Rolf Kümmerli

Abstract: Bacteria secrete a large variety of beneficial metabolites into the environment, which can be shared as public goods among producing bacteria, but also be exploited by non-producing cheats. Here, we focus on cooperative production of iron-chelating molecules (siderophores) in the bacterium Pseudomonas aeruginosa to study how relevant ecological factors influence selection for cheating. We designed patch-structured metapopulations that allowed us introducing among-patch ecological variation. We found that cheating readily evolved in uniform iron-limited environments. This finding is explained by severe iron limitation demanding high siderophore-production efforts, which results in high metabolic costs accruing to cooperators, and thereby facilitates the spread of cheats. In contrast, we observed a significant reduction or even negation of selection for cheating in metapopulations where we introduced patches with increased iron availability and/or opportunities to recycle siderophores. These findings are compatible with the view that cheats are less likely to invade in environments that allow bacteria to reduce siderphore-production efforts, as this lowers the overall metabolic costs accruing to cooperators. Because we increased iron availability and siderophore recycling opportunities moderately, and only in some patches, our findings demonstrate that already small local variations in ecological conditions as occurring in nature can significantly affect selection for public-good secretion in microbes. In addition, we found that most (84.6%) of the evolved cheats were partially deficient for siderophore production and not loss-of-function mutants. Genetic considerations indicate that mutations leading to partial deficiency occur more frequent than mutations leading to loss of function, but also suggest that partially-deficient mutants might often be the more competitive cheats.

Abstract: While adaptive adjustment of sex ratio in function of colony kin structure and food availability commonly occurs in social Hymenoptera, long-term studies have revealed substantial unexplained between-year variation in sex ratio at the population level. In order to identify factors that contribute to increased between-year variation in population sex ratio, we conducted a comparative analysis across 47 Hymenoptera species differing in their breeding system. We found that between-year variation in population sex ratio steadily increased as one moves from solitary species, to primitively eusocial species, to single-queen eusocial species, to multiple-queen eusocial species. Specifically, between-year variation in population sex ratio was low (6.6% of total possible variation) in solitary species, which is consistent with the view that in solitary species sex ratio can only vary in response to fluctuations in ecological factors such as food availability. In contrast, we found significantly higher (19.5%) between-year variation in population sex ratio in multiple-queen eusocial species, which supports the view that in these species sex ratio can also fluctuate in response to temporal changes in social factors such as queen number, queen-worker control over sex ratio, and factors influencing caste determination. The simultaneous adjustment of sex ratio in response to temporal fluctuations in ecological and social factors seems to preclude the existence of a single sex ratio optimum. The absence of such an optimum may reflect an additional cost associated with the evolution of complex breeding systems in Hymenoptera societies.

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Abstract: In social groups where relatedness among interacting individuals is low, cooperation can often only be maintained through mechanisms that repress competition among group members. Repression-of-competition mechanisms, such as policing and punishment, seem to be of particular importance in human societies, where cooperative interactions often occur among unrelated individuals. In line with this view, economic games have shown that the ability to punish defectors enforces cooperation among humans. Here, I examine a real-world example of a repression-of-competition system, the police institutions common to modern human societies. Specifically, I test evolutionary policing theory by comparing data on policing effort, per capita crime rate, and similarity (used as a proxy for genetic relatedness) among citizens across the 26 cantons of Switzerland. This comparison revealed full support for all three predictions of evolutionary policing theory. First, when controlling for policing efforts, crime rate correlated negatively with the similarity among citizens. This is in line with the prediction that high similarity results in higher levels of cooperative self-restraint (i.e. lower crime rates) because it aligns the interests of individuals. Second, policing effort correlated negatively with the similarity among citizens, supporting the prediction that more policing is required to enforce cooperation in low-similarity societies, where individuals' interests diverge most. Third, increased policing efforts were associated with reductions in crime rates, indicating that policing indeed enforces cooperation. These analyses strongly indicate that humans respond to cues of their social environment and adjust cheating and policing behaviour as predicted by evolutionary policing theory.

Abstract: Repression of competition within social groups has been suggested as a key mechanism driving the evolution of cooperation, because it aligns the individual’s proximate interest with the interest of the group. Despite its enormous potential for explaining cooperation across all levels of biological organization, ranging from fair meiosis, to policing in insect societies, to sanctions in mutualistic interactions between species, there has been no direct experimental test of whether repression of competition favours the spread of cooperators in a well-mixed population with cheats. To address this, we carried out an experimental evolution study to test the effect of repression of competition upon a cooperative trait - the production of iron-scavenging siderophore molecules - in the bacterium Pseudomonas aeruginosa. We found that cooperation was favoured when competition between siderophore producers and non-siderophore-producing cheats was repressed, but not in a treatment where competition between the two strains was permitted. We further show that repression of competition altered the cost of cooperation, but did not affect the relatedness among interacting individuals. This confirms that repression of competition per se, as opposed to increased relatedness, has driven the observed increase in bacterial cooperation.

Abstract: The results of numerous economic games suggest that humans behave more cooperatively than would be expected if they were maximizing selfish interests. It has been argued that this is because individuals gain satisfaction from the success of others, and that such prosocial preferences require a novel evolutionary explanation. However, in previous games, imperfect behavior would automatically lead to an increase in cooperation, making it impossible to decouple any form of mistake or error from prosocial cooperative decisions. Here we empirically test between these alternatives by decoupling imperfect behavior from prosocial preferences in modified versions of the public goods game, in which individuals would maximize their selfish gain by completely (100%) cooperating. We found that, although this led to higher levels of cooperation, it did not lead to full cooperation, and individuals still perceived their group mates as competitors. This is inconsistent with either selfish or prosocial preferences, suggesting that the most parsimonious explanation is imperfect behavior triggered by psychological drives that can prevent both complete defection and complete cooperation. More generally, our results illustrate the caution that must be exercised when interpreting the evolutionary implications of economic experiments, especially the absolute level of cooperation in a particular treatment.

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Abstract: Split sex ratio – a pattern where colonies within a population specialise in either male or queen production – is a widespread phenomenon in ants and other social Hymenoptera. It has often been attributed to variation in colony kin structure, which affects the degree of queen-worker conflict over optimal sex allocation. However, recent findings suggest that split sex ratio is a more diverse phenomenon, which can evolve for multiple reasons. Here, we provide an overview of the main conditions favouring split sex ratio. We show that each split sex-ratio type arises due to a different combination of factors determining colony kin structure, queen or worker control over sex ratio, and the type of conflict between colony members.

Abstract: There has been extensive theoretical debate over whether population viscosity (limited dispersal) can favour cooperation. While limited dispersal increases the probability of interactions occurring between relatives, which can favour cooperation, it can also lead to an increase in competition between relatives and this can reduce or completely negate selection for cooperation. Despite much theoretical attention, there is a lack of empirical research investigating these issues. We cultured Pseudomonas aeruginosa bacteria in medium with different degrees of viscosity and examined the fitness consequences for a cooperative trait - the production of iron-scavenging siderophore molecules. We found that increasing viscosity of the growth medium 1) significantly limited bacterial dispersal and the diffusion of siderophore molecules and 2) increased the fitness of individuals that produced siderophores relative to mutants that did not. We propose that viscosity promotes siderophore production in this system because the benefits of siderophore production are more likely to accrue to relatives (i.e. greater indirect benefits), and at the same time bacteria are more likely to gain direct fitness benefits by taking up siderophore molecules produced by themselves (i.e. the trait becomes less cooperative). Our results suggest that viscosity of the microbial growth environment is a crucial factor determining the dynamics of wildtype bacteria and siderophore-deficient mutants in natural habitats, such as the viscous mucus in cystic fibrosis lung.

Abstract: There is strong evidence that natural selection can favour phenotypic plasticity as a mechanism to maximize fitness in animals. Here, we aim to investigate phenotypic plasticity of a cooperative trait in bacteria – the production of an iron-scavenging molecule (pyoverdin) by Pseudomonas aeruginosa. Pyoverdin production is metabolically costly to the individual cell, but provides a benefit to the local group and can potentially be exploited by nonpyoverdinproducing cheats. Here, we subject bacteria to changes in the social environment in media with different iron availabilities and test whether cells can adjust pyoverdin production in response to these changes. We found that pyoverdin production per cell significantly decreased at higher cell densities and increased in the presence of cheats. This phenotypic plasticity significantly influenced the costs and benefits of cooperation. Specifically, the investment of resources into pyoverdin production was reduced in iron-rich environments and at high cell densities, but increased under iron limitation, and when pyoverdin was exploited by cheats. Our study demonstrates that phenotypic plasticity in a cooperative trait as a response to changes in the environment occurs in even the simplest of organisms, a bacterium.

Abstract: Numerous theoretical studies have investigated how limited dispersalmay provide an explanation for the evolution of cooperation, by leading to interactions between relatives. However, despite considerable theoretical attention, there has been a lack of empirical tests. In this article,we test how patterns of dispersal influence the evolution of cooperation, using iron-scavenging in the bacterium Pseudomonas aeruginosa as our cooperative trait.We found that relatively limited dispersal does not favor cooperation. The reason for this is that although limited dispersal increases the relatedness between interacting individuals, it also leads to increased local competition for resources between relatives. This result supports Taylor’s prediction that in the simplest possible scenario, the effects of increased relatedness and local competition exactly cancel out. In contrast, we show that one way for cooperation to be favored is if individuals disperse in groups (budding dispersal), because this maintains high relatedness while reducing local competition between relatives (relatively global competition).

Abstract: Phenotypic noise and social evolution in microbes have recently attracted huge interdisciplinary interest. A new study highlights the interaction between these phenomena and its implications for self-destructive cooperation.

Abstract: Among papionin primates, the Barbary macaque (Macaca sylvanus) shows the most extensive interactions between infants and group members other than the mother. Two different types of interactions occur: (1) long-lasting dyadic interactions between a handler and an infant, and (2) brief triadic interactions between two handlers involving an infant. Previous investigations showed that infant handling by males is best explained as use of infants to manage relationships with other males. In contrast, no adaptive explanation for infant handling by females emerged. Here, we compared the infant-handling pattern between subadult/adult males and subadult/adult females in a free-ranging group of 46 Barbary macaques on Gibraltar to test whether the relationship management hypothesis also applies to female handlers. We further investigated the infant-handling pattern of juveniles and used microsatellite markers to estimate relatedness between infant handlers and the infant’s mother. We found that males, females and juveniles all participated extensively in triadic interactions using infants of above-average related females. In contrast, only males and juveniles were highly involved in dyadic interactions with infants of related females, while females rarely handled infants other than their own. The pattern of infant handling was entirely compatible with the predictions of the relationship management hypothesis for males and mostly so for females. Moreover, our genetic analysis revealed that males and females differ in their partner choice: while females preferred to interact with related females, males had no significant preference to interact with related males. We further discuss the observed above-average relatedness values between infant handlers and the infant’s mother in the light of kin-selection theory.

Abstract: Due to their haplo-diploid sex determination system and the resulting conflict over optimal sex allocation between queens and workers, social Hymenoptera have become important model species to study variation in sex allocation. While many studies indeed reported sex allocation to be affected by social factors such as colony kin structure or queen number, others, however, found that sex allocation was impacted by ecological factors such as food availability. In this paper, we present one of the rare studies that simultaneously investigated the effects of social and ecological factors on social insect nest reproductive parameters (sex and reproductive allocation, nest productivity) across several years. We found that the sex ratio was extremely male biased in a polygynous (multiple queens per nest) population of the ant Formica exsecta. Nest-level sex allocation followed the pattern predicted by the queen-replenishment hypothesis, which holds that gynes (new queens) should only be produced and recruited in nests with low queen number (i.e. reduced local resource competition) to ensure nest survival. Accordingly, queen number (social factor) was the main determinant on whether a nest produced gynes or males. However, ecological factors had a large impact on nest productivity and therefore on a nest's resource pool, which determines the degree of local resource competition among co-breeding queens and at what threshold in queen number nests should switch from male to gyne production. Additionally, our genetic data revealed that gynes are recruited back to their parental nests after mating. However, our genetic data are also consistent with some adult queens dispersing on foot from nests where they were produced to nests that never produced queens. As worker production is reduced in gyne-producing nests, queen migration might be offset by workers moving in the other direction, leading to a nest network characterized by reproductive division of labour. Altogether our study shows that both, social and ecological factors can influence long-term nest reproductive strategies in insect societies.

Abstract: In polygynous (multiple queens per nest) colonies of social insects, queens can increase their reproductive share by laying more eggs or by increasing the proportion of eggs that develop into reproductive individuals instead of workers. We used polymorphic microsatellite loci to determine the genetically effective contribution of queens to the production of gynes (new queens), males, and 2 different cohorts of workers in a polygynous population of the ant Formica exsecta. For this purpose, we developed a new method that can be used for diploid and haplodiploid organisms to quantify the degree of reproductive specialization among breeders in societies where there are too many breeders to ascertain parentage. Using this method, we found a high degree of reproductive specialization among nest-mate queens in both female- and male-producing colonies (sex ratio is bimodally distributed in the study population). For example, a high effective proportion of queens (25% and 79%, respectively) were specialized in the production of males in female- and male-producing colonies. Our analyses further revealed that in female-producing colonies, significantly fewer queens contributed to gyne production than to worker production. Finally, we found significant changes in the identity of queens contributing to different cohorts of workers. Altogether, these data demonstrate that colonies of F. exsecta, and probably those of many other highly polygynous social insect species, are composed of reproductive individuals differing in their investment to gynes, males, and workers. These findings demonstrate a new aspect of the highly dynamic social organization of complex animal societies.

Abstract: Explaining the evolution of cooperation among non-relatives is one of the major challenges for evolutionary biology. In this study, we experimentally examined human cooperation in the iterated Snowdrift game (ISD), which has received little attention so far, and compared it with human cooperation in the iterated Prisoner's Dilemma (IPD), which has become the paradigm for the evolution of cooperation. We show that iteration in the ISD leads to consistently higher levels of cooperation than in the IPD. We further demonstrate that the most successful strategies known for the IPD (generous Tit-for-Tat and Pavlov) were also successfully used in the ISD. Interestingly, we found that female players cooperated significantly more often than male players in the IPD but not in the ISD. Moreover, female players in the IPD applied Tit-for-Tat-like or Pavlovian strategies significantly more often than male players, thereby achieving significantly higher pay-offs than male players did. These data demonstrate that the willingness to cooperate does not only depend on the type of the social dilemma, but also on the class of individuals involved. Altogether, our study shows that the ISD can potentially explain high levels of cooperation among non-relatives in humans. In addition, the ISD seems to reflect the social dilemma more realistically than the IPD because individuals obtain immediate direct benefits from the cooperative acts they perform and costs of cooperation are shared between cooperators.

Abstract: A key feature differentiating animal societies is the partitioning of reproduction among breeders. We studied how reproduction is partitioned among nestmate queens of the ant Formica exsecta in laboratory colonies. In polygynous (multiple-queen) colonies, queens can increase their reproductive success by laying more eggs or by increasing the proportion of eggs that develop into reproductive individuals instead of workers. We found that reproductive skew among queens for egg production was low, but that 84% of all queens contributed exclusively to one type of brood, either males or workers (no new queens are produced in the laboratory). Furthermore, our data revealed that the degree of reproductive specialization among queens significantly increased during brood development. Contrary to predictions of most reproductive skew models, the extent of reproductive skew was not associated with relatedness among co-breeding queens. We also found no association between the pattern of queen specialization and relatedness between queens and their mates. Such an association would occur if queens mated to related males specialize in male production to avoid the cost of inbreeding. Altogether, our findings show a yet undescribed pattern of reproductive specialization among nestmate queens in ants and emphasizes the need to investigate reproductive contributions of queens for each type of offspring separately. (c) 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Abstract: The theory of inclusive fitness provides a powerful explanation for reproductive altruism in social insects, whereby workers gain inclusive fitness benefit by rearing the brood of related queens. Some ant species, however, have unicolonial population structures where multiple nests, each containing numerous queens, are interconnected and individuals move freely between nests. In such cases, nestmate relatedness values may often be indistinguishable from zero, which is problematic for inclusive fitness-based explanations of reproductive altruism. We conducted a detailed population genetic study in the polygynous ant Formica exsecta, which has been suggested to form unicolonial populations in its native habitat. Analyses based on adult workers indeed confirmed a genetic structuring consistent with a unicolonial population structure. However, at the population level the genetic structuring inferred from worker pupae was not consistent with a unicolonial population structure, but rather suggested a multicolonial population structure of extended family-based nests. These contrasting patterns suggest limited queen dispersal and free adult worker dispersal. That workers indeed disperse as adults was confirmed by mark-recapture measures showing consistent worker movement between nests. Together, these findings describe a new form of social organization, which possibly also characterizes other ant species forming unicolonial populations in their native habitats. Moreover, the genetic analyses also revealed that while worker nestmate relatedness was indistinguishable from zero at a small geographical scale, it was significantly positive at the population level. This highlights the need to consider the relevant geographical scale when investigating the role of inclusive fitness as a selective force maintaining reproductive altruism.

Abstract: In animal societies, cooperation for the common wealth and latent conflicts due to the selfish interests of individuals are in delicate balance. In many ant species, colonies contain multiple breeders and workers interact with nestmates of varying degrees of relatedness. Therefore, workers could increase their inclusive fitness by preferentially caring for their closest relatives, yet evidence for nepotism in insect societies remains scarce and controversial. We experimentally demonstrate that workers of the ant Formica exsecta do not discriminate between highly related and unrelated brood, but that brood viability differs between queens. We further show that differences in brood viability are sufficient to explain a relatedness pattern that has previously been interpreted as evidence for nepotism. Hence, our findings support the view that nepotism remains elusive in social insects and emphasize the need for further controlled experiments.

Abstract: In polygynous (multiple queens per nest) ants, queen dispersal is often limited with young queens being recruited within the parental colony. This mode of dispersal leads to local resource competition between nestmate queens and is frequently associated with extremely male-biased sex ratios at the population level. The queen-replenishment hypothesis has been recently proposed to explain colony sex ratio investment under such conditions. It predicts that colonies containing many queens (subject to high local resource competition) should only produce males, whereas colonies hosting few queens (reduced or no local resource competition) should produce new queens in addition to males. We experimentally tested this hypothesis in the ant Formica exsecta by manipulating queen number over three consecutive years in 120 colonies of a highly polygynous population. Queens were transferred from 40 colonies into another 40 colonies while queen number was not manipulated in 40 control colonies. Genetic analyses of worker offspring revealed that our treatment significantly changed the number of reproductive queens. The sex ratio of colonies was significantly different between treatments in the third breeding season following the experiment initiation. We found that, as predicted by the queen-replenishment hypothesis, queen removal resulted in a significant increase in the proportion of colonies that produced new queens. These results provide the first experimental evidence for the queen-replenishment hypothesis, which might account for sex ratio specialization in many highly polygynous ant species.

Abstract: The relationship between social rank and reproductive success is one of the key questions for understanding differences in primate social group structures. We determined the paternity of 18 infants in a social group of Barbary macaques (Macaca sylvanus) born over a period of 6 yr in the provisioned, free-ranging colony in Gibraltar. We successfully used 13 pairs of primers of variable microsatellite loci to amplify DNA from blood and hair samples and applied the computer programs CERVUS 2.0 and KINSHIP 1.3 to assign paternity to 13 candidate males. We collected data for 19 females that had given birth to 66 infants over a period of 7 yr. We used paternity analyses and female birth records to test the hypothesis that social rank is correlated with reproductive success. Results showed that numbers of paternities and maternities were equally distributed among all reproducing individuals in the social group regardless of rank. Subadult males reproduced as often as adult males. High-ranking females did not start to reproduce earlier than low-ranking females. Interestingly, there was a tendency toward a positive correlation between the ranks of mothers and the ranks of the corresponding fathers. It might be concluded either that a correlation between social rank and reproductive success is generally absent in Barbary macaques or that artificially favorable environmental conditions in Gibraltar preclude any correlation between social rank and reproductive success.

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Abstract: The Barbary macaque (Macaca sylvanus) shows the most extensive infant-carrying behaviour in the genus Macaca. Different hypotheses have been investigated and discussed in previous studies, but none was able to explain all types of observed behaviour. In this study, a group of 46 wild Barbary macaques in Gibraltar was observed during three months of early infant life. Data were collected on dyadic and triadic interactions of all categories of carriers (males, females, juveniles). There was a high level of competition for access to infants. Males preferred to carry infants of multiparous and high-ranking females. Females other than the mother were very rarely involved in infant handling. Juveniles carried their newborn relatives. Adult carriers and mothers used infants as tools to form coalitions to maintain or improve rank position. There is some evidence that position in the hierarchy correlates with reproductive success in Barbary macaques, it is suggested that infant handling is a mating strategy. As the treatment of infants by carriers is consistently very gentle, infants may benefit from integration into the social network.

Abstract: Genetic determination of paternities in social groups of primates has become very important for interpretation of behavioural data. In the past, reproductive success, helping behaviour among relatives and other kin-based hypotheses were often investigated only on the basis of behavioural data. Today, genetic markers such as microsatellites provide a tool to test assumptions based on behavioural observations. Since 1994, the Anthropological Institute of Zürich has had an established research programme in Gibraltar. Over this period, several studies have been conducted. One of these focused on the mating behaviour of 6 focal females. Mating success of males was recorded. To test whether mating success is correlated with reproductive success, it is essential to determine paternities of the sired offspring. To obtain stronger results for the studies already conducted and for future studies, the aim of this work was to establish a set of microsatellite markers permitting determination of paternity. Fifty-five samples (32 blood samples and 23 hair samples) of known animals were available. These samples included 15 known mother-infant pairs (including 5 out of the 6 infants from the study on mating success) and samples from 9–13 potential fathers. Samples from 3 potential fathers were unavailable. Eight human microsatellite loci were tested; 4 of them (D1S207, D7S503, D11S925, D17S791) were known to show variation in Barbary macaques from an earlier study. Four additional human microsatellite systems (D2S141, D2S305, D3D1279, D6S311) known to show variation among other Old World monkeys were tested. Genetic data were analysed with the computer programmes CERVUS 2.0 and Kinship 1.3. Results indicate that there are 2 major problems. (1) Microsatellite variation was lower than expected. The Gibraltar macaque population is very isolated and seems to show some degree of inbreeding. (2) The missing samples of the three potential fathers had a major influence on the likelihood of paternities. The computer programme CERVUS takes this problem into consideration, but the likelihood values for some of the paternities assigned to the remaining males were very low. Results are compared and discussed with the results of the behavioural study on mating success.