Nonhuman Reciprocal Altruism
KeywordsRepeated Interaction Reciprocal Altruism Indirect Reciprocity Neighboring Territory Generalize Reciprocity
An evolutionarily stable strategy of enforcing cooperation by conditionally helping based on past experience of the recipient’s help.
How does the ruthlessly competitive process of natural selection lead to unselfish traits, such as a tendency to help others? Many birds and mammals give alarm calls that help others escape predators, rather than simply and selfishly running away to get farther from the predator than other group members. Primates spend time and energy grooming the fur of others in their group. Vampire bats regurgitate a portion of their food to feed hungry groupmates, even nonrelatives, which failed to feed. If these costly investments in helping others could have been spent furthering one’s own reproductive success, then why would natural selection reward these behaviors? The puzzle is that cooperative individuals pay a cost to increase the reproductive success of others, while more selfish individuals are not paying those same costs. All else being equal, selfishness should outbreed cooperation.
Evolutionary explanations of cooperation solve this puzzle. For example, natural selection rewards altruism when it is targeted to close kin. This is because close kin are more likely to carry the same genes underlying the altruistic trait, so genes linked to altruistic traits favor replication of those same genes in other individuals, a process called kin selection.
Robert Trivers (1971) proposed “reciprocal altruism” as an explanation for apparent altruism between nonkin. Reciprocal altruism theory views acts of helping as cooperative investments that yield a reciprocal cooperative return, and it makes the prediction that individuals will preferentially help those individuals who are likely to later help them, even if those individuals are unrelated. Many evolutionary biologists prefer the term “reciprocity” because “reciprocal altruism” is not truly “altruistic.” In the standard terminology of evolutionary biology, altruism is helping behavior that decreases the actor’s lifetime reproductive success. Reciprocity, by contrast, provides a long-term mutual benefit to both actor and receiver.
What is Reciprocity?
Here’s how reciprocity works: Individual A makes a cooperative investment in individual B, such as social grooming, food sharing, or risking one’s safety to help an individual in need. This investment increases the probability that individual B will later make a reciprocal investment in A. The term “investment” implies that it is in some way contingent on the returns. So if A stops helping B, then B will eventually stop helping A, and vice versa. This contingency prevents free-riding, or cheating, because B cannot continually receive help from A without reciprocating. Reciprocity requires repeated interactions and contingent helping based on past experience (Axelrod and Hamilton 1981).
Some authors contrast “direct reciprocity” where A helps B because B helps A with “indirect reciprocity” where A helps B because B helps C. In this case, A evaluates B as a potential cooperator, and B helps C to build a reputation as a good cooperator. There is also the concept of “generalized reciprocity” where A helps B because A was helped by any other individual. The tendency of humans to both cooperate and punish noncooperators, even in one-shot economic games without repeated interactions, has been called “strong reciprocity,” but this behavior is most likely a by-product of natural selection shaping human decision-making in such a way that humans treat most or all social interactions as if they might be repeated (Delton et al. 2011).
What is the Evidence for Nonhuman Reciprocity?
There are many natural examples of organisms in nature making cooperative investments that are contingent on the cooperative returns. Unless otherwise noted, the older examples below are taken from a review by Carter (2014) and the references cited therein, while more recent studies (post-2013) are cited here. In the cleaner-client fish mutualism, small cleaners eat dead skin off larger “client” fish, which benefits both parties. But the cleaners can also “cheat” by eating mucus or live tissue, which benefits the cleaner but hurts the client. Both cleaners and clients enforce cooperation through reward and punishment (direct reciprocity) and through image scoring (indirect reciprocity). Clients abandon or chase cleaners that cheat, and they avoid cleaners that they observe cheating with other clients. Cleaners behave more cooperatively when they are punished and when they are observed by other clients. Cleaners also enforce good behavior in other cleaners; they will punish cheating cleaners that might otherwise drive good clients away, an example of third-party punishment.
Even brainless organisms can perform a simple version of reciprocity. Plants contingently trade resources with symbiotic partners such as fungi and bacteria. By diverting resources to different structures, plants can selectively eliminate symbionts that do not provide good returns. For example, plants provide mycorrhizal fungi with carbon in exchange for phosphorus. Both parties reward high returns and punish low returns, by delivering more or less of the resource to match the amount of the return.
Some authors consider individual recognition and memory to be a prerequisite for reciprocity, in addition to contingency and repeated interactions. In one set of experiments, rats were trained to pull a lever to deliver food to conspecifics, and the experimenters then showed that the rats were more likely to deliver food to partners that previously delivered food to them. Anonymous help increased pulling by 20 %, which shows “generalized reciprocity,” and help from the same partner increased it an additional 51 %, which shows “direct reciprocity” based on recognition and memory of specific individual’s past behavior.
In nature, contingency in helping is most detectable in scenarios where animals cannot choose their partners. One example involves songbirds on neighboring territories. As male songbirds on neighboring territories become familiar with each other, they tend to reduce aggression towards one another as compared to strangers, which is called “the Dear Enemy effect.” By experimentally simulating territorial intrusions by neighboring males, experimenters found that male song sparrows increase their aggression to previously intruding neighbors but not to those that did not. Either reducing or escalating aggression is based on what the neighboring rival did previously.
Reciprocity might also occur between songbird parents raising offspring together. Great Tit parents were found to feed nestlings in a balanced alternating pattern unexplainable by foraging or begging times. Each parent increased feeding rates after their partners contributed but reduced their feeding rate by about 25 % until their partner contributed (Johnstone et al. 2014). These two examples from songbirds, rival males and allied parents, show that reciprocity results from the mix of cooperation and conflict that occurs in all social interactions that evolve via natural selection.
Some of the best experimental evidence of reciprocity comes from mobbing behavior of birds. Experimenters used fake owls to induce cooperative mobbing in 44 triads of pied flycatcher mated pairs, with each triad consisting of three equidistant nestboxes. One pair (the victims) was exposed to a fake owl near their nestbox to induce mobbing, another pair (the defectors) was prevented from mobbing, and the third pair (the helpers) was left untreated. Therefore, the “helpers” always helped the “victims” with mobbing, but the “defectors” never did. Later, when the authors simultaneously presented the previous “helpers” and “defectors” with owls, the previous “victims” helped the previous helpers in 30 of 32 trials. In a follow-up experiment, when the previous “defectors” were presented with an owl, the “helpers” (but typically not the “victims”) joined the “defectors” in mobbing, as expected if only the “victims” experienced a defection. Later experiments further ruled out the possibility that reciprocal mobbing at nestboxes was purely a by-product benefit of selfish behavior. Astonishingly, the degree of reciprocity was also sensitive to whether the failure of partners to mob was caused by their complete absence. When experimenters used playbacks of recordings to make pairs seem present but unwilling to join, the rate of defection increased dramatically.
Much like mobbing birds, pairs of fish will also sometimes cooperatively approach and inspect predators, such as larger predatory fish. They appear to do this to assess the situation while maintaining the safety of a companion. One hypothesis is that the fish enforce partner cooperation by approaching closer only if their partner swims beside them. This hypothesis is supported by several experimental results. There are differences in predator inspection behavior of fish from populations with either high or low predation. Predator approach behavior is riskier for single fish and leading fish. Predator inspection involves partner recognition, it is contingent on a partner’s past and present predator inspection behavior, and it is more likely to occur with partners that have a history of social interaction.
As in several of the examples above, reciprocity often involves clear turn-taking. Other examples include two hermaphroditic fish that take turns trading egg or sperm and when migrating birds take turns flying in the more costly lead position of a flight formation (Voelkl et al. 2015). But strict turn-taking is not a prerequisite for cooperation, and it does not occur in many long-term reciprocal relationships that may involve the exchange of different kinds of help. For example, primates create and maintain enduring social bonds that involve multiple forms of cooperative investments. Chimpanzees of both sexes appear to exchange several different commodities, including grooming, sex, support, and food, resulting in balanced relationships over extended periods. Similar to humans, nonhuman primates cooperate in a more strictly contingent manner with partners that are actually less bonded. Most experimental evidence for strict short-term contingency therefore comes from more simple systems such as those with rats, plants, and fish described, because it is difficult to alter a complex friendship-like social bond in a short window of time.
Many cooperative social bonds form between relatives, which can make reciprocity difficult to distinguish from nepotism. Moreover, reciprocity and nepotism can occur simultaneously because reciprocity can enforce cooperation between relatives. The best evidence for this comes from vampire bats (see “Blood Sharing in Vampire Bats,” this volume).
Many authors view reciprocity as a controversial explanation for cooperation, but this debate is mostly or entirely semantic: it revolves around different definitions of reciprocity that are narrow versus broad or functional versus mechanistic. For instance, some authors use “reciprocity” for a calculated investment where individuals suppress selfishness to intentionally and strategically help another with the expected outcome of receiving a given amount in return, which requires the ability to plan ahead, value future over present outcomes, and maybe even count. This very narrowly defined kind of reciprocity is the basis for human trade, but it all but excludes its importance in anything but humans. It also departs from the original broader definition, proposed by Trivers (1971) and Axelrod and Hamilton (1981).
One criticism of reciprocity theory is that it historically focused on dyads in isolation and thus ignored the vast importance of partner switching and choice. Why reward and punish a single partner, when one can simply switch to a different partner? Biological market theory (Noë and Hammerstein 1994) addresses this gap by starting with the assumption that cooperative investments lead to cooperative returns and then producing testable predictions for how market effects, such as the supply and demand of available partners, will influence both partner choice and partner control (reward and punishment). When one partner holds more bargaining power, trade can be asymmetric. For example, when experimenters created a situation when only one low-ranking monkey could open a food box, she subsequently received far more grooming. But when a second monkey was given this food-provisioning power, the grooming she received went up, while the grooming the first provider received decreased. The monkeys make cooperative investments based not only on past returns but also the relative value of alternative investments.
Reciprocity is a controversial but important explanation for cooperation.
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