Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

Tamarins: Alpha female,queen bee or white rat?

The saddleback tamarin (Saguinus fuscicollis)combines a number of behavioral and physiological attributes which seem to violate “rules” of ethology. Of particular interest is the combination of facultative polyandry and high paternal investment. The social organization and breeding system of the tamarin also appear to combine reproductive restraint with an extremely high reproductive potential. These paradoxes may be resolved by noting that the combination of ecological circumstances and breeding systems has produced a species of limited genetic variability. Inclusive fitness is an important factor in situations of low genetic variability and may explain these apparent paradoxes.     

Models of social evolution: can we do better to predict ‘who helps whom to achieve what’?

Models of social evolution and the evolution of helping have been classified in numerous ways. Two categorical differences have, however, escaped attention in the field. Models tend not to justify why they use a particular assumption structure about who helps whom: a large number of authors model peer-to-peer cooperation of essentially identical individuals, probably for reasons of mathematical convenience; others are inspired by particular cooperatively breeding species, and tend to assume unidirectional help where subordinates help a dominant breed more efficiently. Choices regarding what the help achieves (i.e. which life-history trait of the helped individual is improved) are similarly made without much comment: fecundity benefits are much more commonly modelled than survival enhancements, despite evidence that these may interact when the helped individual can perform life-history reallocations (load-lightening and related phenomena). We review our current theoretical understanding of effects revealed when explicitly asking ‘who helps whom to achieve what’, from models of mutual aid in partnerships to the very few models that explicitly contrast the strength of selection to help enhance another individual''s fecundity or survival. As a result of idiosyncratic modelling choices in contemporary literature, including the varying degree to which demographic consequences are made explicit, there is surprisingly little agreement on what types of help are predicted to evolve most easily. We outline promising future directions to fill this gap.     

There is no fitness but fitness,and the lineage is its bearer

Inclusive fitness has been the cornerstone of social evolution theory for more than a half-century and has matured as a mathematical theory in the past 20 years. Yet surprisingly for a theory so central to an entire field, some of its connections to evolutionary theory more broadly remain contentious or underappreciated. In this paper, we aim to emphasize the connection between inclusive fitness and modern evolutionary theory through the following fact: inclusive fitness is simply classical Darwinian fitness, averaged over social, environmental and demographic states that members of a gene lineage experience. Therefore, inclusive fitness is neither a generalization of classical fitness, nor does it belong exclusively to the individual. Rather, the lineage perspective emphasizes that evolutionary success is determined by the effect of selection on all biological and environmental contexts that a lineage may experience. We argue that this understanding of inclusive fitness based on gene lineages provides the most illuminating and accurate picture and avoids pitfalls in interpretation and empirical applications of inclusive fitness theory.     

Bi‐parental vs. cooperative breeding in a passerine: fitness‐maximizing strategies of males in response to risk of extra‐pair paternity?

In socially monogamous species, males that risk cuckoldry more than others might gain inclusive fitness by yielding paternity to relatives. We tested this prediction in the Tibetan ground tit Pseudopodoces humilis , an unusual facultative cooperative breeder wherein most helpers (87% males) join a mated pair shortly before clutch completion. Extra-pair paternity among bi-parental broods occurred less often (26% of broods, 9% of young) compared with cooperative broods (68%, 25%). In the former, most extra-pair sires (88%) were pair breeders unrelated to the cuckolded males, whereas in the latter, sires (87%) were mainly helpers related to the dominant males. Brood productivity did not differ between the bi-parental and cooperative breeders, but helpers' partitioning over group paternity reduced the realized reproductive success of helped males. After taking inclusive fitness into account, however, there was no difference in success of dominant males between the two social systems. One possible explanation for the differences in the rates of cuckoldry in the two systems was body size, because pair-bond males in bi-parental situations were significantly larger than those in cooperative ones. We propose two alternative strategies for males to maximize fitness: breed as a pair if large to avoid cuckoldry from helpers, or breed cooperatively if small but compromise some paternity to relatives. Our results provide an unusual route to the incidence of cooperative groups, based on constraints imposed by low competitive ability of breeding males rather than some external ecological or demographic factors.     

Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp

Inclusive fitness theory predicts that in colonies of social Hymenoptera headed by a multiple‐mated queen, workers should benefit from policing eggs laid by other workers. Foster & Ratnieks provided evidence that in the vespine wasp Dolichovespula saxonica, workers police other workers’ eggs only in colonies headed by a multiple‐mated queen, but not in those headed by a single‐mated one. This conclusion, however, was based on a relatively small sample size, and the original study did not control for possible confounding variables such as the seasonal colony progression of the nests. Our aim, therefore, was to reinvestigate whether or not facultative worker policing occurs in D. saxonica. Remarkably, our data show that in the studied Danish population, there was no correlation between worker–worker relatedness and the percentage of worker‐derived males. In addition, we show that variability in cuticular hydrocarbon profiles among the workers did not significantly correlate with relatedness and that workers therefore probably did not have sufficient information on queen mating frequency from the workers’ cuticular hydrocarbon profiles. Hence, there was no evidence that workers facultatively policed other workers’ eggs in response to queen mating frequency. Nevertheless, our data do show that the seasonal progression of the nest and the location in which the males were reared both explain the patterns of worker reproduction found. Overall, our results suggest that the earlier evidence for facultative worker policing in D. saxonica may have been caused by accidental correlations with certain confounding variables, or, alternatively, that there are large interpopulation differences in the expression of worker policing.     

How to distinguish altruism from spite (and why we should bother)

Social behaviour is often described as altruistic, spiteful, selfish or mutually beneficial. These terms are appealing, but it has not always been clear how they are defined and what purpose they serve. Here, I show that the distinctions among them arise from the ways in which fitness is partitioned: none can be drawn when the fitness consequences of an action are wholly aggregated, but they manifest clearly when the consequences are partitioned into primary and secondary (neighbourhood) effects. I argue that the primary interaction is the principal source of adaptive design, because (i) it is this interaction that determines the fit of an adaptation and (ii) it is the actor and primary recipients whom an adaptation foremost affects. The categories of social action are thus instrumental to any account of evolved function.     

Altruism in viscous populations — an inclusive fitness model

Summary A viscous population (Hamilton, 1964) is one in which the movement of organisms from their place of birth is relatively slow. This viscosity has two important effects: one is that local interactions tend to be among relatives, and the other is that competition for resources tends to be among relatives. The first effect tends to promote and the second to oppose the evolution of altruistic behaviour. In a simulation model of Wilsonet al. (1992) these two factors appear to exactly balance one another, thus opposing the evolution of local altruistic behaviour. Here I show, with an inclusive fitness model, that the same result holds in a patchstructured population.     

Decompositions of Price’s formula in an inhomogeneous population structure

The central tool for the study of allele frequency change due to selection is the remarkably simple but powerful formula of Price [Nature 227 (1970) 520] . Here, I provide what might be called a structural analysis of this formula. The formula essentially accumulates the average allele frequency change over many instances of a fitness‐determining interaction, but there are different ways of organizing this average and these lead to quite different computational algorithms. I present three of these: an analysis by population state, an analysis by recipient and an analysis by actor. A comparison of these can lead to a heightened understanding of the different factors behind selective allele frequency change. In particular, I pay attention to the effects of structural inhomogeneity on reproductive value (RV) and emphasize that Price’s formula measures RV‐weighted allele frequency change. I examine in detail a simple example as a crucial way of cementing the different theoretical pathways. My aim was to produce a simple transparent presentation and therefore I work with a simple population structure and have omitted a number of technical details that are found elsewhere.     

Kin selection, quorum sensing and virulence in pathogenic bacteria

Bacterial growth and virulence often depends upon the cooperative release of extracellular factors excreted in response to quorum sensing (QS). We carried out an in vivo selection experiment in mice to examine how QS evolves in response to variation in relatedness (strain diversity), and the consequences for virulence. We started our experiment with two bacterial strains: a wild-type that both produces and responds to QS signal molecules, and a lasR (signal-blind) mutant that does not release extracellular factors in response to signal. We found that: (i) QS leads to greater growth within hosts; (ii) high relatedness favours the QS wild-type; and (iii) low relatedness favours the lasR mutant. Relatedness matters in our experiment because, at relatively low relatedness, the lasR mutant is able to exploit the extracellular factors produced by the cells that respond to QS, and hence increase in frequency. Furthermore, our results suggest that because a higher relatedness favours cooperative QS, and hence leads to higher growth, this will also lead to a higher virulence, giving a relationship between relatedness and virulence that is in the opposite direction to that usually predicted by virulence theory.     

First principles of Hamiltonian medicine

We introduce the field of Hamiltonian medicine, which centres on the roles of genetic relatedness in human health and disease. Hamiltonian medicine represents the application of basic social-evolution theory, for interactions involving kinship, to core issues in medicine such as pathogens, cancer, optimal growth and mental illness. It encompasses three domains, which involve conflict and cooperation between: (i) microbes or cancer cells, within humans, (ii) genes expressed in humans, (iii) human individuals. A set of six core principles, based on these domains and their interfaces, serves to conceptually organize the field, and contextualize illustrative examples. The primary usefulness of Hamiltonian medicine is that, like Darwinian medicine more generally, it provides novel insights into what data will be productive to collect, to address important clinical and public health problems. Our synthesis of this nascent field is intended predominantly for evolutionary and behavioural biologists who aspire to address questions directly relevant to human health and disease.     

Social semantics: how useful has group selection been?

In our social semantics review (J. Evol. Biol., 2007, 415–432), we discussed some of the misconceptions and sources of confusion associated with group selection. Wilson (2007, this issue) claims that we made three errors regarding group selection. Here, we aim to expand upon the relevant points from our review in order to refute this claim. The last 45 years of research provide clear evidence of the relative use of the kin and group selection approaches. Kin selection methodologies are more tractable, allowing the construction of models that can be applied more easily to specific biological examples, including those chosen by Wilson to illustrate the utility of the group selection approach. In contrast, the group selection approach is not only less useful, but also appears to frequently have negative consequences by fostering confusion that leads to wasted effort. More generally, kin selection theory allows the construction of a unified conceptual overview that can be applied across all taxa, whereas there is no formal theory of group selection.