Pleiotropic constraints promote the evolution of cooperation in cellular groups

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how the evolution of pleiotropic genetic architectures—which link the expression of cooperative and private traits—can protect against cheater lineages and allow cooperation to evolve. We develop an age-structured model of cellular groups and show that cooperation breaks down more slowly within groups that tie expression to a private trait than in groups that do not. We then show that this results in group selection for pleiotropy, which strongly promotes cooperation by limiting the emergence of cheater lineages. These results predict that pleiotropy will rapidly evolve, so long as groups persist long enough for cheater lineages to threaten cooperation. Our results hold when pleiotropic links can be undermined by mutations, when pleiotropy is itself costly, and in mixed-genotype groups such as those that occur in microbes. Finally, we consider features of multicellular organisms—a germ line and delayed reproductive maturity—and show that pleiotropy is again predicted to be important for maintaining cooperation. The study of cancer in multicellular organisms provides the best evidence for pleiotropic constraints, where abberant cell proliferation is linked to apoptosis, senescence, and terminal differentiation. Alongside development from a single cell, we propose that the evolution of pleiotropic constraints has been critical for cooperation in many cellular groups.

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. In this study, an age-structured model of cellular groups shows that pleiotropy promotes the evolution of cooperation and may have been important for the origins of multicellularity.     

Emotional Dynamics in the Age of Misinformation

According to the World Economic Forum, the diffusion of unsubstantiated rumors on online social media is one of the main threats for our society. The disintermediated paradigm of content production and consumption on online social media might foster the formation of homogeneous communities (echo-chambers) around specific worldviews. Such a scenario has been shown to be a vivid environment for the diffusion of false claim. Not rarely, viral phenomena trigger naive (and funny) social responses—e.g., the recent case of Jade Helm 15 where a simple military exercise turned out to be perceived as the beginning of the civil war in the US. In this work, we address the emotional dynamics of collective debates around distinct kinds of information—i.e., science and conspiracy news—and inside and across their respective polarized communities. We find that for both kinds of content the longer the discussion the more the negativity of the sentiment. We show that comments on conspiracy posts tend to be more negative than on science posts. However, the more the engagement of users, the more they tend to negative commenting (both on science and conspiracy). Finally, zooming in at the interaction among polarized communities, we find a general negative pattern. As the number of comments increases—i.e., the discussion becomes longer—the sentiment of the post is more and more negative.     

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.     

Evolutionary Dynamics of Human Toll-Like Receptors and Their Different Contributions to Host Defense

Infectious diseases have been paramount among the threats to health and survival throughout human evolutionary history. Natural selection is therefore expected to act strongly on host defense genes, particularly on innate immunity genes whose products mediate the direct interaction between the host and the microbial environment. In insects and mammals, the Toll-like receptors (TLRs) appear to play a major role in initiating innate immune responses against microbes. In humans, however, it has been speculated that the set of TLRs could be redundant for protective immunity. We investigated how natural selection has acted upon human TLRs, as an approach to assess their level of biological redundancy. We sequenced the ten human TLRs in a panel of 158 individuals from various populations worldwide and found that the intracellular TLRs—activated by nucleic acids and particularly specialized in viral recognition—have evolved under strong purifying selection, indicating their essential non-redundant role in host survival. Conversely, the selective constraints on the TLRs expressed on the cell surface—activated by compounds other than nucleic acids—have been much more relaxed, with higher rates of damaging nonsynonymous and stop mutations tolerated, suggesting their higher redundancy. Finally, we tested whether TLRs have experienced spatially-varying selection in human populations and found that the region encompassing TLR10-TLR1-TLR6 has been the target of recent positive selection among non-Africans. Our findings indicate that the different TLRs differ in their immunological redundancy, reflecting their distinct contributions to host defense. The insights gained in this study foster new hypotheses to be tested in clinical and epidemiological genetics of infectious disease.     

Cooperation and Shared Beliefs about Trust in the Assurance Game

Determinants of cooperation include ingroup vs. outgroup membership, and individual traits, such as prosociality and trust. We investigated whether these factors can be overridden by beliefs about people’s trust. We manipulated the information players received about each other’s level of general trust, “high” or “low”. These levels were either measured (Experiment 1) or just arbitrarily assigned labels (Experiment 2). Players’ choices whether to cooperate or defect in a stag hunt (or an assurance game)—where it is mutually beneficial to cooperate, but costly if the partner should fail to do so—were strongly predicted by what they were told about the other player’s trust label, as well as by what they were told that the other player was told about their own label. Our findings demonstrate the importance for cooperation in a risky coordination game of both first- and second-order beliefs about how much people trust each other. This supports the idea that institutions can influence cooperation simply by influencing beliefs.     

Evolving the neuroendocrine physiology of human and primate cooperation and collective action

While many hormones play vital roles in facilitating or reinforcing cooperative behaviour, the neurohormones underlying competitive and cooperative behaviours are largely conserved across all mammals. This raises the question of how endocrine mechanisms have been shaped by selection to produce different levels of cooperation in different species. Multiple components of endocrine physiology—from baseline hormone concentrations, to binding proteins, to the receptor sensitivity and specificity—can evolve independently and be impacted by current socio-ecological conditions or individual status, thus potentially generating a wide range of variation within and between species. Here, we highlight several neurohormones and variation in hormone receptor genes associated with cooperation, focusing on the role of oxytocin and testosterone in contexts ranging from parenting and pair-bonding to reciprocity and territorial defence. While the studies reviewed herein describe the current state of the literature with regard to hormonal modulators of cooperation and collective action, there is still a paucity of research on hormonal mechanisms that help facilitate large-scale collective action. We end by discussing several potential areas for future research.     

Favoring recruitment as a conservation strategy to improve the resilience of long‐lived reptile populations: Insights from a population viability analysis

In long‐lived species, although adult survival typically has the highest elasticity, temporal variations in less canalized demographic parameters are the main drivers of population dynamics. Targeting recruitment rates may thus be the most effective strategy to manage these species. We analyzed 1,136 capture–recapture histories collected over 9 years in an isolated population of the critically endangered Lesser Antillean iguana, using a robust design Pradel model to estimate adult survival and recruitment rates. From an adult population size estimated at 928 in 2013, we found a yearly decline of 4% over the 8‐year period. As expected under the canalization hypothesis for a long‐lived species, adult survival was high and constant, with little possibility for improvement, whereas the recruitment rate varied over time and likely drove the observed population decline. We then used a prospective perturbation analysis to explore whether managing the species’ immature cohorts would at least slow the population decline. The prospective perturbation analysis suggested that a significant and sustained conservation effort would be needed to achieve a recruitment rate high enough to slow the population decline. We posit that the high recruitment rate achieved in 2014—likely due to the maintenance in 2012 of the main nesting sites used by this population—would be sufficient to slow this population''s decline if it was sustained each year. Based on the results of diverse pilot studies we conducted, we identified the most likely threats targeting the eggs and immature cohorts, stressing the need to improve reproductive success and survival of immature iguanas. The threats we identified are also involved in the decline of several reptile species, and species from other taxa such as ground‐nesting birds. These findings on a little‐studied taxon provide further evidence that focusing on the immature life stages of long‐lived species can be key to their conservation.     

Social structure of primate interaction networks facilitates the emergence of cooperation

Animal cooperation has puzzled biologists for a long time as its existence seems to contravene the basic notion of evolutionary biology that natural selection favours ‘selfish’ genes that promote only their own well-being. Evolutionary game theory has shown that cooperators can prosper in populations of selfish individuals if they occur in clusters, interacting more frequently with each other than with the selfish. Here we show that social networks of primates possess the necessary social structure to promote the emergence of cooperation. By simulating evolutionary dynamics of cooperative behaviour on interaction networks of 70 primate groups, we found that for most groups network reciprocity augmented the fixation probability for cooperation. The variation in the strength of this effect can be partly explained by the groups’ community modularity—a network measure for the groups’ heterogeneity. Thus, given selective update and partner choice mechanisms, network reciprocity has the potential to explain socially learned forms of cooperation in primate societies.     

Threshold Games and Cooperation on Multiplayer Graphs

ObjectiveThe study investigates the effect on cooperation in multiplayer games, when the population from which all individuals are drawn is structured—i.e. when a given individual is only competing with a small subset of the entire population.MethodTo optimize the focus on multiplayer effects, a class of games were chosen for which the payoff depends nonlinearly on the number of cooperators—this ensures that the game cannot be represented as a sum of pair-wise interactions, and increases the likelihood of observing behaviour different from that seen in two-player games. The chosen class of games are named “threshold games”, and are defined by a threshold, M > 0, which describes the minimal number of cooperators in a given match required for all the participants to receive a benefit. The model was studied primarily through numerical simulations of large populations of individuals, each with interaction neighbourhoods described by various classes of networks.ResultsWhen comparing the level of cooperation in a structured population to the mean-field model, we find that most types of structure lead to a decrease in cooperation. This is both interesting and novel, simply due to the generality and breadth of relevance of the model—it is likely that any model with similar payoff structure exhibits related behaviour. More importantly, we find that the details of the behaviour depends to a large extent on the size of the immediate neighbourhoods of the individuals, as dictated by the network structure. In effect, the players behave as if they are part of a much smaller, fully mixed, population, which we suggest an expression for.

Highlights

• Observed behaviour depends on the size of each player’s immediate interaction neighbourhood.
• When the number of players is much larger than the number of required cooperators, average payoff decreases.
• Most network structures lead to a decrease in cooperation compared to the fully mixed case.

     

Social Value Induction and Cooperation in the Centipede Game

The Centipede game provides a dynamic model of cooperation and competition in repeated dyadic interactions. Two experiments investigated psychological factors driving cooperation in 20 rounds of a Centipede game with significant monetary incentives and anonymous and random re-pairing of players after every round. The main purpose of the research was to determine whether the pattern of strategic choices observed when no specific social value orientation is experimentally induced—the standard condition in all previous investigations of behavior in the Centipede and most other experimental games—is essentially individualistic, the orthodox game-theoretic assumption being that players are individualistically motivated in the absence of any specific motivational induction. Participants in whom no specific state social value orientation was induced exhibited moderately non-cooperative play that differed significantly from the pattern found when an individualistic orientation was induced. In both experiments, the neutral treatment condition, in which no orientation was induced, elicited competitive behavior resembling behavior in the condition in which a competitive orientation was explicitly induced. Trait social value orientation, measured with a questionnaire, influenced cooperation differently depending on the experimentally induced state social value orientation. Cooperative trait social value orientation was a significant predictor of cooperation and, to a lesser degree, experimentally induced competitive orientation was a significant predictor of non-cooperation. The experimental results imply that the standard assumption of individualistic motivation in experimental games may not be valid, and that the results of such investigations need to take into account the possibility that players are competitively motivated.     

When cooperation begets cooperation: the role of key individuals in galvanizing support

Life abounds with examples of conspecifics actively cooperating to a common end, despite conflicts of interest being expected concerning how much each individual should contribute. Mathematical models typically find that such conflict can be resolved by partial-response strategies, leading investors to contribute relatively equitably. Using a case study approach, we show that such model expectations can be contradicted in at least four disparate contexts: (i) bi-parental care; (ii) cooperative breeding; (iii) cooperative hunting; and (iv) human cooperation. We highlight that: (a) marked variation in contributions is commonplace; and (b) individuals can often respond positively rather than negatively to the contributions of others. Existing models have surprisingly limited power in explaining these phenomena. Here, we propose that, although among-individual variation in cooperative contributions will be influenced by differential costs and benefits, there is likely to be a strong genetic or epigenetic component. We then suggest that selection can maintain high investors (key individuals) when their contributions promote support by increasing the benefits and/or reducing the costs for others. Our intentions are to raise awareness in—and provide testable hypotheses of—two of the most poorly understood, yet integral, questions regarding cooperative ventures: why do individuals vary in their contributions and when does cooperation beget cooperation?     

Using Latent Selection Difference to Model Persistence in a Declining Population

Population persistence is a direct measure of the viability of a population. Monitoring the distribution of declining populations or subpopulations over time can yield estimates of persistence, which we show can be modeled as a latent selection difference (LSD) contrasting attributes of sites where populations have persisted versus those that have not. Predicted persistence can be modeled with predictor covariates to identify factors correlated with species persistence. We demonstrate how to model persistence based on changes in occupancy that can include adjustments for detection probability. Using a known historical distribution of the western grebe (Aechmophorus occidentalis), we adapted methods originally developed for occupancy modeling to evaluate how environmental covariates including emergent vegetation and human developments have affected western grebe persistence in Alberta. The relative probability of persistence was correlated with the extent of shoreline bulrush (Scirpus lacustris), which is important vegetation for nesting cover. We also documented that western grebe populations were less likely to persist on lakes in the boreal forest, primarily located on the northern boundary of the species'' range. Factors influencing occupancy were different than those determining persistence by western grebes; persistence and occupancy were not correlated. Persistence was more likely on lakes with recreational development, reflecting reliance by grebes on the larger, fish-bearing waterbodies that also are attractive for lakeshore development. Unfortunately, the correlation with recreational development on Alberta''s lakes puts grebes at risk for loss of brood-rearing habitats—primary threats to altricial birds—if steps are not taken to prevent disturbance to bulrush stands. Identifying factors related to the persistence of a species—especially one in decline—is a fundamental step in conservation management.     

Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria

Recent theoretical models have postulated a role for haploid–diploid conflict and for kin selection favouring sperm cooperation and altruism in the diversification and specialization of sperm form. A critical assumption of these models—that haploid gene expression contributes to variation in sperm form—has never been demonstrated and remains contentious. By quantifying within-male variation in sperm length using crosses between males and females from populations that had been subjected to divergent experimental selection, we demonstrate that haploid gene expression does not contribute to variation in sperm length in both Drosophila melanogaster and Scathophaga stercoraria. This finding casts doubt on the importance of haploid–diploid conflict and kin selection as evolutionary influences of sperm phenotypes.     

Cooperation Improves Success during Intergroup Competition: An Analysis Using Data from Professional Soccer Tournaments

The benefit mutually gained by cooperators is considered the ultimate explanation for why cooperation evolved among non-relatives. During intergroup competition, cooperative behaviours within groups that provide a competitive edge over their opposition should be favoured by selection, particularly in lethal human warfare. Aside from forming larger groups, three other ways that individuals within a group can cooperate to improve their chances of gaining a mutual benefit are: (i) greater networking, (ii) contributing more effort, and (iii) dividing labour. Greater cooperation is expected to increase the chances of gaining a group benefit by improving proficiency in the tasks critical to success—yet empirical tests of this prediction using real-world cases are absent. In this study, we used data derived from 12 international and professional soccer competitions to test the predictions that: 1) greater levels of cooperative behaviour are associated with winning group contests, 2) the three forms of cooperation differ in relative importance for winning matches, 3) competition and tournament-type affect the levels of cooperation and shooting proficiency in matches, and 4) greater levels of networking behaviour are associated with increased proficiency in the most critical task linked with winning success in soccer—shooting at goal. Winners were best predicted by higher shooting proficiency, followed by greater frequencies of networking interactions within a team but unexpectedly, fewer networking partners and less division of labour. Although significant variation was detected across competitions and tournament-types, greater levels of networking behaviour were consistently associated with increased proficiency in shooting at goal, which in turn was linked with winning success. This study empirically supports the idea that intergroup competition can favour cooperation among non-relatives.     

Cooperation,clumping and the evolution of multicellularity

The evolution of multicellular organisms represents one of the major evolutionary transitions in the history of life. A potential advantage of forming multicellular clumps is that it provides an efficiency benefit to pre-existing cooperation, such as the production of extracellular ‘public goods’. However, this is complicated by the fact that cooperation could jointly evolve with clumping, and clumping could have multiple consequences for the evolution of cooperation. We model the evolution of clumping and a cooperative public good, showing that (i) when considered separately, both clumping and public goods production gradually increase with increasing genetic relatedness; (ii) in contrast, when the traits evolve jointly, a small increase in relatedness can lead to a major shift in evolutionary outcome—from a non-clumping state with low public goods production to a cooperative clumping state with high values of both traits; (iii) high relatedness makes it easier to get to the cooperative clumping state and (iv) clumping can be inhibited when it increases the number of cells that the benefits of cooperation must be shared with, but promoted when it increases relatedness between those cells. Overall, our results suggest that public goods sharing can facilitate the formation of well-integrated cooperative clumps as a first step in the evolution of multicellularity.     

Malnutrition in the Field. Nigerian Civil War 1968-9

A short-term, large-scale medical and feeding programme has been provided for a population of 150,000 in the bush area near Udi in eastern Nigeria (Biafra). By January 1969 8,000 patients were receiving medical treatment each week for varying degrees of protein malnutrition (including kwashiorkor), vitamin deficiency, and dehydration; while 100,000 received weekly rations of a protein-supplemented diet. Close cooperation between the medical team—which consisted of one doctor, four nurses, and two relief workers—and the local Ibo people contributed to the success of the relief programme.     

Development of the SAFE Checklist Tool for Assessing Site-Level Threats to Child Protection: Use of Delphi Methods and Application to Two Sites in India

Background

The child protection community is increasingly focused on developing tools to assess threats to child protection and the basic security needs and rights of children and families living in adverse circumstances. Although tremendous advances have been made to improve measurement of individual child health status or household functioning for use in low-resource settings, little attention has been paid to a more diverse array of settings in which many children in adversity spend time and how context contributes to threats to child protection. The SAFE model posits that insecurity in any of the following fundamental domains threatens security in the others: Safety/freedom from harm; Access to basic physiological needs and healthcare; Family and connection to others; Education and economic security. Site-level tools are needed in order to monitor the conditions that can dramatically undermine or support healthy child growth, development and emotional and behavioral health. From refugee camps and orphanages to schools and housing complexes, site-level threats exist that are not well captured by commonly used measures of child health and well-being or assessments of single households (e.g., SDQ, HOME).

Methods

The present study presents a methodology and the development of a scale for assessing site-level child protection threats in various settings of adversity. A modified Delphi panel process was enhanced with two stages of expert review in core content areas as well as review by experts in instrument development, and field pilot testing.

Results

Field testing in two diverse sites in India—a construction site and a railway station—revealed that the resulting SAFE instrument was sensitive to the differences between the sites from the standpoint of core child protection issues.     

The future of evolutionary diversity in reef corals

One-third of the world''s reef-building corals are facing heightened extinction risk from climate change and other anthropogenic impacts. Previous studies have shown that such threats are not distributed randomly across the coral tree of life, and future extinctions have the potential to disproportionately reduce the phylogenetic diversity of this group on a global scale. However, the impact of such losses on a regional scale remains poorly known. In this study, we use phylogenetic metrics in conjunction with geographical distributions of living reef coral species to model how extinctions are likely to affect evolutionary diversity across different ecoregions. Based on two measures—phylogenetic diversity and phylogenetic species variability—we highlight regions with the largest losses of evolutionary diversity and hence of potential conservation interest. Notably, the projected loss of evolutionary diversity is relatively low in the most species-rich areas such as the Coral Triangle, while many regions with fewer species stand to lose much larger shares of their diversity. We also suggest that for complex ecosystems like coral reefs it is important to consider changes in phylogenetic species variability; areas with disproportionate declines in this measure should be of concern even if phylogenetic diversity is not as impacted. These findings underscore the importance of integrating evolutionary history into conservation planning for safeguarding the future diversity of coral reefs.     

Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales

Background

Resolving threats to widely distributed marine megafauna requires definition of the geographic distributions of both the threats as well as the population unit(s) of interest. In turn, because individual threats can operate on varying spatial scales, their impacts can affect different segments of a population of the same species. Therefore, integration of multiple tools and techniques — including site-based monitoring, genetic analyses, mark-recapture studies and telemetry — can facilitate robust definitions of population segments at multiple biological and spatial scales to address different management and research challenges.

Methodology/Principal Findings

To address these issues for marine turtles, we collated all available studies on marine turtle biogeography, including nesting sites, population abundances and trends, population genetics, and satellite telemetry. We georeferenced this information to generate separate layers for nesting sites, genetic stocks, and core distributions of population segments of all marine turtle species. We then spatially integrated this information from fine- to coarse-spatial scales to develop nested envelope models, or Regional Management Units (RMUs), for marine turtles globally.

Conclusions/Significance

The RMU framework is a solution to the challenge of how to organize marine turtles into units of protection above the level of nesting populations, but below the level of species, within regional entities that might be on independent evolutionary trajectories. Among many potential applications, RMUs provide a framework for identifying data gaps, assessing high diversity areas for multiple species and genetic stocks, and evaluating conservation status of marine turtles. Furthermore, RMUs allow for identification of geographic barriers to gene flow, and can provide valuable guidance to marine spatial planning initiatives that integrate spatial distributions of protected species and human activities. In addition, the RMU framework — including maps and supporting metadata — will be an iterative, user-driven tool made publicly available in an online application for comments, improvements, download and analysis.