Genetic composition of social groups influences male aggressive behaviour and fitness in natural genotypes of Drosophila melanogaster

Indirect genetic effects (IGEs) describe how an individual''s behaviour—which is influenced by his or her genotype—can affect the behaviours of interacting individuals. IGE research has focused on dyads. However, insights from social networks research, and other studies of group behaviour, suggest that dyadic interactions are affected by the behaviour of other individuals in the group. To extend IGE inferences to groups of three or more, IGEs must be considered from a group perspective. Here, I introduce the ‘focal interaction’ approach to study IGEs in groups. I illustrate the utility of this approach by studying aggression among natural genotypes of Drosophila melanogaster. I chose two natural genotypes as ‘focal interactants’: the behavioural interaction between them was the ‘focal interaction’. One male from each focal interactant genotype was present in every group, and I varied the genotype of the third male—the ‘treatment male’. Genetic variation in the treatment male''s aggressive behaviour influenced the focal interaction, demonstrating that IGEs in groups are not a straightforward extension of IGEs measured in dyads. Further, the focal interaction influenced male mating success, illustrating the role of IGEs in behavioural evolution. These results represent the first manipulative evidence for IGEs at the group level.     

The excuse principle can maintain cooperation through forgivable defection in the Prisoner's Dilemma game

Reciprocal altruism describes a situation in which an organism acts in a manner that temporarily reduces its fitness while increasing another organism''s fitness, but there is an ultimate fitness benefit based on an expectation that the other organism will act in a similar manner at a later time. It creates the obvious dilemma in which there is always a short-term benefit to cheating, therefore cooperating individuals must avoid being exploited by non-cooperating cheaters. This is achieved by following various decision rules, usually variants of the tit-for-tat (TFT) strategy. The strength of TFT, however, is also its weakness—mistakes in implementation or interpretation of moves, or the inability to cooperate, lead to a permanent breakdown in cooperation. We show that pied flycatchers (Ficedula hypoleuca) use a TFT with an embedded ‘excuse principle’ to forgive the neighbours that were perceived as unable to cooperate during mobbing of predators. The excuse principle dramatically increases the stability of TFT-like behavioural strategies within the Prisoner''s Dilemma game.     

Nutritional biology: a neglected basic discipline of nutritional science

On the basis of a scientific-philosophical analysis, this paper tries to show that the approaches in current nutritional science—including its subdisciplines which focus on molecular aspects—are predominantly application-oriented. This becomes particularly evident through a number of conceptual problems characterized by the triad of ‘dearth of theoretical foundation,’ ‘particularist research questions,’ and ‘reductionist understanding of nutrition.’ The thesis presented here is that an interpretive framework based on nutritional biology is able to shed constructive light on the fundamental problems of nutritional science. In this context, the establishment of ‘nutritional biology’ as a basic discipline in research and education would be a first step toward recognizing the phenomenon of ‘nutrition’ as an oecic process as a special case of an organism–environment interaction. Modern nutritional science should be substantively grounded on ecological—and therefore systems biology as well as organismic—principles. The aim of nutritional biology, then, should be to develop near-universal ‘law statements’ in nutritional science—a task which presents a major challenge for the current science system.     

Odour boosts visual object approach in flies

Multisensory integration is synergistic—input from one sensory modality might modulate the behavioural response to another. Work in flies has shown that a small visual object presented in the periphery elicits innate aversive steering responses in flight, likely representing an approaching threat. Object aversion is switched to approach when paired with a plume of food odour. The ‘open-loop’ design of prior work facilitated the observation of changing valence. How does odour influence visual object responses when an animal has naturally active control over its visual experience? In this study, we use closed-loop feedback conditions, in which a fly''s steering effort is coupled to the angular velocity of the visual stimulus, to confirm that flies steer toward or ‘fixate’ a long vertical stripe on the visual midline. They tend either to steer away from or ‘antifixate’ a small object or to disengage active visual control, which manifests as uncontrolled object ‘spinning’ within this experimental paradigm. Adding a plume of apple cider vinegar decreases the probability of both antifixation and spinning, while increasing the probability of frontal fixation for objects of any size, including a normally typically aversive small object.     

Unconscious mental imagery

Historically, mental imagery has been defined as an experiential state—as something necessarily conscious. But most behavioural or neuroimaging experiments on mental imagery—including the most famous ones—do not actually take the conscious experience of the subject into consideration. Further, recent research highlights that there are very few behavioural or neural differences between conscious and unconscious mental imagery. I argue that treating mental imagery as not necessarily conscious (as potentially unconscious) would bring much needed explanatory unification to mental imagery research. It would also help us to reassess some of the recent aphantasia findings inasmuch as at least some subjects with aphantasia would be best described as having unconscious mental imagery.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

The evolution of matrilineal kinship organization

Matrilineal kinship organization is a human social system that emphasizes interactions between matrilineal kin, i.e. individuals related only through females. The ‘matrilineal puzzle’ refers to the potential for tension characteristic of this social system, owing to the conflict between the interests and responsibilities of men in their roles as brother/uncle versus husband/father. From an evolutionary perspective, matrilineal kinship organization is puzzling when it diverts investment of resources from the individuals who provide the potentially highest reproductive returns. I use a game-theoretic framework to investigate a particular form of matrilineal inheritance—the transfer of property from a maternal uncle to a sororal nephew. The analysis reveals two mechanisms that may make this strategy a stable evolutionary outcome. First, a polygynous male has multiple wives, and hence multiple brothers-in-law; with matrilineal inheritance, each additional brother-in-law may transfer resources to the male''s wife''s offspring, thus potentially contributing to the male''s inclusive fitness. Second, the husband of a polyandrous female is effectively ‘sharing’ paternity with other men; depending on the number of husbands, he may be better off investing in his sister''s offspring. I conclude by discussing how these results address the challenges posed by the occurrence of matrilineal kinship organization.     

Biological trade and markets

Cooperation between organisms can often be understood, like trade between merchants, as a mutually beneficial exchange of services, resources or other ‘commodities’. Mutual benefits alone, however, are not sufficient to explain the evolution of trade-based cooperation. First, organisms may reject a particular trade if another partner offers a better deal. Second, while human trade often entails binding contracts, non-human trade requires unwritten ‘terms of contract’ that ‘self-stabilize’ trade and prevent cheating even if all traders strive to maximize fitness. Whenever trading partners can be chosen, market-like situations arise in nature that biologists studying cooperation need to account for. The mere possibility of exerting partner choice stabilizes many forms of otherwise cheatable trade, induces competition, facilitates the evolution of specialization and often leads to intricate forms of cooperation. We discuss selected examples to illustrate these general points and review basic conceptual approaches that are important in the theory of biological trade and markets. Comparing these approaches with theory in economics, it turns out that conventional models—often called ‘Walrasian’ markets—are of limited relevance to biology. In contrast, early approaches to trade and markets, as found in the works of Ricardo and Cournot, contain elements of thought that have inspired useful models in biology. For example, the concept of comparative advantage has biological applications in trade, signalling and ecological competition. We also see convergence between post-Walrasian economics and biological markets. For example, both economists and biologists are studying ‘principal–agent’ problems with principals offering jobs to agents without being sure that the agents will do a proper job. Finally, we show that mating markets have many peculiarities not shared with conventional economic markets. Ideas from economics are useful for biologists studying cooperation but need to be taken with caution.     

Virtual bargaining: a theory of social decision-making

An essential element of goal-directed decision-making in social contexts is that agents'' actions may be mutually interdependent. However, the most well-developed approaches to such strategic interactions, based on the Nash equilibrium concept in game theory, are sometimes too broad and at other times ‘overlook’ good solutions to fundamental social dilemmas and coordination problems. The authors propose a new theory of social decision-making—virtual bargaining—in which individuals decide among a set of moves on the basis of what they would agree to do if they could openly bargain. The core principles of a formal account are outlined (vis-à-vis the notions of ‘feasible agreement’ and explicit negotiation) and further illustrated with the introduction of a new game, dubbed the ‘Boobytrap game’ (a modification on the canonical Prisoner''s Dilemma paradigm). In the first empirical data of how individuals play the Boobytrap game, participants'' experimental choices accord well with a virtual bargaining perspective, but do not match predictions from a standard Nash account. Alternative frameworks are discussed, with specific empirical tests between these and virtual bargaining identified as future research directions. Lastly, it is proposed that virtual bargaining underpins a vast range of human activities, from social decision-making to joint action and communication.     

Post-hatch heat warms adult beaks: irreversible physiological plasticity in Japanese quail

Across taxa, the early rearing environment contributes to adult morphological and physiological variation. For example, in birds, environmental temperature plays a key role in shaping bill size and clinal trends across latitudinal/thermal gradients. Such patterns support the role of the bill as a thermal window and in thermal balance. It remains unknown whether bill size and thermal function are reversibly plastic. We raised Japanese quail in warm (30°C) or cold (15°C) environments and then at a common intermediate temperature. We predicted that birds raised in cold temperatures would develop smaller bills than warm-reared individuals, and that regulation of blood flow to the bill in response to changing temperatures would parallel the bill''s role in thermal balance. Cold-reared birds developed shorter bills, although bill size exhibited ‘catch-up’ growth once adults were placed at a common temperature. Despite having lived in a common thermal environment as adults, individuals that were initially reared in the warmth had higher bill surface temperatures than cold-reared individuals, particularly under cold conditions. This suggests that blood vessel density and/or the control over blood flow in the bill retained a memory of early thermal ontogeny. We conclude that post-hatch temperature reversibly affects adult bill morphology but irreversibly influences the thermal physiological role of bills and may play an underappreciated role in avian energetics.     

Stochastic evolutionary dynamics of direct reciprocity

Evolutionary game theory is the study of frequency-dependent selection. The success of an individual depends on the frequencies of strategies that are used in the population. We propose a new model for studying evolutionary dynamics in games with a continuous strategy space. The population size is finite. All members of the population use the same strategy. A mutant strategy is chosen from some distribution over the strategy space. The fixation probability of the mutant strategy in the resident population is calculated. The new mutant takes over the population with this probability. In this case, the mutant becomes the new resident. Otherwise, the existing resident remains. Then, another mutant is generated. These dynamics lead to a stationary distribution over the entire strategy space. Our new approach generalizes classical adaptive dynamics in three ways: (i) the population size is finite; (ii) mutants can be drawn non-locally and (iii) the dynamics are stochastic. We explore reactive strategies in the repeated Prisoner''s Dilemma. We perform ‘knock-out experiments’ to study how various strategies affect the evolution of cooperation. We find that ‘tit-for-tat’ is a weak catalyst for the emergence of cooperation, while ‘always cooperate’ is a strong catalyst for the emergence of defection. Our analysis leads to a new understanding of the optimal level of forgiveness that is needed for the evolution of cooperation under direct reciprocity.     

The multiple facets of Peto's paradox: a life-history model for the evolution of cancer suppression

Large animals should have higher lifetime probabilities of cancer than small animals because each cell division carries an attendant risk of mutating towards a tumour lineage. However, this is not observed—a (Peto''s) paradox that suggests large and/or long-lived species have evolved effective cancer suppression mechanisms. Using the Euler–Lotka population model, we demonstrate the evolutionary value of cancer suppression as determined by the ‘cost’ (decreased fecundity) of suppression verses the ‘cost’ of cancer (reduced survivorship). Body size per se will not select for sufficient cancer suppression to explain the paradox. Rather, cancer suppression should be most extreme when the probability of non-cancer death decreases with age (e.g. alligators), maturation is delayed, fecundity rates are low and fecundity increases with age. Thus, the value of cancer suppression is predicted to be lowest in the vole (short lifespan, high fecundity) and highest in the naked mole rat (long lived with late female sexual maturity). The life history of pre-industrial humans likely selected for quite low levels of cancer suppression. In modern humans that live much longer, this level results in unusually high lifetime cancer risks. The model predicts a lifetime risk of 49% compared with the current empirical value of 43%.     

The evolution of sex-specific grandparental harm

Recent empirical studies indicate that grandparents favour some categories of grandchildren over others. Here, we expand the previous theoretical foundation for this finding and show that grandchild-harming phenotypes are predicted to evolve by ‘sexually antagonistic zygotic drive (SA-zygotic drive) of the sex chromosomes’. We use the logic of Hamilton''s rule to develop a new ‘no-cost-to-self nepotism rule’ that greatly simplifies the determination of the invasion criteria for mutations that cause grandparents to harm grandchildren. We use this theory to generate predictions that distinguish SA-zygotic drive from theory based solely on paternity assurance. The major diagnostic prediction is that grandmothers, and to a lesser degree grandfathers, will evolve grandson-harming phenotypes that reduce the level of sib competition experienced by their more closely related granddaughters, especially in their sons'' families. This prediction is supported by data from recent studies showing (i) grandmothers invest more in granddaughters than grandsons, and counterintuitively, (ii) paternal grandmothers reduce the survival of their grandsons. We conclude that SA-zygotic drive is plausibly operating in humans via sexually antagonistic grandparental care.     

Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes

The compositions of bacterial genomes can be changed rapidly and dramatically through a variety of processes including horizontal gene transfer. This form of change is key to bacterial evolution, as it leads to ‘evolution in quantum leaps’. Horizontal gene transfer entails the incorporation of genetic elements transferred from another organism—perhaps in an earlier generation—directly into the genome, where they form ‘genomic islands’, i.e. blocks of DNA with signatures of mobile genetic elements. Genomic islands whose functions increase bacterial fitness, either directly or indirectly, have most likely been positively selected and can be termed ‘fitness islands’. Fitness islands can be divided into several subtypes: ‘ecological islands’ in environmental bacteria and ‘saprophytic islands’, ‘symbiosis islands’ or ‘pathogenicity islands’ (PAIs) in microorganisms that interact with living hosts. Here we discuss ways in which PAIs contribute to the pathogenic potency of bacteria, and the idea that genetic entities similar to genomic islands may also be present in the genomes of eukaryotes.     

Occam's Razor in sensorimotor learning

A large number of recent studies suggest that the sensorimotor system uses probabilistic models to predict its environment and makes inferences about unobserved variables in line with Bayesian statistics. One of the important features of Bayesian statistics is Occam''s Razor—an inbuilt preference for simpler models when comparing competing models that explain some observed data equally well. Here, we test directly for Occam''s Razor in sensorimotor control. We designed a sensorimotor task in which participants had to draw lines through clouds of noisy samples of an unobserved curve generated by one of two possible probabilistic models—a simple model with a large length scale, leading to smooth curves, and a complex model with a short length scale, leading to more wiggly curves. In training trials, participants were informed about the model that generated the stimulus so that they could learn the statistics of each model. In probe trials, participants were then exposed to ambiguous stimuli. In probe trials where the ambiguous stimulus could be fitted equally well by both models, we found that participants showed a clear preference for the simpler model. Moreover, we found that participants’ choice behaviour was quantitatively consistent with Bayesian Occam''s Razor. We also show that participants’ drawn trajectories were similar to samples from the Bayesian predictive distribution over trajectories and significantly different from two non-probabilistic heuristics. In two control experiments, we show that the preference of the simpler model cannot be simply explained by a difference in physical effort or by a preference for curve smoothness. Our results suggest that Occam''s Razor is a general behavioural principle already present during sensorimotor processing.     

The police are not the army: context-dependent aggressiveness in a clonal ant

Animals often exhibit particular ‘personalities’, i.e. their behaviour is correlated across different situations. Recent studies suggest that this limitation of behavioural plasticity may be adaptive, since continuous adjustment of one''s behaviour may be time-consuming and costly. In social insects, particularly aggressive workers might efficiently take over fighting in the contexts of both nest defence and ‘policing’, i.e. the regulation of kin conflict in the society. Here, we examine whether workers who engage in aggressive policing in the ant Platythyrea punctata play a prominent role also in nest defence against intruders. The participation of individuals in policing and nest defence was highly skewed and a minority of workers exhibited most of the aggression. Workers who attacked reproductives after experimental colony fusion were less active during nest defence and vice versa. This suggests that workers show situation-dependent behavioural plasticity rather than consistently aggressive personalities.     

What aspects of autism predispose to talent?

In this paper, we explore the question, why are striking special skills so much more common in autism spectrum conditions (ASC) than in other groups? Current cognitive accounts of ASC are briefly reviewed in relation to special skills. Difficulties in ‘theory of mind’ may contribute to originality in ASC, since individuals who do not automatically ‘read other minds’ may be better able to think outside prevailing fashions and popular theories. However, originality alone does not confer talent. Executive dysfunction has been suggested as the ‘releasing’ mechanism for special skills in ASC, but other groups with executive difficulties do not show raised incidence of talents. Detail-focused processing bias (‘weak coherence’, ‘enhanced perceptual functioning’) appears to be the most promising predisposing characteristic, or ‘starting engine’, for talent development. In support of this notion, we summarize data from a population-based twin study in which parents reported on their 8-year-olds'' talents and their ASC-like traits. Across the whole sample, ASC-like traits, and specifically ‘restricted and repetitive behaviours and interests’ related to detail focus, were more pronounced in children reported to have talents outstripping older children. We suggest that detail-focused cognitive style predisposes to talent in savant domains in, and beyond, autism spectrum disorders.     

Running backwards: soft landing–hard takeoff,a less efficient rebound

Human running at low and intermediate speeds is characterized by a greater average force exerted after ‘landing’, when muscle–tendon units are stretched (‘hard landing’), and a lower average force exerted before ‘takeoff’, when muscle–tendon units shorten (‘soft takeoff’). This landing–takeoff asymmetry is consistent with the force–velocity relation of the ‘motor’ (i.e. with the basic property of muscle to resist stretching with a force greater than that developed during shortening), but it may also be due to the ‘machine’ (e.g. to the asymmetric lever system of the foot operating during stance). Hard landing and soft takeoff—never the reverse—were found in running, hopping and trotting animals using diverse lever systems, suggesting that the different machines evolved to comply with the basic force–velocity relation of the motor. Here we measure the mechanical energy of the centre of mass of the body in backward running, an exercise where the normal coupling between motor and machine is voluntarily disrupted, in order to see the relevance of the motor–machine interplay in human running. We find that the landing–takeoff asymmetry is reversed. The resulting ‘soft landing’ and ‘hard takeoff’ are associated with a reduced efficiency of positive work production. We conclude that the landing–takeoff asymmetry found in running, hopping and trotting is the expression of a convenient interplay between motor and machine. More metabolic energy must be spent in the opposite case when muscle is forced to work against its basic property (i.e. when it must exert a greater force during shortening and a lower force during stretching).     

Human–wildlife conflict in the roof of the world: Understanding multidimensional perspectives through a systematic review

Human–wildlife conflicts have intensified by many folds and at different levels in recent years. The same is true in the case of the Hindu Kush Himalaya (HKH), the roof of the world, and a region known for its wealth in biodiversity. We present a systematic literature review (SLR) using the search, appraisal, synthesis, and analysis (SALSA) framework; and for spatial and network analysis, we employed the VOSviewer software. The review—covering 240 peer—articles within a span of 27 years (from 1982 to 2019)—revealed that in the last decade, there was a 57% increase in publications but with a disproportionate geographical and thematic focus. About 82% of the research concentrated on protected areas and large carnivores and mega herbivores played a big role in such conflicts. About 53% of the studies were based on questionnaires, and the main driver reported was habitat disturbance of animals due to land‐cover change, urbanization, and increase in human population. On the management front, the studies reported the use of traditional protection techniques like guarding and fencing. Our analysis of 681 keywords revealed a prominent focus on ‘human‐wildlife conflict,’ ‘Nepal,’ ‘Bhutan,’ ‘Snow Leopard,’ and ‘Leopard’ indicating the issue linked with these species and countries. The involvement of 640 authors from 36 countries indicates increasing interest, and Nepal and India are playing key roles in the region. As for the spatial analysis that was conducted, while it showed regional variations, there were conspicuous limitations in terms of having a transboundary focus. Thus, particular attention ought to be paid to building transboundary partnerships and improving management interventions; there is also a pressing need to understand the patterns of human–wildlife convergence, especially involving meso‐mammals.     

Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.     

Social network- and community-level influences on contraceptive use: evidence from rural Poland

The diffusion of ‘modern’ contraceptives—as a proxy for the spread of low-fertility norms—has long interested researchers wishing to understand global fertility decline. A fundamental question is how local cultural norms and other people''s behaviour influence the probability of contraceptive use, independent of women''s socioeconomic and life-history characteristics. However, few studies have combined data at individual, social network and community levels to simultaneously capture multiple levels of influence. Fewer still have tested if the same predictors matter for different contraceptive types. Here, we use new data from 22 high-fertility communities in Poland to compare predictors of the use of (i) any contraceptives—a proxy for the decision to control fertility—with those of (ii) ‘artificial’ contraceptives—a subset of more culturally taboo methods. We find that the contraceptive behaviour of friends and family is more influential than are women''s own characteristics and that community level characteristics additionally influence contraceptive use. Highly educated neighbours accelerate women''s contraceptive use overall, but not their artificial method use. Highly religious neighbours slow women''s artificial method use, but not their contraceptive use overall. Our results highlight different dimensions of sociocultural influence on contraceptive diffusion and suggest that these may be more influential than are individual characteristics. A comparative multilevel framework is needed to understand these dynamics.