Resource and competitive dynamics shape the benefits of public goods cooperation in a plant pathogen

Cooperative benefits depend on a variety of ecological factors. Many cooperative bacteria increase the population size of their groups by making a public good available. Increased local population size can alleviate the constraints of kin competition on the evolution of cooperation by enhancing the between-group fitness of cooperators. The cooperative pathogenesis of Agrobacterium tumefaciens causes infected plants to exude opines--resources that provide a nearly exclusive source of nutrient for the pathogen. We experimentally demonstrate that opines provide cooperative A. tumefaciens cells a within-group fitness advantage over saprophytic agrobacteria. Our results are congruent with a resource-consumer competition model, which predicts that cooperative, virulent agrobacteria are at a competitive disadvantage when opines are unavailable, but have an advantage when opines are available at sufficient levels. This model also predicts that freeloading agrobacteria that catabolize opines but cannot infect plants competitively displace the cooperative pathogen from all environments. However, we show that these cooperative public goods also promote increased local population size. A model built from the Price Equation shows that this effect on group size can contribute to the persistence of cooperative pathogenesis despite inherent kin competition for the benefits of pathogenesis.     

Molecular population genetics and the search for adaptive evolution in plants

The first papers on plant molecular population genetics were published approximately 10 years ago. Since that time, well over 50 additional studies of plant nucleotide polymorphism have been published, and many of these studies focused on detecting the signature of balancing or positive selection at a locus. In this review, we discuss some of the theoretical and statistical issues surrounding the detection of selection, with focus on plant populations, and we also summarize the empirical plant molecular population genetics literature. At face value, the literature suggests that a history of balancing or positive selection in plant genes is rampant. In two well-studied taxa (maize and Arabidopsis) over 20% of studied genes have been interpreted as containing the signature of selection. We argue that this is probably an overstatement of the prevalence of natural selection in plant genomes, for two reasons. First, demographic effects are difficult to incorporate and have generally not been well integrated into the plant population genetics literature. Second, the genes studied to date are not a random sample, so selected genes may be overrepresented. The next generation of studies in plant molecular population genetics requires additional sampling of local populations, explicit comparisons among loci, and improved theoretical methods to control for demography. Eventually, candidate loci should be confirmed by explicit consideration of phenotypic effects.     

The social evolution of dispersal with public goods cooperation

Selection can favour the evolution of individually costly dispersal if this alleviates competition between relatives. However, conditions that favour altruistic dispersal also mediate selection for other social behaviours, such as public goods cooperation, which in turn is likely to mediate dispersal evolution. Here, we investigate – both experimentally (using bacteria) and theoretically – how social habitat heterogeneity (i.e. the distribution of public goods cooperators and cheats) affects the evolution of dispersal. In addition to recovering the well‐known theoretical result that the optimal level of dispersal increases with genetic relatedness of patch mates, we find both mathematically and experimentally that dispersal is always favoured when average patch occupancy is low, but when average patch occupancy is high, the presence of public goods cheats greatly alters selection for dispersal. Specifically, when public goods cheats are localized to the home patch, higher dispersal rates are favoured, but when cheats are present throughout available patches, lower dispersal rates are favoured. These results highlight the importance of other social traits in driving dispersal evolution.     

Within-host parasite cooperation and the evolution of virulence

Infections by multiple genotypes are common in nature and are known to select for higher levels of virulence for some parasites. When parasites produce public goods (PGs) within the host, such co-infections have been predicted to select for lower levels of virulence. However, this prediction is based on simplifying assumptions regarding epidemiological feedbacks on the multiplicity of infections (MOI). Here, we analyse the case of parasites producing a PG (for example, siderophore-producing bacteria) using a nested model that ties together within-host and epidemiological processes. We find that the prediction that co-infection should select for less virulent strains for PG-producing parasites is only valid if both parasite transmission and virulence are linear functions of parasite density. If there is a trade-off relationship such that virulence increases more rapidly than transmission, or if virulence also depends on the total amount of PGs produced, then more complex relationships between virulence and the MOI are predicted. Our results reveal that explicitly taking into account the distribution of parasite strains among hosts could help better understand the selective pressures faced by parasites at the population level.     

The importance of mechanisms for the evolution of cooperation

Studies aimed at explaining the evolution of phenotypic traits have often solely focused on fitness considerations, ignoring underlying mechanisms. In recent years, there has been an increasing call for integrating mechanistic perspectives in evolutionary considerations, but it is not clear whether and how mechanisms affect the course and outcome of evolution. To study this, we compare four mechanistic implementations of two well-studied models for the evolution of cooperation, the Iterated Prisoner''s Dilemma (IPD) game and the Iterated Snowdrift (ISD) game. Behavioural strategies are either implemented by a 1 : 1 genotype–phenotype mapping or by a simple neural network. Moreover, we consider two different scenarios for the effect of mutations. The same set of strategies is feasible in all four implementations, but the probability that a given strategy arises owing to mutation is largely dependent on the behavioural and genetic architecture. Our individual-based simulations show that this has major implications for the evolutionary outcome. In the ISD, different evolutionarily stable strategies are predominant in the four implementations, while in the IPD each implementation creates a characteristic dynamical pattern. As a consequence, the evolved average level of cooperation is also strongly dependent on the underlying mechanism. We argue that our findings are of general relevance for the evolution of social behaviour, pleading for the integration of a mechanistic perspective in models of social evolution.     

Perspective: repression of competition and the evolution of cooperation

Abstract Repression of competition within groups joins kin selection as the second major force in the history of life shaping the evolution of cooperation. When opportunities for competition against neighbors are limited within groups, individuals can increase their own success only by enhancing the efficiency and productivity of their group. Thus, characters that repress competition within groups promote cooperation and enhance group success. Leigh first expressed this idea in the context of fair meiosis, in which each chromosome has an equal chance of transmission via gametes. Randomized success means that each part of the genome can increase its own success only by enhancing the total number of progeny and thus increasing the success of the group. Alexander used this insight about repression of competition in fair meiosis to develop his theories for the evolution of human sociality. Alexander argued that human social structures spread when they repress competition within groups and promote successful group-against-group competition. Buss introduced a new example with his suggestion that metazoan success depended on repression of competition between cellular lineages. Maynard Smith synthesized different lines of thought on repression of competition. In this paper, I develop simple mathematical models to illustrate the main processes by which repression of competition evolves. With the concepts made clear, I then explain the history of the idea. I finish by summarizing many new developments in this subject and the most promising lines for future study.     

The evolution of cooperation and altruism--a general framework and a classification of models

One of the enduring puzzles in biology and the social sciences is the origin and persistence of intraspecific cooperation and altruism in humans and other species. Hundreds of theoretical models have been proposed and there is much confusion about the relationship between these models. To clarify the situation, we developed a synthetic conceptual framework that delineates the conditions necessary for the evolution of altruism and cooperation. We show that at least one of the four following conditions needs to be fulfilled: direct benefits to the focal individual performing a cooperative act; direct or indirect information allowing a better than random guess about whether a given individual will behave cooperatively in repeated reciprocal interactions; preferential interactions between related individuals; and genetic correlation between genes coding for altruism and phenotypic traits that can be identified. When one or more of these conditions are met, altruism or cooperation can evolve if the cost-to-benefit ratio of altruistic and cooperative acts is greater than a threshold value. The cost-to-benefit ratio can be altered by coercion, punishment and policing which therefore act as mechanisms facilitating the evolution of altruism and cooperation. All the models proposed so far are explicitly or implicitly built on these general principles, allowing us to classify them into four general categories.     

Correlational selection does not explain the evolution of a behavioural syndrome

Correlated suites of behaviours, or behavioural syndromes, appear to be widespread, and yet few studies have explored how they arise and are maintained. One possibility holds that correlational selection can generate and maintain behavioural syndrome if certain behavioural combinations enjoy greater fitness than other combinations. Here we test this correlational selection hypothesis by comparing behavioural syndrome structure with a multivariate fitness surface based on reproductive success of male water striders. We measured the structure of a behavioural syndrome including dispersal ability, exploration behaviour, latency to remount and sex recognition sensitivity in males. We then measured the relationship between these behaviours and mating success in a range of sex ratio environments. Despite the presence of some significant correlational selection, behavioural syndrome structure was not associated with correlational selection on behaviours. Although we cannot conclusively reject the correlational selection hypothesis, our evidence suggests that correlational selection and resulting linkage disequilibrium might not be responsible for maintaining the strong correlations between behaviours. Instead, we suggest alternative ways in which this behavioural syndrome may have arisen and outline the need for physiological and quantitative genetic tests of these suggestions.     

Evolutionary dynamics of n-player games played by relatives

One of the core concepts in social evolution theory is kin selection. Kin selection provides a perspective to understand how natural selection operates when genetically similar individuals are likely to interact. A family-structured population is an excellent example of this, where relatives are engaged in social interactions. Consequences of such social interactions are often described in game-theoretical frameworks, but there is a growing consensus that a naive inclusive fitness accounting with dyadic relatedness coefficients are of limited use when non-additive fitness effects are essential in those situations. Here, I provide a general framework to analyse multiplayer interactions among relatives. Two important results follow from my analysis. First, it is generally necessary to know the n-tuple genetic association of family members when n individuals are engaged in social interactions. However, as a second result, I found that, for a special class of games, we need only measures of lower-order genetic association to fully describe its evolutionary dynamics. I introduce the concept of degree of the game and show how this degree is related to the degree of genetic association.     

The evolution of altruism: Correlation,cost, and benefit

A simple and general criterion is derived for the evolution of altruism when individuals interact in pairs. It is argued that the treatment of this problem in kin selection theory and in game theory are special cases of this general criterion.My thanks to James Crow, Carter Denniston, Lee Dugarkin, David Wilson, and an anonymous referee of this journal for helpful discussion.     

Hamilton's rule and the causes of social evolution

Hamilton''s rule is a central theorem of inclusive fitness (kin selection) theory and predicts that social behaviour evolves under specific combinations of relatedness, benefit and cost. This review provides evidence for Hamilton''s rule by presenting novel syntheses of results from two kinds of study in diverse taxa, including cooperatively breeding birds and mammals and eusocial insects. These are, first, studies that empirically parametrize Hamilton''s rule in natural populations and, second, comparative phylogenetic analyses of the genetic, life-history and ecological correlates of sociality. Studies parametrizing Hamilton''s rule are not rare and demonstrate quantitatively that (i) altruism (net loss of direct fitness) occurs even when sociality is facultative, (ii) in most cases, altruism is under positive selection via indirect fitness benefits that exceed direct fitness costs and (iii) social behaviour commonly generates indirect benefits by enhancing the productivity or survivorship of kin. Comparative phylogenetic analyses show that cooperative breeding and eusociality are promoted by (i) high relatedness and monogamy and, potentially, by (ii) life-history factors facilitating family structure and high benefits of helping and (iii) ecological factors generating low costs of social behaviour. Overall, the focal studies strongly confirm the predictions of Hamilton''s rule regarding conditions for social evolution and their causes.     

Genome-wide signatures of population bottlenecks and diversifying selection in European wolves

Genomic resources developed for domesticated species provide powerful tools for studying the evolutionary history of their wild relatives. Here we use 61K single-nucleotide polymorphisms (SNPs) evenly spaced throughout the canine nuclear genome to analyse evolutionary relationships among the three largest European populations of grey wolves in comparison with other populations worldwide, and investigate genome-wide effects of demographic bottlenecks and signatures of selection. European wolves have a discontinuous range, with large and connected populations in Eastern Europe and relatively smaller, isolated populations in Italy and the Iberian Peninsula. Our results suggest a continuous decline in wolf numbers in Europe since the Late Pleistocene, and long-term isolation and bottlenecks in the Italian and Iberian populations following their divergence from the Eastern European population. The Italian and Iberian populations have low genetic variability and high linkage disequilibrium, but relatively few autozygous segments across the genome. This last characteristic clearly distinguishes them from populations that underwent recent drastic demographic declines or founder events, and implies long-term bottlenecks in these two populations. Although genetic drift due to spatial isolation and bottlenecks seems to be a major evolutionary force diversifying the European populations, we detected 35 loci that are putatively under diversifying selection. Two of these loci flank the canine platelet-derived growth factor gene, which affects bone growth and may influence differences in body size between wolf populations. This study demonstrates the power of population genomics for identifying genetic signals of demographic bottlenecks and detecting signatures of directional selection in bottlenecked populations, despite their low background variability.     

Multilevel selection: the evolution of cooperation in non-kin groups

Hamiltons (1964a, 1964b) landmark papers are rightly recognized as the formal basis for our understanding of the evolution of altruistic traits. However, Hamiltons equation as he originally expressed it is simplistic. A genetically oriented approach to studying multilevel selection can provide insights into how the terminology and assumptions used by Hamilton can be generalized. Using contextual analysis I demonstrated that Hamiltons rule actually embodies three distinct processes, group selection, individual selection, and transmission genetics or heritability. Whether an altruistic trait will evolve depends the balance of all of these factors. The genetical approach, and particularly, contextual analysis provides a means of separating these factors and examining them one at a time. Perhaps the greatest issue with Hamiltons equation is the interpretation of r. Hamilton (1964a) interpreted this as relatedness. In this paper I show that what Hamilton called relatedness is more generally interpreted as the proportion for variance among groups, and that many processes in addition to relatedness can increase the variance among groups. I also show that the evolution of an altruistic trait is driven by the ratio of the heritability at the group level to the heritability at the individual level. Under some circumstances this ratio can be greater than 1. In this situation altruism can evolve even if selection favoring selfish behavior is stronger than selection favoring altruism.     

The effect of dispersal and neighbourhood in games of cooperation

The prisoner's dilemma (PD) and the snowdrift (SD) games are paradigmatic tools to investigate the origin of cooperation. Whereas spatial structure (e.g. nonrandom spatial distribution of strategies) present in the spatially explicit models facilitates the emergence of cooperation in the PD game, recent investigations have suggested that spatial structure can be unfavourable for cooperation in the SD game. The frequency of cooperators in a spatially explicit SD game can be lower than it would be in an infinitely large well-mixed population. However, the source of this effect cannot be identified with certainty as spatially explicit games differ from well-mixed games in two aspects: (i) they introduce spatial correlations, (ii) and limited neighbourhood. Here we extend earlier investigations to identify the source of this effect, and thus accordingly we study a spatially explicit version of the PD and SD games with varying degrees of dispersal and neighbourhood size. It was found that dispersal favours selfish individuals in both games. We calculated the frequency of cooperators at strong dispersal limit, which in concordance with the numerical results shows that it is the short range of interactions (i.e. limited neighbourhood) and not spatial correlations that decreases the frequency of cooperators in spatially explicit models of populations. Our results demonstrate that spatial correlations are always beneficial to cooperators in both the PD and SD games. We explain the opposite effect of dispersal and neighbourhood structure, and discuss the relevance of distinguishing the two effects in general.     

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an ‘asocial’ phenotype with solitary female nests and a ‘social’ phenotype with multi‐female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half‐siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

The genetic diversity and population structures of indigenous pig breeds in Zhejiang Province revealed by GGRS sequencing

Chinese indigenous pigs in Zhejiang Province are well known for their high fecundity. In order to verify breed subdivision at the genomic level, we investigated genetic diversity and population structure of seven breeds and made comparisons with three Western pig breeds using next‐generation sequencing data. Parameters obtained from allelic richness and proportion of polymorphic markers indicated that the genetic diversity of the Chinese indigenous pigs was higher than that of the Western pigs, with the highest and lowest values found in the Chaluand and the Landrace pigs respectively. Both neighbor‐joining tree and principal components analysis could distinguish breeds from one another and structure analysis showed less differentiation among Western pigs than among the Chinese pigs. The average linkage disequilibrium decay over distance was significantly less in the Chinese pigs compared with the Western pigs, ranging from 188.2 to 280.6 kb for the Chinese pigs and 680.3 to 752.8 kb for the Western breeds and showing an average r² threshold value of 0.3. Results obtained from high‐density SNP comparison over the whole genome on genetic diversity and population structure were in agreement with the current breed classification of the pigs in Zhejiang Province. More importantly, the results presented here advances our current understanding of the genomic biology of Chinese indigenous pigs in Zhejiang Province and allows for implementation of conservation strategies in additional breeds.     

Genome-wide population structure and evolutionary history of the Frizarta dairy sheep

In the present study, we used genomic data, generated with a medium density single nucleotide polymorphisms (SNP) array, to acquire more information on the population structure and evolutionary history of the synthetic Frizarta dairy sheep. First, two typical measures of linkage disequilibrium (LD) were estimated at various physical distances that were then used to make inferences on the effective population size at key past time points. Population structure was also assessed by both multidimensional scaling analysis and k-means clustering on the distance matrix obtained from the animals’ genomic relationships. The Wright’s fixation F_ST index was also employed to assess herds’ genetic homogeneity and to indirectly estimate past migration rates. The Wright’s fixation F_IS index and genomic inbreeding coefficients based on the genomic relationship matrix as well as on runs of homozygosity were also estimated. The Frizarta breed displays relatively low LD levels with r² and |Dʹ| equal to 0.18 and 0.50, respectively, at an average inter-marker distance of 31 kb. Linkage disequilibrium decayed rapidly by distance and persisted over just a few thousand base pairs. Rate of LD decay (β) varied widely among the 26 autosomes with larger values estimated for shorter chromosomes (e.g. β=0.057, for OAR6) and smaller values for longer ones (e.g. β=0.022, for OAR2). The inferred effective population size at the beginning of the breed’s formation was as high as 549, was then reduced to 463 in 1981 (end of the breed’s formation) and further declined to 187, one generation ago. Multidimensional scaling analysis and k-means clustering suggested a genetically homogenous population, F_ST estimates indicated relatively low genetic differentiation between herds, whereas a heat map of the animals’ genomic kinship relationships revealed a stratified population, at a herd level. Estimates of genomic inbreeding coefficients suggested that most recent parental relatedness may have been a major determinant of the current effective population size. A denser than the 50k SNP panel may be more beneficial when performing genome wide association studies in the breed.     

The extent of linkage disequilibrium in a large cattle population of western Africa and its consequences for association studies

Several previous studies concluded that linkage disequilibrium (LD) in livestock populations from developed countries originated from the impact of strong selection. Here, we assessed the extent of LD in a cattle population from western Africa that was bred in an extensive farming system. The analyses were performed on 363 individuals in a Bos indicus x Bos taurus population using 42 microsatellite markers on BTA04, BTA07 and BTA13. A high level of expected heterozygosity (0.71), a high mean number of alleles per locus (9.7) and a mild shift in Hardy-Weinberg equilibrium were found. Linkage disequilibrium extended over shorter distances than what has been observed in cattle from developed countries. Effective population size was assessed using two methods; both methods produced large values: 1388 when considering heterozygosity (assuming a mutation rate of 10(-3)) and 2344 when considering LD on whole linkage groups (assuming a constant population size over generations). However, analysing the decay of LD as a function of marker spacing indicated a decreasing trend in effective population size over generations. This decrease could be explained by increasing selective pressure and/or by an admixture process. Finally, LD extended over small distances, which suggested that whole-genome scans will require a large number of markers. However, association studies using such populations will be effective.