From the Cover: Auditory plasticity and speech motor learning

Is plasticity in sensory and motor systems linked? Here, in the context of speech motor learning and perception, we test the idea sensory function is modified by motor learning and, in particular, that speech motor learning affects a speaker''s auditory map. We assessed speech motor learning by using a robotic device that displaced the jaw and selectively altered somatosensory feedback during speech. We found that with practice speakers progressively corrected for the mechanical perturbation and after motor learning they also showed systematic changes in their perceptual classification of speech sounds. The perceptual shift was tied to motor learning. Individuals that displayed greater amounts of learning also showed greater perceptual change. Perceptual change was not observed in control subjects that produced the same movements, but in the absence of a force field, nor in subjects that experienced the force field but failed to adapt to the mechanical load. The perceptual effects observed here indicate the involvement of the somatosensory system in the neural processing of speech sounds and suggest that speech motor learning results in changes to auditory perceptual function.     

From the Cover: Evolution of microbial markets

Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.     

From the Cover: Evolution of fairness in the one-shot anonymous Ultimatum Game

Classical economic models assume that people are fully rational and selfish, while experiments often point to different conclusions. A canonical example is the Ultimatum Game: one player proposes a division of a sum of money between herself and a second player, who either accepts or rejects. Based on rational self-interest, responders should accept any nonzero offer and proposers should offer the smallest possible amount. Traditional, deterministic models of evolutionary game theory agree: in the one-shot anonymous Ultimatum Game, natural selection favors low offers and demands. Experiments instead show a preference for fairness: often responders reject low offers and proposers make higher offers than needed to avoid rejection. Here we show that using stochastic evolutionary game theory, where agents make mistakes when judging the payoffs and strategies of others, natural selection favors fairness. Across a range of parameters, the average strategy matches the observed behavior: proposers offer between 30% and 50%, and responders demand between 25% and 40%. Rejecting low offers increases relative payoff in pairwise competition between two strategies and is favored when selection is sufficiently weak. Offering more than you demand increases payoff when many strategies are present simultaneously and is favored when mutation is sufficiently high. We also perform a behavioral experiment and find empirical support for these theoretical findings: uncertainty about the success of others is associated with higher demands and offers; and inconsistency in the behavior of others is associated with higher offers but not predictive of demands. In an uncertain world, fairness finishes first.     

From the Cover: Model of genetic variation in human social networks

Social networks exhibit strikingly systematic patterns across a wide range of human contexts. Although genetic variation accounts for a significant portion of the variation in many complex social behaviors, the heritability of egocentric social network attributes is unknown. Here, we show that 3 of these attributes (in-degree, transitivity, and centrality) are heritable. We then develop a “mirror network” method to test extant network models and show that none account for observed genetic variation in human social networks. We propose an alternative “Attract and Introduce” model with two simple forms of heterogeneity that generates significant heritability and other important network features. We show that the model is well suited to real social networks in humans. These results suggest that natural selection may have played a role in the evolution of social networks. They also suggest that modeling intrinsic variation in network attributes may be important for understanding the way genes affect human behaviors and the way these behaviors spread from person to person.     

From the Cover: Economic contract theory tests models of mutualism

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.     

From the Cover: Whole-agent selectivity within the macaque face-processing system

The primate brain contains a set of face-selective areas, which are thought to extract the rich social information that faces provide, such as emotional state and personal identity. The nature of this information raises a fundamental question about these face-selective areas: Do they respond to a face purely because of its visual attributes, or because the face embodies a larger social agent? Here, we used functional magnetic resonance imaging to determine whether the macaque face patch system exhibits a whole-agent response above and beyond its responses to individually presented faces and bodies. We found a systematic development of whole-agent preference through the face patches, from subadditive integration of face and body responses in posterior face patches to superadditive integration in anterior face patches. Superadditivity was not observed for faces atop nonbody objects, implying categorical specificity of face–body interaction. Furthermore, superadditivity was robust to visual degradation of facial detail, suggesting whole-agent selectivity does not require prior face recognition. In contrast, even the body patches immediately adjacent to anterior face areas did not exhibit superadditivity. This asymmetry between face- and body-processing systems may explain why observers attribute bodies’ social signals to faces, and not vice versa. The development of whole-agent selectivity from posterior to anterior face patches, in concert with the recently described development of natural motion selectivity from ventral to dorsal face patches, identifies a single face patch, AF (anterior fundus), as a likely link between the analysis of facial shape and semantic inferences about other agents.Making sense of the world around us is a computationally daunting challenge and one of the brain’s great feats. The face patch system of the macaque monkey (ref. 1; Fig. 1A) is a uniquely valuable model for understanding how the brain constructs a meaningful representation of the visual world (2). This network of areas along the superior temporal sulcus (STS) of the temporal lobe responds selectively to the sight of faces, parses their visual properties, and supports their perception (3, 4). However, face recognition is just one part of a greater perceptual goal. Faces are singularly rich sources of social information: They convey the identities (5), emotions (6), and intentions (7) of entire agents. This unique aspect of faces raises a critical question: Do face patches respond to a face because they are fundamentally selective for facial shapes, or because these areas represent the larger agent embodied by the face?Open in a separate windowFig. 1.Experimental plan. (A) Schematic of the macaque face and body patches along the STS of a right hemisphere, with the anterior temporal pole on the right. (B) Three hypothetical responses of a model face patch to a face and body viewed together. Red and blue bars indicate the response of the patch to lone faces and headless bodies, respectively. Purple outlines show possible whole-agent response signatures given the responses to face and body. A strictly selective response to whole monkeys would be equivalent to the response to isolated faces, an additive response would equal the sum of the responses to individually presented faces and bodies, and a superadditive response would exceed this sum. Note that whereas a strictly selective or additive response could be created by a mix of selective face and body cells, a superadditive response is highly indicative of joint representation of face and body by single neurons (18).Currently, it is thought that two distinct temporal lobe networks—the face patches and a parallel system of body-selective patches (8–10)—separately process the visual features of social agents. However, the sight of a body can alter the perception of a face (11), and some neurons in the upper STS have been found to integrate face and body information (12). Although face patch neurons respond poorly to images of headless bodies (3), an untested possibility exists that they integrate information from a paired face and body to represent an agent as a whole.Learning whether face patches represent whole agents would address the larger question of where the machinery of facial perception transitions into the machinery of social cognition—the ability to combine posture, motion, and other social information to understand and interact with others (13, 14). One indication that this transition may occur within the face system is that dorsal patches are specifically sensitive to the naturalness of facial motion (15), an important quality for social understanding (16). Integration of face and body is an ideal signature with which to confirm whether social processing begins in the face patches because, unlike traits such as “theory of mind” that are challenging to test with precision (17), it is easily operationalized. The hypothesis that dorsal face areas represent social agents, and not merely facial features, predicts a ventral-to-dorsal development of whole-agent integration across the temporal lobe. In contrast, the prevailing view that face patches are strictly face-selective modules predicts that adding a body to a face will produce no effect in any patch. Identifying how each face patch responds to whole agents would test these two possibilities, and clarify if and how social knowledge evolves within the face-processing system.In this study, we set out to determine whether macaque face or body patches integrate face and body information to represent whole animals. We did this by pairing pictures of faces with pictures of bodies or matched nonbody objects (Fig. S1), then using functional magnetic resonance imaging (fMRI) to observe the response signatures that these stimuli evoked (Fig. 1B). If face patches were strictly category-selective for faces, they would respond to pictures of whole monkeys just as much as they responded to faces alone. If, alternatively, face patches were composed of independently face- and body-selective cells, their response would be additive, the sum of the separate responses to lone faces and lone bodies. However, a superadditive response to whole monkeys would argue against these models of strict category selectivity and for synergistic whole-animal processing within the face patches (18). By observing whether the whole-animal responses differed from the responses to faces on top of nonbody objects, we determined the selectivity of face patches’ responses to whole animals. Finally, we tested whether the face patches integrate the form of whole animals even in the absence of identifiable facial features, observing how they responded to visually obscured faces paired with bodies and nonbody objects. Comparing the results of these three experiments, we could determine whether face patches may be strictly concerned with the visual details of faces, or whether they sometimes process social information gathered from across an agent.Open in a separate windowFig. S1.Sample stimuli from the whole agent stimulus set. These stimuli represent all of the stimuli derived from the picture of a single monkey; the full stimulus set contained 14 additional examples of each stimulus type. Objects presented in the lower visual field were chosen to match the overall shape and size of the bodies. The empty/empty condition was presented in baseline blocks.     

From the Cover: Extra-pair paternity explains cooperation in a bird species

In many social animals, females mate with multiple males, but the adaptive value of female extra-pair mating is not fully understood. Here, we tested whether male pied flycatchers (Ficedula hypoleuca) engaging in extra-pair copulations with neighboring females were more likely to assist their neighbors in antipredator defense. We found that extra-pair sires joined predator-mobbing more often, approached predators more closely, and attacked predators more aggressively than males without extra-pair offspring in the neighboring nest. Extra-pair mating may incentivize males to assist in nest defense because of the benefits that this cooperative behavior has on their total offspring production. For females, this mating strategy may help recruit more males to join in antipredator defense, offering better protection and ultimately improving reproductive success. Our results suggest a simple mechanism by which extra-pair mating can improve reproductive success in breeding birds. In summary, males siring extra-pair offspring in neighboring nests assist neighbors in antipredator defense more often than males without extra-pair offspring.

Prey react to predators in different ways: by moving away, staying motionless waiting for the predator to leave, or summoning others to cooperatively attack or harass the predator (1, 2). Prey mob predators by emitting repeated, loud, and easily localizable calls and performing stereotyped movements that recruit more prey individuals to join the mobbing (3). Such behavioral patterns are considered adaptive antipredator strategies, and they occur in a variety of species (4, 5). Mobbing benefits prey by reducing hunting efficiency of the predator, either through distracting it or by driving it away (6, 7). At an individual level, mobbing also carries costs (8) as cooperative individuals spend time and energy and risk injury or death. Cooperative antipredator behaviors may hence be prone to freeloaders that benefit from collective defense but refrain from joining forces with others.Cooperation in mobbing may be understood as byproduct mutualism when mobbing predators at nests of close neighbors directly affects protection of own offspring (9). Cooperation among neighbors breeding further apart may be explained as direct reciprocity (10–12) in which only cooperating individuals are supported by their neighbors in a tit-for-tat–like strategy (4, 13–15). Predator harassment entails a risk of injury and death (14, 16), while driving predators away is the main function of mobbing, which significantly decreases future risk of predation (6, 17). Cooperative actions are often more efficient in larger groups (1). Larger aggregations of breeders may also increase opportunities for male and female neighbors to interact, with extra-pair mating being more prevalent in dense aggregations (18) and among close neighbors (19, 20).Extra-pair mating behaviors are widespread in nature, but the adaptive reasons of this reproductive strategy in females are far from being understood (18, 21). Extra-pair mating causes paternity uncertainty, which reduces the risk of infanticide in multimale groups (22, 23). Extra-pair mating may also shift male incentives from a sole focus on care at the nest to investing in activities that benefit close neighbors (18, 20). Since males potentially sire offspring in neighboring broods, they may benefit from providing antipredator protection and assist neighbors in mobbing activities. Field studies suggest a link between sex-related cooperative behavior, especially in the context of antipredator protection (7, 20, 24), clumped distribution of breeding individuals (25), and extra-pair mating (26–28).Several recent studies have linked predation risk to the occurrence of extra-pair paternity: higher frequencies of extra-pair offspring have been reported in populations of Japanese great tit (Parus minor) that were naturally exposed to stronger nest predation pressures (29). In blue tits (Cyanistes caeruleus), whole-brood mortality due to predation is negatively associated with levels of extra-pair paternity (20). Studies manipulating the level of perceived predation risk found that repeated playbacks of predator calls delayed dawn singing in songbird communities (30) but had no effect on extra-pair paternity in blue tits (31) or great tits (Parus major) (32). In contrast, blue tit females that were exposed to predator models during the period of peak fertility intensified their promiscuous behavior along with or as a consequence of the disruption of morning copulatory routines within the pair (33). In some cases, cooperative investment in increased safety of the whole neighborhood comes at the expense of paternity loss in own brood for some males, while concomitantly increasing the reproductive output of other males (34). However, the specific link between extra-pair paternity and investment in neighborhood defense has never been explicitly addressed.In this study, we tested whether the propensity of male pied flycatchers (Ficedula hypoleuca) to engage in antipredator defense at neighboring nests (9) is associated with the presence of extra-pair offspring in that nest. The pied flycatcher often breeds semicolonially, and to provide an ecologically valid breeding environment for the birds, we created experimental neighborhoods in the form of triplets of nest boxes in close proximity. Males in focal nests (A) were allowed to be near fertile females and thus potentially sire extra-pair offspring in neighboring nests (B and C) but not the other way around. Using stuffed predators at nests B and C, we monitored whether focal males (nest A) joined antipredator mobbing at these neighboring nests. Genotype-based paternity assignment enabled us to test whether participation in antipredator defense varied according to extra-pair paternity within neighborhoods.     

From the Cover: Democratic decisions establish stable authorities that overcome the paradox of second-order punishment

Individuals usually punish free riders but refuse to sanction those who cooperate but do not punish. This missing second-order peer punishment is a fundamental problem for the stabilization of cooperation. To solve this problem, most societies today have implemented central authorities that punish free riders and tax evaders alike, such that second-order punishment is fully established. The emergence of such stable authorities from individual decisions, however, creates a new paradox: it seems absurd to expect individuals who do not engage in second-order punishment to strive for an authority that does. Herein, we provide a mathematical model and experimental results from a public goods game where subjects can choose between a community with and without second-order punishment in two different ways. When subjects can migrate continuously to either community, we identify a bias toward institutions that do not punish tax evaders. When subjects have to vote once for all rounds of the game and have to accept the decision of the majority, they prefer a society with second-order punishment. These findings uncover the existence of a democracy premium. The majority-voting rule allows subjects to commit themselves and to implement institutions that eventually lead to a higher welfare for all.The success of collective action and the maintenance of commonly shared infrastructure is often endangered by free riders, subjects who reap the benefits of public goods without contributing to them (1, 2). To mitigate the free riders’ destructive potential, many communities install specialized authorities that monitor the subjects’ behavior and sanction wrong-doers (3–7). Examples, such as modern courts and the police system, indicate that the maintenance of such institutions is costly. They also constitute a commonly shared infrastructure, which can be exploited just as the original public good that the institution was designed for to protect. Thus, a second-order dilemma arises.Second-order dilemmas appear in various forms and are considered as a serious obstacle to the evolution of cooperation (8–10). For example, in the absence of a policing authority, group members may take the job onto themselves, punishing others directly. There is overwhelming evidence that subjects are willing to sanction free riders at a cost to themselves (11–14), although individuals typically refuse to exert second-order punishment (15). However, peer punishment can have detrimental consequences on welfare, as the punishment costs may override the benefits of increased cooperation (16) and due to the problems of antisocial punishment (17) and retaliation (18, 19). Peer punishment may pay in the long run, but only when interactions take place in small and stable groups (20). These restrictions may be the reason why modern states have abolished decentralized sanctioning (21).To explain the transition from decentralized peer punishment to institutional pool punishment (22), recent theoretical and experimental evidence highlights the critical role of second-order punishment (23–26). These studies indicate that such institutions can only persist when they additionally punish individuals who do not support the central authority. The presence of a powerful authority restricts the subjects’ strategic options and effectively forces them to cooperate. As this implies a considerable loss of individual freedom, it is unclear under which conditions subjects would voluntarily submit to such a Leviathan (27). There are different views on this problem: Hardin argued that “we accept compulsory taxes because we recognize that voluntary taxes would favor the conscienceless” (2). However, previous studies have also shown that maintaining costly institutions may result in lower average payoffs (23, 25). Under which conditions would subjects agree to implement a central authority that enforces its continued existence with second-order punishment?To investigate this question, we conducted an experimental public goods game. The experiment consisted of three independent blocks, each block having several rounds (Materials and Methods). During the first two blocks of the experiment, consisting of 10 rounds each, subjects first had to decide whether they want to participate in the game or abstain to secure a small payoff. Participants were then asked whether they want to pay taxes to a central authority and whether they want to cooperate by contributing money to a common pool. If at least one subject paid taxes, the central authority was established and either punished both noncontributors and tax evaders (institution with second-order punishment) or just noncontributors (institution without second-order punishment). If subjects failed to establish such an authority, the public goods game took the form of a conventional social dilemma (mutual cooperation was the optimal outcome for the group, in which case each individual’s best choice was to free ride).

Table 1.

Overview of the experimental design

From the Cover: Patterning droplets with durotaxis

Numerous cell types have shown a remarkable ability to detect and move along gradients in stiffness of an underlying substrate—a process known as durotaxis. The mechanisms underlying durotaxis are still unresolved, but generally believed to involve active sensing and locomotion. Here, we show that simple liquid droplets also undergo durotaxis. By modulating substrate stiffness, we obtain fine control of droplet position on soft, flat substrates. Unlike other control mechanisms, droplet durotaxis works without imposing chemical, thermal, electrical, or topographical gradients. We show that droplet durotaxis can be used to create large-scale droplet patterns and is potentially useful for many applications, such as microfluidics, thermal control, and microfabrication.     

From the Cover: Long-term social dynamics drive loss of function in pathogenic bacteria

Laboratory experiments show that social interactions between bacterial cells can drive evolutionary change at the population level, but significant challenges limit attempts to assess the relevance of these findings to natural populations, where selection pressures are unknown. We have increasingly sophisticated methods for monitoring phenotypic and genotypic dynamics in bacteria causing infectious disease, but in contrast, we lack evidence-based adaptive explanations for those changes. Evolutionary change during infection is often interpreted as host adaptation, but this assumption neglects to consider social dynamics shown to drive evolutionary change in vitro. We provide evidence to show that long-term behavioral dynamics observed in a pathogen are driven by selection to outcompete neighboring conspecific cells through social interactions. We find that Pseudomonas aeruginosa bacteria, causing lung infections in patients with cystic fibrosis, lose cooperative iron acquisition by siderophore production during infection. This loss could be caused by changes in iron availability in the lung, but surprisingly, we find that cells retain the ability to take up siderophores produced by conspecifics, even after they have lost the ability to synthesize siderophores. Only when cooperative producers are lost from the population is the receptor for uptake lost. This finding highlights the potential pitfalls of interpreting loss of function in pathogenic bacterial populations as evidence for trait redundancy in the host environment. More generally, we provide an example of how sequence analysis can be used to generate testable hypotheses about selection driving long-term phenotypic changes of pathogenic bacteria in situ.Some of the most important bacterial pathogens are opportunistic in the sense that they infect a compromised human host from the surrounding environment. In cases where such infections become persistent, the evolutionary changes accompanying the transition from the environment to the human body have been the subject of intensive research, and we now have some information on what distinguishes clinical from environmental isolates (1). Surprisingly, our understanding of how this process is driven by selection often remains speculative. To study bacterial cells, we must remove them from the host environment into the laboratory, which may release them from the selection pressures that we wish to understand.In parallel, progress has been made in understanding how bacterial populations respond to selection through in vitro experimental evolution. These studies show that phenotypic dynamics result not only in response to the environment but also, to social interactions as bacteria cooperate and compete with one another (2). Selection to outcompete neighbors can even lead to loss of traits that increase survival in the environment but are costly to produce (3–5). Such loss has been shown for a range of traits, such as extracellular enzymes, signaling molecules, and iron chelators (2). These exoproducts act as “public goods”: products that are beneficial to the group but vulnerable to exploitation by cheats that reap the benefit without paying the cost (6). Understanding selection on public goods is clinically relevant, because many are virulence factors (7, 8), and social interactions have also been shown experimentally to affect infection dynamics in vivo (9, 10).We investigate the importance of social interactions in infectious populations of Pseudomonas aeruginosa, which is both a model organism of social evolution research and the primary cause of chronic lung infection in patients with the genetic disorder cystic fibrosis (CF). CF patients usually acquire their first P. aeruginosa infection in childhood, and these infections can persist for years, despite antibiotic treatment (11). P. aeruginosa produces an iron-scavenging molecule, pyoverdine, that acts as a cooperative public good in vitro (12). Iron is essential for growth but bound to transferrin, heme, and hemoglobin in the human host (13). P. aeruginosa circumvents this by releasing pyoverdine, which binds to iron and is taken up by a specific receptor. Detection of pyoverdine and expression of pyoverdine genes in sputum samples confirm that the pathway is active, and likely beneficial, in the CF lung environment (14, 15). However, cells that are deficient in production (i.e., potential cheaters) have also repeatedly been isolated from patients (16, 17). The pyoverdine metabolism is, therefore, an ideal system for testing whether social dynamics observed in the laboratory also occur in human hosts.Our aim is to identify selection pressures driving any changes that we observe in pyoverdine production in the lung. Pyoverdine production may be an adaptive response to acquire a limited nutrient. It may be lost, therefore, in response to availability of other iron sources (18–20). Alternatively, production may be lost from the population even if iron is limiting as a result of cooperator–cheat dynamics. Crucially, patterns of evolution of the pyoverdine system differ depending on whether adaptation to the human lung or social interactions drive selection (Fig. 1). If pyoverdine does not provide a growth benefit in the lung, the entire system will be redundant, including receptor function. In contrast, if pyoverdine production is lost because of cheating, receptor function will remain beneficial as long as extrinsic pyoverdine is available. Only when cheating is not possible does the receptor also become redundant. We can, therefore, distinguish between the two selection pressures by determining if and when receptor function is maintained in bacteria that have lost the ability to produce pyoverdine.Open in a separate windowFig. 1.The pyoverdine system. (Upper) The pyoverdine receptor FpvA spans the cell wall. In the absence of bound pyoverdine, the anti-σ factor FpvR inhibits the expression of σ-factors FpvI and PvdS. Pyoverdine acquires iron from transferrin. When ferripyoverdine binds to the receptor, FpvR releases FpvI and PvdS. Release of FpvI initiates synthesis of the receptor FpvA, and PvdS initiates synthesis of pyoverdine (illustrated by arrows). (Lower Left) If pyoverdine production is lost as an adaptation to the lung, receptor function also becomes redundant, irrespective of whether pyoverdine produced by neighbors is available. (Lower Right) However, if pyoverdine production is lost because of cheating, we expect to see retention of receptor function in the presence of pyoverdine produced by others and function only lost in the absence of pyoverdine.Two Danish collections of genome-sequenced P. aeruginosa isolates provide the opportunity to study selection on pyoverdine metabolism in CF patients (Dataset S1). The first collection gives a detailed insight into changes occurring during the first 10 y of infection across 36 young CF patients with 54 different clone types (21), representing the transition from initial colonization to chronic infection. With frequent and extensive sampling from each patient (451 isolates; on average, 13 per patient), we can estimate the point of colonization of each clone type and thereby, the time period over which a given isolate has evolved. The second collection provides insight into the long-term dynamics of two clone types causing chronic infections, with samples from 24 adult patients (85 isolates) infected with the two Danish transmissible clone types DK1 and DK2 (22–24). The two transmissible clone types established and spread in the Danish CF patient group from 1973 and all of the older patients (who got chronically infected up to the beginning of the 1990s) harbor one or both of these. Afterward, segregation of patients in the clinic has largely eliminated transmission of these clone types. The DK1 and DK2 isolates, thus, typically come from now older CF patients who have each been sampled a few times, providing insight into the long-term dynamics but not on a fine scale at the early infection stage. For some of the analyses, as specified below, only the isolates from the young patients have been used.     

From the Cover: Efficient computation of optimal actions

Optimal choice of actions is a fundamental problem relevant to fields as diverse as neuroscience, psychology, economics, computer science, and control engineering. Despite this broad relevance the abstract setting is similar: we have an agent choosing actions over time, an uncertain dynamical system whose state is affected by those actions, and a performance criterion that the agent seeks to optimize. Solving problems of this kind remains hard, in part, because of overly generic formulations. Here, we propose a more structured formulation that greatly simplifies the construction of optimal control laws in both discrete and continuous domains. An exhaustive search over actions is avoided and the problem becomes linear. This yields algorithms that outperform Dynamic Programming and Reinforcement Learning, and thereby solve traditional problems more efficiently. Our framework also enables computations that were not possible before: composing optimal control laws by mixing primitives, applying deterministic methods to stochastic systems, quantifying the benefits of error tolerance, and inferring goals from behavioral data via convex optimization. Development of a general class of easily solvable problems tends to accelerate progress—as linear systems theory has done, for example. Our framework may have similar impact in fields where optimal choice of actions is relevant.     

From the Cover: The absence of reward induces inequity aversion in dogs

One crucial element for the evolution of cooperation may be the sensitivity to others'' efforts and payoffs compared with one''s own costs and gains. Inequity aversion is thought to be the driving force behind unselfish motivated punishment in humans constituting a powerful device for the enforcement of cooperation. Recent research indicates that non-human primates refuse to participate in cooperative problem-solving tasks if they witness a conspecific obtaining a more attractive reward for the same effort. However, little is known about non-primate species, although inequity aversion may also be expected in other cooperative species. Here, we investigated whether domestic dogs show sensitivity toward the inequity of rewards received for giving the paw to an experimenter on command in pairs of dogs. We found differences in dogs tested without food reward in the presence of a rewarded partner compared with both a baseline condition (both partners rewarded) and an asocial control situation (no reward, no partner), indicating that the presence of a rewarded partner matters. Furthermore, we showed that it was not the presence of the second dog but the fact that the partner received the food that was responsible for the change in the subjects'' behavior. In contrast to primate studies, dogs did not react to differences in the quality of food or effort. Our results suggest that species other than primates show at least a primitive version of inequity aversion, which may be a precursor of a more sophisticated sensitivity to efforts and payoffs of joint interactions.     

From the Cover: Development of socio-emotional competence in bonobos

Social and emotional skills are tightly interlinked in human development, and both are negatively impacted by disrupted social development. The same interplay between social and emotional skills, including expressions of empathy, has received scant attention in other primates however, despite the growing interest in caring, friendships, and the fitness benefits of social skills. Here we examine the development of socio-emotional competence in juvenile bonobos (Pan paniscus) at a sanctuary in the Democratic Republic of the Congo, focusing on the interplay between various skills, including empathy-related responding. Most subjects were rehabilitated orphans, but some were born at the sanctuary and mother-reared there. We observed how juveniles with different rearing backgrounds responded to stressful events, both when the stress affected themselves (e.g., a lost fight) or others (e.g., witnessing the distress of others). The main dependent variable was the consolation of distressed parties by means of calming body contact. As in children, consolation was predicted by overall social competence and effective emotion regulation, as reflected in the speed of recovery from self-distress and behavioral measures of anxiety. Juveniles more effective at self-regulation were more likely to console others in distress, and such behavior was more typical of mother-reared juveniles than orphans. These results highlight the interplay between the development of social and emotional skills in our ape relatives and the importance of the mother–offspring bond in shaping socio-emotional competence.Socio-emotional competence encompasses an array of skills, such as successfully forming and maintaining social relationships, behaving appropriately in social situations, being sensitive to the emotions of others, and effectively managing one’s own emotions (1). Emotion regulation (ER) is an essential part of socio-emotional competence and is defined as the process of modifying, inhibiting, evaluating, and monitoring internal states and reactions to enable an individual to adaptively respond to arousing situations so as to achieve individual goals (1, 2). Throughout development, social and emotional skills are tightly interconnected and “people who are unable to modulate the intensity and duration of their internal emotional responses and emotionally driven behavior are likely to be physiologically over-aroused and to behave in ways that do not foster constructive social interactions” (3).Studies of child development show that effectively managing one’s own emotions allows for greater empathy with others, including caring responses known as sympathetic concern (4–6). Sympathetic concern interacts with other social skills that emerge across development, including perspective-taking (5–9). It is reliably predicted by ER, with low-regulating individuals more likely to become emotionally overwhelmed when exposed to another’s distress, resulting in a more self-centered personal distress (6, 8, 9). This connection develops at an early age: infants with signs of better ER show less personal distress in response to peer cries than those with poorer ER (10). Overall, socially competent behavior, which includes expressions of sympathy and prosocial behavior, as well as socially appropriate responses and popularity, reliably relates to better ER in children and adults (1–3, 7–11).This socio-emotional framework is rarely applied to other species, however. This is curious, because if it is critically important for humans one would expect it to also apply to some degree to our closest relatives, the anthropoid apes. To explore this issue, we measured purported markers of socio-emotional competence in young bonobos along with consolation behavior, which previous research has suggested to be a marker of sympathetic concern (12–14). Consolation is defined as spontaneous contact comfort aimed at distressed parties by means of touching, stroking, embracing, and kissing (15) (Fig. 1), a behavior well-known of both children and apes (4–6, 12–16). In human children, consolation behavior appears already in the first year of life (10, 17), suggesting that although the cognitive component of empathy increases across development, it is no prerequisite for expressions of concern. ER seems to be critical: infants without effective ER do not orient to others because they cannot overcome their own personal distress in the face of another’s distress (10, 18).Open in a separate windowFig. 1.One juvenile bonobo embraces a distressed companion during postconflict consolation. Photograph by Zanna Clay at the Lola ya Bonobo Sanctuary in the Democratic Republic of the Congo.Whereas few animal studies have explicitly addressed ER, experimental research has revealed relevant similarities. For example, primates and other animals show human-like skin conductance and heart rate responses to emotionally arousing or calming stimuli (19–23). Chimpanzees (Pan troglodytes) spontaneously match images of positive vs. negative facial expressions to videos depicting pleasant vs. aversive situations, suggesting awareness of the emotional connotations of their species’ facial displays (19). Studies addressing emotional control typically adopt a deferred gratification paradigm. Apes, and to a lesser extent monkeys and nonprimates (24–26), are able to control the urge to reach for a reward if holding back increases the chance of a better reward later on. Moreover, like children, apes seek to distract themselves in an apparent attempt to control the temptation of immediate gratification (26). Such research suggests the importance of ER for ape behavior.An area with significant overlap in human and nonhuman developmental research is that of social deprivation. Socially deprived children demonstrate poor emotional and social competence, including lower sympathetic concern, increased risk for psychiatric disorders, and enlarged amygdala volumes, indicative of high anxiety (27–30). Although adoptive care can mitigate these negative effects, orphaned children typically show lasting socio-emotional disruptions (30). Similar effects of early deprivation have been documented in chimpanzees, rhesus monkeys (Macaca mulatta), and other primates, including increased anxiety, an inability to develop social relationships, lack of recognition of social signals, and stereotypical behaviors (31–36). A study of socially deprived monkeys found a deficiency in species-typical reconciliation with opponents after conflict, which is an essential social skill (34, 36). Although some negative effects of social deprivation can be overcome, this mostly applies to deprivation later in development, such as after weaning, or after having received substitutive maternal care (37, 38).Bonobos at a forested African sanctuary offered an opportunity to measure many of these variables in both mother-raised and orphaned juveniles, thus allowing a test of predictions derived from the above studies. Most study subjects were wild-caught orphans rescued from the illegal bush-meat and pet trades and subsequently rehabilitated with the help of human mother substitutes. The bonobo is a species of particular interest given its close genetic similarity to our own (39) and its reputation of social tolerance, peacefulness, and reduced levels of violence compared with its congener, the chimpanzee (40). Bonobos also seem to have high empathy levels (41) and are equipped with the neural substrate to support these tendencies (42). Consistent with empathy-based predictions (43), our previous study found consolation to be typical of closely bonded individuals, both kin and nonkin. Both reconciliation between former opponents and consolation of distressed parties occurred across all age classes, highlighting successful social rehabilitation within the sanctuary environment. Nevertheless, mother-reared juveniles were significantly more likely to offer consolation to others than orphans of any age (44).A year after our first study, we observed the same bonobo juveniles in greater detail to investigate the interplay between socio-emotional competence at baseline while experiencing self-distress (i.e., as a victim of a fight), and in response to the distress of others (i.e., as a bystander to conflict). Our main dependent variable was spontaneously offered consolation after naturally occurring aggressive and/or stressful episodes. We predicted that juvenile bonobos scoring higher on measures of overall sociality and socio-emotional competence, including ER, would be more likely to console distressed parties. We evaluated these effects using a generalized linear mixed model (GLMM), which helps determine independent contributions, controlled for age, sex, and other factors.     

From the Cover: Influence of paced maternal breathing on fetal–maternal heart rate coordination

Pregnant mothers often report a special awareness of and bonding with their unborn child. Little is known about this relationship although it may offer potential for the assessment of the fetal condition. Recently we found evidence of short epochs of fetal–maternal heart rate synchronization under uncontrolled conditions with spontaneous maternal breathing. Here, we examine whether the occurrence of such epochs can be influenced by maternal respiratory arrhythmia induced by paced breathing at several different rates (10, 12, 15, and 20 cycles per minute). To test for such weak and nonstationary synchronizations among the fetal–maternal subsystems, we apply a multivariate synchronization analysis technique and test statistics based on twin surrogates. We find a clear increase in synchronization epochs mostly at high maternal respiratory rates in the original but not in the surrogate data. On the other hand, fewer epochs are found at low respiratory rates both in original and surrogate data. The results suggest that the fetal cardiac system seems to possess the capability to adjust its rate of activation in response to external—i.e., maternal—stimulation. Hence, the pregnant mothers'' special awareness to the unborn child may also be reflected by fetal–maternal interaction of cardiac activity. Our approach opens up the chance to examine this interaction between independent but closely linked physiological systems.     

From the Cover: Evidence suggesting that desire-state attribution may govern food sharing in Eurasian jays

State-attribution is the ability to ascribe to others an internal life like one’s own and to understand that internal, psychological states such as desire, hope, belief, and knowledge underlie others’ actions. Despite extensive research, comparative studies struggle to adequately integrate key factors of state-attribution that have been identified by evolutionary and developmental psychology as well as research on empathy. Here, we develop a behavioral paradigm to address these issues and investigate whether male Eurasian jays respond to the changing desire-state of their female partners when sharing food. We demonstrate that males feed their mates flexibly according to the female’s current food preference. Critically, we show that the males need to see what the female has previously eaten to know what food she will currently want. Consequently, the males’ sharing pattern was not simply a response to their mate’s behavior indicating her preference as to what he should share, nor was it a response to the males’ own desire-state. Our results raise the possibility that these birds may be capable of ascribing desire to their mates.     

From the Cover: Habitual control of goal selection in humans

Humans choose actions based on both habit and planning. Habitual control is computationally frugal but adapts slowly to novel circumstances, whereas planning is computationally expensive but can adapt swiftly. Current research emphasizes the competition between habits and plans for behavioral control, yet many complex tasks instead favor their integration. We consider a hierarchical architecture that exploits the computational efficiency of habitual control to select goals while preserving the flexibility of planning to achieve those goals. We formalize this mechanism in a reinforcement learning setting, illustrate its costs and benefits, and experimentally demonstrate its spontaneous application in a sequential decision-making task.The distinction between habitual and planned action is fundamental to behavioral research (1–4). Habits enable computationally efficient decision making, but at the cost of behavioral flexibility. They form as stimulus–response pairings are “stamped in” following reward, as in Thorndike’s law of effect (3). Planning, in contrast, enables more flexible and productive decision making. It is accomplished by first searching over a causal model linking candidate actions to their expected outcomes and then selecting actions based on their anticipated rewards. Planning imposes a severe computational cost, however, as the size and complexity of a model grows.Past research emphasizes the competition between habitual and planned control of behavior (5, 6). Habitual control is favored when an individual has extensive experience with a task and when the optimal behavior policy is relatively consistent across time; meanwhile, planning is favored for novel tasks and when the optimal policy is variable, provided that an agent represents an adequate model of their task (7).Methods of integrating habitual and planned control have received less attention (8–10), yet real-world tasks often favor elements of each. Consider, for instance, a seasoned journalist who reports on new events each day. At a high level of abstraction, her reporting is structured around a repetitive series of goal-directed actions: follow leads, interview sources, evade meddling editors, etc. Because these actions are reliably valuable for any news event, their selection is an excellent candidate for habitual control. The concrete steps necessary to carry out any individual action will be highly variable, however—optimal behavior when interviewing a pop star may be suboptimal when interviewing the Pope. Thus, the implementation of the abstract actions is an excellent candidate for planning. This example illustrates the utility of nesting elements of both habits and plans in a hierarchy of behavioral control (11–13).Indeed, it is widely recognized that humans mentally organize their behavior around hierarchically organized goals and subgoals (3, 14, 15). In principle, hierarchical organization can be implemented exclusively by habitual control (16), or exclusively by planning (13, 17). However, these homogenous mechanisms foreclose the possibility of tailoring the means of control (habit vs. planning) to the affordances of a particular level of behavioral abstraction. Our aim is to show that humans solve this dilemma by exerting habitual control over the process of goal selection, while using planning to attain the goal once selected.Traditionally, habits are modeled as a learned association between a perceptual stimulus and motor response. Our proposal entails an extension of habit learning to the relation between superordinate and subordinate goals: a superordinate goal can serve as the internally represented stimulus triggering a cognitive response of subordinate goal selection. Thus, for instance, the goal of getting an interview with a key source might be stamped in due to the history of reward associated with selecting this goal in past news-reporting episodes.Colloquially, this captures the idea of a “habit of thought”: habitual control can contribute to the effective deployment of cognitive routines that facilitate productive and flexible cognition. This proposal is consonant with recent research emphasizing the pervasive role of model-free control in related elements of higher-level cognition (18, 19), including the gating of working memory (20) and the construction of hierarchical task representations (21). These models offer an appealing functional explanation for the neuronal connections between striatum and frontal cortex (22).     

From the Cover: Enlisting wild grass genes to combat nitrification in wheat farming: A nature-based solution

Active nitrifiers and rapid nitrification are major contributing factors to nitrogen losses in global wheat production. Suppressing nitrifier activity is an effective strategy to limit N losses from agriculture. Production and release of nitrification inhibitors from plant roots is termed “biological nitrification inhibition” (BNI). Here, we report the discovery of a chromosome region that controls BNI production in “wheat grass” Leymus racemosus (Lam.) Tzvelev, located on the short arm of the “Lr#3Ns^b” (Lr#n), which can be transferred to wheat as T3BL.3Ns^bS (denoted Lr#n-SA), where 3BS arm of chromosome 3B of wheat was replaced by 3Ns^bS of L. racemosus. We successfully introduced T3BL.3Ns^bS into the wheat cultivar “Chinese Spring” (CS-Lr#n-SA, referred to as “BNI-CS”), which resulted in the doubling of its BNI capacity. T3BL.3Ns^bS from BNI-CS was then transferred to several elite high-yielding hexaploid wheat cultivars, leading to near doubling of BNI production in “BNI-MUNAL” and “BNI-ROELFS.” Laboratory incubation studies with root-zone soil from field-grown BNI-MUNAL confirmed BNI trait expression, evident from suppression of soil nitrifier activity, reduced nitrification potential, and N₂O emissions. Changes in N metabolism included reductions in both leaf nitrate, nitrate reductase activity, and enhanced glutamine synthetase activity, indicating a shift toward ammonium nutrition. Nitrogen uptake from soil organic matter mineralization improved under low N conditions. Biomass production, grain yields, and N uptake were significantly higher in BNI-MUNAL across N treatments. Grain protein levels and breadmaking attributes were not negatively impacted. Wide use of BNI functions in wheat breeding may combat nitrification in high N input–intensive farming but also can improve adaptation to low N input marginal areas.

Nitrification and denitrification are critical soil biological processes, which, left unchecked, can accelerate generation of harmful reactive nitrogen (N) forms (NO₃ ⁻, N₂O, and NOx) that trigger a “nitrogen cascade,” damaging ecosystems, water systems, and soil fertility (1 –8). Excessive nitrifier activity and a rapid generation of soil nitrates plague modern cereal production systems. This has led to shifting crop N nutrition toward an “all nitrate form,” which is largely responsible for N losses and a decline in agronomic nitrogen-use efficiency (NUE) (6, 7, 9 –11).Wheat, one of the three founding crops for food security (12), consumes nearly a fifth of factory-produced N fertilizers, and it has an average NUE of 33%, which has remained unchanged for the last two decades (13 –15). Regulating soil nitrifier activity to slow the rate of soil nitrate formation should provide more balanced N forms (NH₄ ⁺ and NO₃ ⁻) for plant uptake (rather than nearly “all NO₃ ⁻” at present), reduce N losses, and facilitate the assimilation of dual N forms. This optimizes the utilization of biochemical machinery for N assimilation, improving stability and possibly enhancing yield potential (16). In addition, the assimilation of NH₄ ⁺ is energetically more efficient (requiring 40% less metabolic energy) than NO₃ ⁻ assimilation (16). Often, a stimulatory growth response is observed in wheat, when 15 to 30% of NO₃ ⁻ is replaced with NH₄ ⁺ in nutrient solutions (17, 18).Synthetic nitrification inhibitors (SNIs) have been shown to suppress N₂O emissions, reduce N losses, and improve agronomic NUE in several cereal crops including wheat (6, 19 –21). However, the lack of cost effectiveness, inconsistency in field performance, inability to function in tropical environments, and the concerns related to the entering of SNIs into food chains have limited their adoption in production agriculture (6, 7, 19, 20).Biological nitrification inhibition (BNI) is a plant function whereby nitrification inhibitors (BNIs) are produced from root systems to suppress soil nitrifier activity (22 –26). Earlier, we reported that the BNI capacity in the root systems of cultivated wheat lack adequate strength to effectively suppress soil nitrifier activity in the rhizosphere (24, 25). Leymus racemosus (hereafter referred to as “wild grass”), a perennial Triticeae evolutionarily related to wheat, produces extensive root systems ( SI Appendix, Fig. S1) and was discovered to have a high BNI capacity several times higher than cultivated wheat. It was also effective in suppressing soil nitrifier activity and in reducing soi -nitrate formation ( SI Appendix, Fig. S2) (25). Subsequently, the chromosome Lr#n = 3Ns^b was found to be controlling a major part of BNI capacity in wild grass, and it is the focus of our current research (25, 27, 28). Earlier, we reported that Lr#I and Lr#J had a minor impact on BNI capacity, but they are not the focus of this research (25).We transferred the Lr#n chromosome (Lr#n-SA = T3BL.3Ns^bS) controlling BNI capacity (hereafter referred to as BNI trait) into the cultivated wheat, Chinese Spring (CS). The results of the transfer of this BNI trait into several elite wheat types with a grain-yield (GY) potential >10 t ha⁻¹, resulting in substantial improvements of BNI capacity in root systems, are reported in this paper.     

From the Cover: Feature Article: Adaptation to a new environment allows cooperators to purge cheaters stochastically

Cooperation via production of common goods is found in diverse life forms ranging from viruses to social animals. However, natural selection predicts a “tragedy of the commons”: Cheaters, benefiting from without producing costly common goods, are more fit than cooperators and should destroy cooperation. In an attempt to discover novel mechanisms of cheater control, we eliminated known ones using a yeast cooperator–cheater system engineered to supply or exploit essential nutrients. Surprisingly, although less fit than cheaters, cooperators quickly dominated a fraction of cocultures. Cooperators isolated from these cocultures were superior to the cheater isolates they had been cocultured with, even though these cheaters were superior to ancestral cooperators. Resequencing and phenotypic analyses revealed that evolved cooperators and cheaters all harbored mutations adaptive to the nutrient-limited cooperative environment, allowing growth at a much lower concentration of nutrient than their ancestors. Even after the initial round of adaptation, evolved cooperators still stochastically dominated cheaters derived from them. We propose the “adaptive race” model: If during adaptation to an environment, the fitness gain of cooperators exceeds that of cheaters by at least the fitness cost of cooperation, the tragedy of the commons can be averted. Although cooperators and cheaters sample from the same pool of adaptive mutations, this symmetry is soon broken: The best cooperators purge cheaters and continue to grow, whereas the best cheaters cause rapid self-extinction. We speculate that adaptation to changing environments may contribute to the persistence of cooperative systems before the appearance of more sophisticated mechanisms of cheater control.