the money, then it is best to send nothing. The majority of people who take the role of Player 2 do send back money, and the amount that they send is proportional to the amount that they have received [8]. Engelmann et al. [9] developed an alternative version of the trust game for chimpanzees, who cannot multiply and do not tolerate strangers at close
Current Biology
Dispatches quarters. In the chimpanzee version of the game, Player 1 is given two options: she can choose a small reward for herself, or send two larger sets of rewards to Player 2. Player 2 obtains one set of the rewards, and can send the other set back to Player 1 or do nothing. This version of the game departs in some important ways from the trust game. First, Player 2 cannot keep the second set of rewards for herself, so she has much less incentive to defect than players in the human version of the game. Second, the game is repeated across several trials, so there are opportunities for direct reciprocity. Finally, the two players are not strangers, they are members of the same group with a long history of previous interactions. Nonetheless, Player 1’s best strategy still depends on the behavior of her partner: sending rewards to Player 2 only pays off if Player 2 actually sends food back; otherwise, Player 1 should choose the smaller reward. The results reported by Engelmann and Hermann [5] demonstrate that chimpanzees are fairly likely to send rewards to their partners initially, but adjust their behavior as they gain more information about their partners’ likelihood of returning food to them. They become more likely to send food to partners that reciprocate and less likely to send food to partners who do not. In an intriguing follow-up experiment, Engelmann and Hermann [5] asked whether close social bonds generate trust. To assess this, they compared chimpanzees’ behavior in the game when they were paired with animals with whom they had strong social bonds outside the confines of the experiment (friends) and animals with whom they had weak social bonds (nonfriends). Eleven of the 14 chimpanzees that they tested were more likely to send food to friends than to nonfriends, and on average chimpanzees sent food to friends about twice as often as they sent food to nonfriends. Engelmann and Hermann [5] conclude that ‘‘.chimpanzees, like humans, evolved robust forms of trust toward their close social partners, which might allow them to forge cooperative relationships even in contexts where threats of defection by cheaters loom large.’’
It is only profitable for individuals to base cooperation on trust if trust is linked to trustworthiness [10]. In this experiment, however, the rate of defection was actually very low, and nonfriends were just as likely to reciprocate as friends. This mismatch had material consequences for the chimpanzees because their reluctance to send rewards to nonfriends cost them opportunities to obtain higher payoffs. There are several possible explanations for the mismatch between trust and trustworthiness. It is possible that the chimpanzees’ decisions about whether to send food to friends and nonfriends were based on their knowledge of their partners’ behavior outside the context of the experiment. If the chimpanzees were uncertain about the behavior of those with whom they do not interact often (nonfriends) and they are averse to losses [11], then taking the small reward when paired with nonfriends might be a more attractive option than risking the loss of a larger reward. An alternative possible explanation is that chimpanzees do not practice strict tit-for-tat reciprocity. A number of studies of monkeys demonstrate that services, such as grooming, are reciprocated over extended time periods [12], and this may be true for chimpanzees as well. Thus, chimpanzees’ decisions about whether to send food to their partners may be based on their long-term history of interactions, not their expectation of immediate returns. A third possibility is that chimpanzees are motivated by generosity toward their friends, not their expectations about reciprocity. This interpretation would imply that chimpanzees would be willing to give up small rewards for themselves in order to provide larger rewards to friends. Engelmann and Hermann [5] are skeptical of this possibility. They cite evidence from a set of previous experiments in which one chimpanzee is offered a choice between one option that provides one reward to the actor and an identical reward to its partner (1/1) and another option that provides one reward to the actor and nothing to its partner (1/0) [13]. If chimpanzees prefer outcomes that benefit others, they are expected to choose the 1/1 option more often when a partner is present to receive rewards
than when they are alone. This has come to be known as the prosocial game. Even though chimpanzees can deliver rewards to others at no cost to themselves, they are no more likely to choose the 1/1 option when another chimpanzee is present than when they are alone. However, it is not clear how chimpanzees would behave in the prosocial game if they were paired with friends. Additional experiments could provide insight about the relative importance of generosity and expectations of reciprocity on chimpanzees’ behavior in the trust game. If chimpanzees are motivated mainly by generosity to friends, then we would expect them to choose the 1/1 option in the prosocial game more often when paired with friends than nonfriends. In Engelmann and Hermann’s [5] experiment, however, the chimpanzees had to give up rewards in order to deliver rewards to their partners. Thus, we also need to know how chimpanzees would behave when there was a conflict between self-interest and generosity. In the Costly Sharing game, the actor is given the choice between 1/1 and 2/0. This means the actor must make a sacrifice to provide rewards to its partner. If chimpanzees consistently choose 1/1 when paired with friends, then generosity is a plausible motivation for the behavior in Engelmann and Hermann’s [5] experiment. If they do not, then trust is a more compelling explanation for the results. I suspect that no one will run the costly sharing game with chimpanzees because they expect the results to be negative, even when chimpanzees are paired with friends. Negative results are hard to publish [14,15] and easy to dismiss [16]. But positive or negative results in the costly sharing game would be interesting because we know that children often behave altruistically in this game when they are randomly paired with classmates [17,18] or anonymous recipients [19]. While positive results in experiments like the chimpanzee trust game suggest similarities between humans and other primates, negative results in experiments can help us to define the differences. We need both kinds of data if we want to understand the origins of cooperation in the human species.
Current Biology 26, R60–R82, January 25, 2016 ª2016 Elsevier Ltd All rights reserved R77
Current Biology
Dispatches REFERENCES 1. Hruschka, D. (2010). Friendship: Development, Ecology and Evolution of a Relationship (Berkeley: University of California Press). 2. Majolo, B., Ames, K., Brumpton, R., Garratt, R., Hall, K., and Wilson, N. (2006). Human friendship favours cooperation in the Iterated Prisoner’s Dilemma. Behaviour 143, 1383– 1395.
7. Berg, J., Dickhaut, J., and McCabe, K. (1995). Trust, reciprocity, and social history. Games Econ. Behav. 10, 122–142. 8. Johnson, N.D., and Mislin, A.A. (2011). Trust games: a meta-analysis. J. Econ. Psychol. 32, 865–889. 9. Engelmann, J.M., Herrmann, E., and Tomasello, M. (2015). Chimpanzees trust conspecifics to engage in low-cost reciprocity. Proc. R. Soc. Lond. B 282, 20142803.
3. Harrison, F., Sciberras, J., and James, R. (2011). Strength of social tie predicts cooperative investment in a human social network. PLoS One 6, e18338.
10. Braynov, S., and Sandholm, T. (2002). Contracting with uncertain level of trust. Comp. Intel. 18, 501–514.
4. Xue, M., and Silk, J.B. (2012). The role of tracking and tolerance in relationships among friends. Evol. Hum. Behav. 33, 17–25.
11. Krupenye, C., Rosati, A.G., and Hare, B. (2015). Bonobos and chimpanzees exhibit human-like framing effects. Biol. Lett. 11, 20140527.
5. Engelmann, J.M., and Hermann, E. (2016). Chimpanzees trust their friends. Curr. Biol. 26, 252–256. 6. Burt, R.S., and Knez, M. (1996). Trust and third-party gossip. In Trust in Organizations: Frontiers of Theory and Research, R.M. Kramer, and T.R. Tyler, eds. (Thousand Oaks: Sage Publications), pp. 68–89.
12. Seyfarth, R.M., and Cheney, D.L. (2012). The evolutionary origins of friendship. Annu. Rev. Psychol. 63, 153–177. 13. Silk, J.B., and House, B.R. (2015). The evolution of altruistic social preferences in human groups. Phil. Trans. R. Soc. B, 20150097.
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Signal Evolution: ‘Shaky’ Evidence for Sensory Bias Sonia Pascoal, Peter Moran, and Nathan W. Bailey* Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, UK *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.11.045
A study of tropical crickets suggests that a twitchy response to ultrasonic bat calls has been co-opted for mate location. The neuroethological approach picks apart some surprising evolutionary steps that could inform the widespread occurrence of complex duetting behaviour. What accounts for the impressive complexity and behavioural coordination of mate signaling in so many species? One idea that researchers have come to appreciate in recent decades is that pre-existing biases in sensory mechanisms can provide a ready-made substrate for sexual selection to exploit in the context of mate attraction [1]. It would seem logical that mating signals evolving in such circumstances should mimic or overlap with cues that provoke positive responses in potential mates, such as colouration or movement associated with tasty food items [2,3]. However, male courtship signals can also evolve to exploit aversive stimuli, such as predator cues.
Examples of the latter are less common, but classic research on sensory exploitation in moths has shown that males in some species produce an ultrasonic signal mimicking predatory bat calls that cause females to freeze, which facilitates mating [4–6]. A recent study by ter Hofstede et al. [7] in Current Biology proposes that a similar mechanism of sensory exploitation may have driven the evolution of a complex, multi-modal mating duet in a group of tropical crickets — the Lebinthini (Figure 1). Their study coincides with a recent publication by Rajamaran et al. [8] on a bushcricket, Onomarchus uninotatus, which displays a similarly complex duet
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involving the same two modalities: acoustic song and vibration [8]. Sexual duetting is a well-established phenomenon in many insect taxa [9]. However, both the field cricket and bushcricket present tricky evolutionary puzzles to crack, because sexual communication in each species involves more than one set of signals and responses whose smooth functioning depend on one another [7,8]. If a sexual signal arose through sensory exploitation, the response to the signal should predate the appearance of the signal itself [10]. To peel apart the co-evolutionary steps that might be involved, ter Hofstede et al. [7] took a phylogenetically-informed approach, and