Ecology and multilevel selection explain aggression in spider colonies

Progress in sociobiology continues to be hindered by abstract debates over methodology and the relative importance of within‐group vs. between‐group selection. We need concrete biological examples to ground discussions in empirical data. Recent work argued that the levels of aggression in social spider colonies are explained by group‐level adaptation. Here, we examine this conclusion using models that incorporate ecological detail while remaining consistent with kin‐ and multilevel selection frameworks. We show that although levels of aggression are driven, in part, by between‐group selection, incorporating universal within‐group competition provides a striking fit to the data that is inconsistent with pure group‐level adaptation. Instead, our analyses suggest that aggression is favoured primarily as a selfish strategy to compete for resources, despite causing lower group foraging efficiency or higher risk of group extinction. We argue that sociobiology will benefit from a pluralistic approach and stronger links between ecologically informed models and data.     

Reviving the superorganism

Individuals become functionally organized to survive and reproduce in their environments by the process of natural selection. The question of whether larger units such as groups and communities can possess similar properties of functional organization, and therefore be regarded as "superorganisms", has a long history in biological thought. Modern evolutionary biology has rejected the concept of superorganisms, explaining virtually all adaptations at the individual or gene level. We criticize the modern literature on three counts. First, individual selection in its strong form is founded on a logical contradiction, in which genes-in-individuals are treated differently than individuals-in-groups or species-in-communities. Imposing consistency clearly shows that groups and communities can be organisms in the same sense that individuals are. Furthermore, superorganisms are more than just a theoretical possibility and actually exist in nature. Second, the view that genes are the "ultimate" unit of selection is irrelevant to the question of functional organization. Third, modern evolutionary biology includes numerous conceptual frameworks for analyzing evolution in structured populations. These frameworks should be regarded as different ways of analyzing a common process which, to be correct, must converge on the same conclusions. Unfortunately, evolutionists frequently regard them as competing theories that invoke different mechanisms, such that if one is "right" the others must be "wrong". The problem of multiple frameworks is aggravated by the fact that major terms, such as "units of selection", are defined differently within each framework, yet many evolutionists who use one framework to argue against another assume shared meanings. We suggest that focusing on the concept of organism will help dispell this fog of semantic confusion, allowing all frameworks to converge on the same conclusions regarding units of functional organization.     

Sociobiology and Creationism: Two Ethnosociologies of American Culture

One of the most important motifs in mythology is the animal-human distinction. The relationship between humans and nonhuman animals is also a major concern of both human sociobiology and "scientific" creationism. In this paper, we suggest that sociobiology and creationism function as ethnosociologies of American society and that neither can be completely understood until they are related to each other and to the key symbols of American culture. We argue that sociobiology and creationism are comments on the secular world view of American culture and exist as transformations of one another.     

Group Selection as Behavioral Adaptation to Systematic Risk

Despite many compelling applications in economics, sociobiology, and evolutionary psychology, group selection is still one of the most hotly contested ideas in evolutionary biology. Here we propose a simple evolutionary model of behavior and show that what appears to be group selection may, in fact, simply be the consequence of natural selection occurring in stochastic environments with reproductive risks that are correlated across individuals. Those individuals with highly correlated risks will appear to form “groups”, even if their actions are, in fact, totally autonomous, mindless, and, prior to selection, uniformly randomly distributed in the population. This framework implies that a separate theory of group selection is not strictly necessary to explain observed phenomena such as altruism and cooperation. At the same time, it shows that the notion of group selection does captures a unique aspect of evolution—selection with correlated reproductive risk–that may be sufficiently widespread to warrant a separate term for the phenomenon.     

Sociobiology and philosophical ethics: Narrowing the gap

Though there are good reasons for thinking that sociobiology is capable of contributing to the solution of one of the central problems of philosophical ethics, the problem of other-benefitting behaviour, philosophers have not welcomed the new discipline with open arms. This has been so for three reasons: it is said that sociobiology studies behaviour, and not its proximal causes, that sociobiology tells us about the evolutionary history of behaviour and not about its justification, and that sociobiology prescribes morally unacceptable ways of acting. I argue that the first of the objections is simply mistaken, and that when we realize this, the second loses some of its force. I also argue in favour of atwo-factor model of motivation with reason and the emotions engaged in a dialogue with each other concerning the morally relevant features of a given situation. This two-factor model helps us overcome the third objection above, namely to the morally unacceptable dictates of sociobiology, and also to weaken claims that sociobiology is committed to a lack of freedom of the will in human action. Broadly speaking, my argument suggest that the ethical framework most suited to accommodating sociobiological insights into human motivation is an Aristotelian structure.     

The Development of Sociobiology in Relation to Animal Behavior Studies, 1946–1975

This paper aims at bridging a gap between the history of American animal behavior studies and the history of sociobiology. In the post-war period, ecology, comparative psychology and ethology were all investigating animal societies, using different approaches ranging from fieldwork to laboratory studies. We argue that this disunity in “practices of place” (Kohler, Robert E. Landscapes & Labscapes: Exploring the Lab-Field Border in Biology. Chicago: University of Chicago Press, 2002) explains the attempts of dialogue between those three fields and early calls for unity through “sociobiology” by J. Paul Scott. In turn, tensions between the naturalist tradition and the rising reductionist approach in biology provide an original background for a history of Edward Wilson’s own version of sociobiology, much beyond the William Hamilton’s papers (Journal of Theoretical Biology 7: 1–16, 17–52, 1964) usually considered as its key antecedent. Naturalists were in a defensive position in the geography of the fields studying animal behavior, and in reaction were a driving force behind the various projects of synthesis called “sociobiology”.     

Culture and sociobiology

Sociobiological concepts are easily misapplied to human behavior because the latter is culturally as well as biologically organized. Because biological and cultural evolution are two linked but conceptually distinct processes, sociobiology is more readily applied to the evolution of cultural capacity than to contemporary cultural behavior. The extent to which the latter is consistent with sociobiological expectation must be determined empirically, although there are theoretical grounds for predicting a limited degree of concordance . [sociobiology, culture, evolution, reductionism, biosocial anthropology]     

The cooperative amoeba: Dictyostelium as a model for social evolution

Social interactions, including cooperation and altruism, are characteristic of numerous species, but many aspects of the evolution, ecology and genetics of social behavior remain unclear. The microbial soil amoeba Dictyostelium discoideum is a model system for the study of social evolution and provides insights into the nature of social cooperation and its genetic basis. This species exhibits altruism during both asexual and sexual cycles of its life history, and recent studies have uncovered several possible genetic mechanisms associated with kin discrimination and cheating behavior during asexual fruiting-body formation. By contrast, the molecular and evolutionary mechanisms that underlie sexual macrocyst formation remain largely enigmatic. D. discoideum, given its utility in molecular genetic studies, should continue to help us address these and other relevant questions in sociobiology, and thereby contribute to a coherent theoretical framework for the nature of social cooperation.     

Does Biology Constrain Culture?

Most social scientists would agree that the capacity for human culture was probably fashioned by natural selection, but they disagree about the implications of this supposition. Some believe that natural selection imposes important constraints on the ways in which culture can vary, while others believe that any such constraints must be negligible. This article employs a "thought experiment" to demonstrate that neither of these positions can be justified by appeal to general properties of culture or of evolution. Natural selection can produce mechanisms of cultural transmission that are neither adaptive nor consistent with the predictions of acultural evolutionary models (those ignoring cultural evolution). On the other hand, natural selection can also produce mechanisms of cultural transmission that are highly consistent with acultural models. Thus, neither side of the sociobiology debate is justified in dismissing the arguments of the other. Natural selection may impose significant constraints on some human behaviors, but negligible constraints on others. Models of simultaneous genetic/cultural evolution will be useful in identifying domains in which acultural evolutionary models are, and are not, likely to be useful.     

The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions

The diversity of social interactions between sexual partners has long captivated biologists, and its evolution has been interpreted largely in terms of 'direct fitness' pay-offs to partners and their descendants. Inter-sexual interactions also have 'indirect effects' by affecting the fitness of relatives, with important consequences for inclusive fitness. However, inclusive fitness arguments have received limited consideration in this context, and definitions of 'direct' and 'indirect' fitness effects in this field are often inconsistent with those of inclusive fitness theory. Here, we use a sociobiology approach based on inclusive fitness theory to distinguish between direct and indirect fitness effects. We first consider direct effects: we review how competition leads to sexual conflict, and discuss the conditions under which repression of competition fosters sexual mutualism. We then clarify indirect effects, and show that greenbeard effects, kin recognition and population viscosity can all lead to episodes of indirect selection on sexual interactions creating potential for sexual altruism and spite. We argue that the integration of direct and indirect fitness effects within a sociobiology approach enables us to consider a more diverse spectrum of evolutionary outcomes of sexual interactions, and may help resolving current debates over sexual selection and sexual conflict.     

Inclusive fitness and the sociobiology of the genome

Inclusive fitness theory provides conditions for the evolutionary success of a gene. These conditions ensure that the gene is selfish in the sense of Dawkins (The selfish gene, Oxford University Press, Oxford, 1976): genes do not and cannot sacrifice their own fitness on behalf of the reproductive population. Therefore, while natural selection explains the appearance of design in the living world (Dawkins in The blind watchmaker: why the evidence of evolution reveals a universe without design, W. W. Norton, New York, 1996), inclusive fitness theory does not explain how. Indeed, Hamilton’s rule is equally compatible with the evolutionary success of prosocial altruistic genes and antisocial predatory genes, whereas only the former, which account for the appearance of design, predominate in successful organisms. Inclusive fitness theory, however, permits a formulation of the central problem of sociobiology in a particularly poignant form: how do interactions among loci induce utterly selfish genes to collaborate, or to predispose their carriers to collaborate, in promoting the fitness of their carriers? Inclusive fitness theory, because it abstracts from synergistic interactions among loci, does not answer this question. Fitness-enhancing collaboration among loci in the genome of a reproductive population requires suppressing alleles that decrease, and promoting alleles that increase the fitness of its carriers. Suppression and promotion are effected by regulatory networks of genes, each of which is itself utterly selfish. This implies that genes, and a fortiori individuals in a social species, do not maximize inclusive fitness but rather interact strategically in complex ways. It is the task of sociobiology to model these complex interactions.     

Antagonistic multilevel selection on size and architecture in variable density settings

In some ecological settings, an individual's fitness depends on both its own phenotype (individual-level selection) as well as the phenotype of the individuals with which it interacts (group-level selection). Using contextual analysis to measure multilevel selection in experimental stands of Arabidopsis thaliana, we detected significant linear selection that reversed across individual versus group levels for two composite phenotypic traits, "size" and "elongation." In both cases, selection at the individual level acted to increase values of these traits, presumably due to their positive effect on resource acquisition. Group selection favored decreased values of the same traits. Nonlinear selection was weak but significant in several cases, including stabilizing selection on developmental rate; individuals with very rapid development likely had lower than average fitness due to their reduced resource level at reproduction, while very delayed reproduction may have resulted in lower fitness if prolonged competition for resources reduced overall environmental quality and fitness of all individuals in a group. Under this scenario, stabilizing selection on individual traits is evidence of selection at the group level. Significant density-dependent selection suggests that a threshold density must be reached before group selection acts. Below this threshold, selection at the individual level affects phenotypic evolution more strongly than group selection. A second experiment measured multilevel selection in progeny stands of the original experimental plants. Multilevel selection again acted antagonistically on a composite trait that included size and elongation as well as on an architectural trait, branch production. The magnitude of individual versus group selection was relatively similar in the progeny generation, and the observed balance of individual versus group selection across densities is generally consistent with the hypotheses that multilevel selection can contribute to phenotypic evolution and to important demographic phenomena, including soft selection and the "law of constant yield."     

Science as Ideology: The Rejection and Reception of Sociobiology in China

The spread of sociobiology in China is not simply an internal event in the development of science. From the day it was introduced to China, its destiny was closely bound up with the development and change of Chinese society. Although it did not create as great disturbance as in America, it did have a significant impact in academic circles. However, scholars have paid little attention to these historical events. Today, sociobiology seems outdated and Wilson's grand agenda seems to have faded with the passing of time, but the mark that he made on the history of science is still striking. A review of the process of reception of sociobiology in China is helpful for understanding this theory as well as the society of China.     

Inclusive Fitness and Human Family Structure

The implications of sociobiology, and especially of "inclusive fitness" or "kin-selection" theory, to human family structures are explored. Kin-selection theory provides a model to formulate testable hypotheses predicting cooperation and conflict for categories of kinsmen; it also suggests an alternative way of looking at incest, endogamy, exogamy, rule of descent, and type of marriage in terms of such biological concepts as mating strategies, inclusive fitness, parental investment, and sexual dimorphism and bimaturism. [sociobiology, kin-selection theory, inclusive fitness, family structure, marriage]     

Religion and Social Structure in The Division of Labor

The article offers a thoroughgoing reinterpretation of The Division of Labor, focusing on the six-stage theory of sociocultural change that lies in the background of Durkheim's well-known contrast between the ideal types of mechanical and organic solidarity. Durkheim's characterization of each stage is described in terms of its structural-functional differentiation and religious unity. The Division's evolutionary theory, which underlies much of Durkheim's mature work, is criticized for its dated ethnographic evidence, and contrasted with alternative evolutionary proposals, including that of sociobiology.     

Reproductive skew in cooperative breeding: Environmental variability,antagonistic selection,choice, and control

A multitude of factors may determine reproductive skew among cooperative breeders. One explanation, derived from inclusive fitness theory, is that groups can partition reproduction such that subordinates do at least as well as noncooperative solitary individuals. The majority of recent data, however, fails to support this prediction; possibly because inclusive fitness models cannot easily incorporate multiple factors simultaneously to predict skew. Notable omissions are antagonistic selection (across generations, genes will be in both dominant and subordinate bodies), constraints on the number of sites suitable for successful reproduction, choice in which group an individual might join, and within‐group control or suppression of competition. All of these factors and more are explored through agent‐based evolutionary simulations. The results suggest the primary drivers for the initial evolution of cooperative breeding may be a combination of limited suitable sites, choice across those sites, and parental manipulation of offspring into helping roles. Antagonistic selection may be important when subordinates are more frequent than dominants. Kinship matters, but its main effect may be in offspring being available for manipulation while unrelated individuals are not. The greater flexibility of evolutionary simulations allows the incorporation of species‐specific life histories and ecological constraints to better predict sociobiology.     

What can microbial genetics teach sociobiology?

Progress in our understanding of sociobiology has occurred with little knowledge of the genetic mechanisms that underlie social traits. However, several recent studies have described microbial genes that affect social traits, thereby bringing genetics to sociobiology. A key finding is that simple genetic changes can have marked social consequences, and mutations that affect cheating and recognition behaviors have been discovered. The study of these mutants confirms a central theoretical prediction of social evolution: that genetic relatedness promotes cooperation. Microbial genetics also provides an important new perspective: that the genome-to-phenome mapping of social organisms might be organized to constrain the evolution of social cheaters. This constraint can occur both through pleiotropic genes that link cheating to a personal cost and through the existence of phoenix genes, which rescue cooperative systems from selfish and destructive strategies. These new insights show the power of studying microorganisms to improve our understanding of the evolution of cooperation.     

HOW TO MEASURE INDIRECT GENETIC EFFECTS: THE CONGRUENCE OF TRAIT-BASED AND VARIANCE-PARTITIONING APPROACHES

Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Ψ. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate Ψ via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.     

A general review of competition genetic effects with an emphasis on swine breeding

A review of previous studies is presented on estimates of genetic parameters and responses to selection with traditional breeding approaches, on correlations between agonistic behavior and growth performance, and on theoretical frameworks for selection incorporating interactions among individuals and on practical methods for incorporating competition effects in breeding programs.     

Transactional skew and assured fitness return models fail to predict patterns of cooperation in wasps

Cooperative breeders often exhibit reproductive skew, where dominant individuals reproduce more than subordinates. Two approaches derived from Hamilton's inclusive fitness model predict when subordinate behavior is favored over living solitarily. The assured fitness return (AFR) model predicts that subordinates help when they are highly likely to gain immediate indirect fitness. Transactional skew models predict dominants and subordinates "agree" on a level of reproductive skew that induces subordinates to join groups. We show the AFR model to be a special case of transactional skew models that assumes no direct reproduction by subordinates. We use data from 11 populations of four wasp species (Polistes, Liostenogaster) as a test of whether transactional frameworks suffice to predict when subordinate behavior should be observed in general and the specific level of skew observed in cooperative groups. The general prediction is supported; in 10 of 11 cases, transactional models correctly predict presence or absence of cooperation. In contrast, the specific prediction is not consistent with the data. Where cooperation occurs, the model accurately predicts highly biased reproductive skew between full sisters. However, the model also predicts that distantly related or unrelated females should cooperate with low skew. This prediction fails: cooperation with high skew is the observed norm. Neither the generalized transactional model nor the special-case AFR model can explain this significant feature of wasp sociobiology. Alternative, nontransactional hypotheses such as parental manipulation and kin recognition errors are discussed.