Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities

Cooperation and diversity abound in nature despite cooperators risking exploitation from defectors and superior competitors displacing weaker ones. Understanding the persistence of cooperation and diversity is therefore a major problem for evolutionary ecology, especially in the context of well-mixed populations, where the potential for exploitation and displacement is greatest. Here we demonstrate that a “loner effect”, described by economic game theorists, can maintain cooperation and diversity in real-world biological settings. We use mathematical models of public-good-producing bacteria to show that the presence of a loner strain, which produces an independent but relatively inefficient good, can lead to rock-paper-scissor dynamics, whereby cooperators outcompete loners, defectors outcompete cooperators, and loners outcompete defectors. These model predictions are supported by our observations of evolutionary dynamics in well-mixed experimental communities of the bacterium Pseudomonas aeruginosa. We find that the coexistence of cooperators and defectors, which respectively produce and exploit the iron-scavenging siderophore pyoverdine, is stabilized by the presence of loners with an independent iron-uptake mechanism. Our results establish the loner effect as a simple and general driver of cooperation and diversity in environments that 40 would otherwise favour defection and the erosion of diversity.Publisher PDFPeer reviewe

Iron acquisition strategies in pseudomonads: mechanisms, ecology, and evolution

Iron is important for bacterial growth and survival, as it is a common co-factor in essential enzymes. Although iron is very abundant in the earth crust, its bioavailability is low in most habitats because ferric iron is largely insoluble under aerobic conditions and at neutral pH. Consequently, bacteria have evolved a plethora of mechanisms to solubilize and acquire iron from environmental and host stocks. In this review, I focus on Pseudomonas spp. and first present the main iron uptake mechanisms of this taxa, which involve the direct uptake of ferrous iron via importers, the production of iron-chelating siderophores, the exploitation of siderophores produced by other microbial species, and the use of iron-chelating compounds produced by plants and animals. In the second part of this review, I elaborate on how these mechanisms affect interactions between bacteria in microbial communities, and between bacteria and their hosts. This is important because Pseudomonas spp. live in diverse communities and certain iron-uptake strategies might have evolved not only to acquire this essential nutrient, but also to gain relative advantages over competitors in the race for iron. Thus, an integrative understanding of the mechanisms of iron acquisition and the eco-evolutionary dynamics they drive at the community level might prove most useful to understand why Pseudomonas spp., in particular, and many other bacterial species, in general, have evolved such diverse iron uptake repertoires

Patterns of infant handling and relatedness in Barbary macaques ( Macaca sylvanus ) on Gibraltar

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 theor

Male and Female Reproductive Success in Macaca sylvanus in Gibraltar: No Evidence for Rank Dependence

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 succes

Between-year variation in population sex ratio increases with complexity of the breeding system in Hymenoptera.

While adaptive adjustment of sex ratio in the 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 moved 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 vary only 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 and queen-worker control over sex ratio, as well as 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

Reproductive specialization in multiple-queen colonies of the ant Formica exsecta

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 societie

Losing out to improve group fitness

A mathematical model provides clues as to why members of a group divide tasks between them even when specialisation reduces the performance of individuals

Losing out to improve group fitness

A mathematical model provides clues as to why members of a group divide tasks between them even when specialisation reduces the performance of individuals

Coordination of siderophore gene expression among clonal cells of the bacterium Pseudomonas aeruginosa

There has been great progress in understanding how bacterial groups coordinate social actions, such as biofilm formation and public-goods secretion. Less clear is whether the seemingly coordinated group-level responses actually mirror what individual cells do. Here, we use a microscopy approach to simultaneously quantify the investment of individual cells of the bacterium Pseudomonas aeruginosa into two public goods, the siderophores pyochelin and pyoverdine. Using gene expression as a proxy for investment, we initially observe no coordination but high heterogeneity and bimodality in siderophore investment across cells. With increasing cell density, gene expression becomes more homogenized across cells, accompanied by a moderate shift from pyochelin to pyoverdine expression. We find positive associations in the expression of pyochelin and pyoverdine genes across cells, with cell-to-cell variation correlating with cellular metabolic states. Our work suggests that siderophore-mediated signalling aligns behaviour of individuals over time and spurs a coordinated three-phase siderophore investment cycle