Inclusive Fitness Theory Research Articles

Social Evolution: The Decline and Fall of Genetic Kin Recognition

Animals should benefit from the ability to recognise their kin, yet curiously this faculty is often absent. New theory confirms that genetic kin recognition is inherently unstable, explaining its rarity.

Historical change and evolutionary theory

Despite advances in fields like genetics, evolutionary psychology, and human behavior and evolution--which generally focus on individual or small group behavior from a biological perspective--evolutionary biology has made little impact on studies of political change and social history. Theories of natural selection often seem inapplicable to human history because our social behavior is embedded in language (which makes possible the concepts of time and social identity on which what we call "history" depends). Peter Corning's Holistic Darwinism reconceptualizes evolutionary biology, making it possible to go beyond the barriers separating the social and natural sciences. Corning focuses on two primary processes: "synergy" (complex multivariate interactions at multiple levels between a species and its environment) and "cybernetics" (the information systems permitting communication between individuals and groups over time). Combining this frame of reference with inclusive fitness theory, it is possible to answer the most important (and puzzling) question in human history: How did a species that lived for millennia in hunter-gatherer bands form centralized states governing large populations of non-kin (including multi-ethnic empires as well as modern nation-states)? The fragility and contemporary ethnic violence in Kenya and the Congo should suffice as evidence that these issues need to be taken seriously. To explain the rise and fall of states as well as changes in human laws and customs--the core of historical research--it is essential to show how the provision of collective goods can overcome the challenge of self-interest and free-riding in some instances, yet fail to do so in others. To this end, it is now possible to consider how a state providing public goods can--under circumstances that often include effective leadership--contribute to enhanced inclusive fitness of virtually all its members. Because social behavior needs to adapt to ecology, but ecological systems are constantly transformed by human technology and social behavior, multilevel evolutionary processes can explain two central features of human history: the rise, transformations, and ultimate fall of centralized governments (the "stuff" of history); and the biological uniqueness of Homo sapiens as the mammalian species that colonized--and became top carnivore--in virtually every habitable environment on the earth's surface. Once scholars admit the necessity of linking processes of natural selection with human transformations of the natural world, it will seem anomalous that it has taken so long to integrate Darwinian biology and the social sciences.

Public goods, sharing genes, and the formation of large groups

Humans exhibit intense attachments to very large groups, sometimes numbering in the millions. The author addresses the question of how inclinations to attach to large groups might have evolved and identifies the problem of collective action and free riding as the central obstacles to overcome. He argues that the nonsubtractibility feature of public goods and the inclusive fitness theory of W. D. Hamilton are key elements in the evolution of sharing behavior in large groups: a source of group attachments. The argument implies that the mix of goods available and produced in past and present environments impacts the configuration of different-sized groups found in human society.

Frequency Dependence and Cooperation: Theory and a Test with Bacteria

Hamilton's inclusive fitness theory provides a leading explanation for the problem of cooperation. A general result from inclusive fitness theory is that, except under restrictive conditions, cooperation should not be subject to frequency-dependent selection. However, several recent studies in microbial systems have demonstrated that the relative fitness of cheaters, which do not cooperate, is greater when cheaters are rarer. Here we demonstrate theoretically that such frequency-dependent selection can occur in microbes when there is (1) sufficient population structuring or (2) an association between the level of cooperation and total population growth. We test prediction (2) and its underlying assumption, using the pathogenic bacterium Pseudomonas aeruginosa, by competing strains that produce iron-scavenging siderophore molecules (cooperators) with nonproducers (cheaters) at various ratios, under conditions that minimize population structuring. We found that both the relative fitness of cheaters and the productivity of the mixed culture were significantly negatively related to initial cheater frequency. Furthermore, when the period of population growth was experimentally shortened, the strength of frequency dependence was reduced. More generally, we argue that frequency-dependent selection on cooperative traits may be more common in microbes than in metazoans because strong selection, structuring, and cooperation-dependent growth will be more common in microbial populations.

Inclusive Fitness Theory from Darwin to Hamilton

ONE of the central dogmas of modern behavioral ecology is that blood kinship plays a critical role in understanding the evolution of social behavior, particularly of costly social behavior such as altruism and cooperation. But it was not always so, and what I would like to do in this Perspectives is provide some historical context that led up to William Hamilton's seminal work developing inclusive fitness theory. The story begins, not surprisingly, with Charles Darwin. The worker bees that sacrifice themselves to protect their hives—the ultimate example of animal altruism—were deeply troubling to Darwin. If increased reproduction is the currency of natural selection, then altruists should disappear—and fast. But they did not disappear, and Darwin was so puzzled by this that he spoke of altruism as a problem that he feared was “one special difficulty, which at first appeared to me to be insuperable, and actually fatal to the whole theory” (Darwin 1859, p. 236). Eventually, however, Darwin came up with an explanation. Since sterile worker bees were helping their blood relatives—especially the queen—Darwin hypothesized that natural selection might favor altruism at the level of blood kin. In a section of On the Origin of Species entitled “Objections to the theory of natural selection and instinct: neuter and sterile insects,” Darwin proposes that the problem of natural selection producing sterile castes that often risk their lives to protect others “disappears when it is remembered that selection may be applied to the family, as well as the individual and may thus gain the desired end” (Darwin 1859, p. 204). Blood kinship, and interactions among relatives, it turned out, was the key to solving Darwin's problems with both social insect sterility and altruism. One hundred and four years later, biologist William Hamilton would formalize Darwin's idea, but the path from Darwin to Hamilton was not smooth (Dugatkin 2006). That fact that it was not is not surprising. The nature of altruism makes it all too easy to drift from a scientific to a political, philosophical, and even a religious approach to this subject. Studying the structure of an atom is not personal, and neither is studying, for example, night vision in mammals. Studying altruism can be personal, however, because we all want to understand the origins of goodness. And it certainly was personal for the next two figures in the story of blood kinship and altruism—Thomas Henry Huxley and Peter Kropotkin (Woodcock and Avakumovic 1950; Desmond 1994).

Nepotism absent in insect societies — or is it?

Inclusive fitness theory, put forward by English biologist William Hamilton in 1964, is considered by many as the most important addition to the theory of natural selection since Darwin. One prediction of the theory is that animals should often show a tendency to nepotistically favour close relatives. Goodisman et al. (2007) test this theory for the first time using molecular methods in a vespine wasp, the eastern yellowjacket, Vespula maculifrons. Somewhat surprisingly, nepotism was found to be absent. This begs the question why nepotism is predicted by theory, yet in a growing list of species is shown to be absent. Is inclusive fitness theory in trouble? As we show, it is not: costs and constraints explain the general absence of queen rearing nepotism, and nepotism in insect societies in fact is well supported in the context of male rearing and manipulation of colony sex ratios.

Social closeness of MZ and DZ twin parents towards nieces and nephews

Twins' marriages to non‐twins yield genetically and socially informative kinships. Monozygotic (MZ) twins' genetic identity makes them ‘genetic parents’ of their nieces/nephews, and their nieces/nephews their ‘genetic children’. The present study is the first to apply twin‐family models to study social relatedness. Analyses of twin families (MZ: N = 248; DZ: N = 75) tested evolutionary‐based concepts concerning social closeness, perceived similarity and caretaking. Hypotheses based on Hamilton's inclusive fitness theory were supported: MZ twin aunts/uncles expressed greater social closeness towards their nieces/nephews than DZ twin aunts/uncles; and female twins from same‐sex pairs expressed greater closeness towards their nieces/nephews than male twins from same‐sex pairs. This study underlines benefits of associations between behavioural‐genetic and evolutionary psychological theories, methods and interpretations. Copyright © 2007 John Wiley & Sons, Ltd.

The formal Darwinism project: a mid‐term report

For 8 years I have been pursuing in print an ambitious and at times highly technical programme of work, the 'Formal Darwinism Project', whose essence is to underpin and formalize the fitness optimization ideas used by behavioural ecologists, using a new kind of argument linking the mathematics of motion and the mathematics of optimization. The value of the project is to give stronger support to current practices, and at the same time sharpening theoretical ideas and suggesting principled resolutions of some untidy areas, for example, how to define fitness. The aim is also to unify existing free-standing theoretical structures, such as inclusive fitness theory, Evolutionary Stable Strategy (ESS) theory and bet-hedging theory. The 40-year-old misunderstanding over the meaning of fitness optimization between mathematicians and biologists is explained. Most of the elements required for a general theory have now been implemented, but not together in the same framework, and 'general time' remains to be developed and integrated with the other elements to produce a final unified theory of neo-Darwinian natural selection.

Frequency Dependence and Cooperation: Theory and a Test with Bacteria

Hamilton’s inclusive fitness theory provides a leading explanation for the problem of cooperation. A general result from inclusive fitness theory is that, except under restrictive conditions, cooperation should not be subject to frequency‐dependent selection. However, several recent studies in microbial systems have demonstrated that the relative fitness of cheaters, which do not cooperate, is greater when cheaters are rarer. Here we demonstrate theoretically that such frequency‐dependent selection can occur in microbes when there is (1) sufficient population structuring or (2) an association between the level of cooperation and total population growth. We test prediction (2) and its underlying assumption, using the pathogenic bacterium Pseudomonas aeruginosa, by competing strains that produce iron‐scavenging siderophore molecules (cooperators) with nonproducers (cheaters) at various ratios, under conditions that minimize population structuring. We found that both the relative fitness of cheaters and the productivity of the mixed culture were significantly negatively related to initial cheater frequency. Furthermore, when the period of population growth was experimentally shortened, the strength of frequency dependence was reduced. More generally, we argue that frequency‐dependent selection on cooperative traits may be more common in microbes than in metazoans because strong selection, structuring, and cooperation‐dependent growth will be more common in microbial populations.

Detecting kin selection at work using inclusive fitness

A recent model shows that altruism can evolve with limited migration and variable group sizes, and the authors claim that kin selection cannot provide a sufficient explanation of their results. It is demonstrated, using a recent reformulation of Hamilton's original arguments, that the model falls squarely within the scope of inclusive fitness theory, which furthermore shows how to calculate inclusive fitness and the relevant relatedness. A distinction is drawn between inclusive fitness, which is a method of analysing social behaviour; and kin selection, a process that operates through genetic similarity brought about by common ancestry, but not by assortation by genotype or by direct assessment of genetic similarity. The recent model is analysed, and it turns out that kin selection provides a sufficient explanation to considerable quantitative accuracy, contrary to the authors' claims. A parallel analysis is possible and would be illuminating for all models of social behaviour in which individuals' effects on each other's offspring numbers combine additively.

Modelling social evolution: the relative merits and limitations of a Hamilton's rule-based approach

Lehmann & Keller (2006) convincingly argue that cooperation or altruism can evolve only when at least one of the following conditions are met: (i) cooperation has direct personal benefits, (ii) individuals are genetically related, (iii) individuals have information on the likely behaviour of others or (iv) individuals recognize other cooperators through a phenotypic label (green beard recognition). The first condition is quite obvious. The three others are also intuitive, given that they provide various conditions under which interacting individuals are positively related, meaning more likely than chance to interact with fellow cooperators (Frank, 1998; Pepper & Smuts, 2002; Foster & Wenseleers, 2006; Foster et al., 2006). By focusing on costs and benefits and relatedness, Lehmann and Keller (2006) are adopting an inclusive fitness or Hamilton’s rule-based approach to classify social evolution models (Hamilton, 1964). Personally, I believe a Hamiltonian perspective is indeed a very intuitive one, and should be adopted more widely. This is true particularly in the area of game theory, where currently little effort is made to interpret results this way, and models are frequently simulation-based, making general, intuitive interpretation of results difficult. In fact, in my own work, Hamilton’s rule has always taken a central place in the derivation and interpretation of model results (e.g. Wenseleers et al., 2003, 2004a, b; Ratnieks et al., 2006). At the same time, however, one may also wonder whether it is possible to translate every single social evolution model into the form of Hamilton’s rule. Here, I am skeptical, the reason being that Hamilton’s rule has well-known limitations. In particular, Hamilton’s rule only works correctly under weak selection and additive gene action (Cavalli-Sforza & Feldman, 1978; Michod, 1982; Grafen, 1985; Bulmer, 1994; Hamilton, 1964, 1995; Frank, 1997; Roze & Rousset, 2003; Rousset, 2004). In addition, evolution is normally assumed to be close to equilibrium, with most of the population fixed for a single type (Frank, 1998). Finally, with Hamilton’s rule being a deterministic equation, it entirely neglects stochasticity, and thus ignores the possibility for deleterious altruistic genotypes to go to fixation as a result of drift (Frank, 1997), which models have shown to be quite possible in small populations (Eshel, 1972; Rousset, 2004). In the section below I will give two worked-out examples where some of these limitations come into play and where, due to violations of assumptions, Hamilton’s rule does not correctly predict evolutionary change. The implication is that partitioning selection into direct and indirect fitness components is not always as straightforward as Lehmann and Keller make out. In many cases, the conditions under which a cooperative genotype would spread relative to a noncooperative one simply cannot be written in the form of Hamilton’s rule. In such situations, the inclusive fitness framework of Lehmann and Keller cannot be used to accurately classify models.

Synergy, partner choice and frequency dependence: their integration into inclusive fitness theory and their interpretation in terms of direct and indirect fitness effects

The aims of our Target Review (Lehmann & Keller, 2006) were to develop a simple model allowing us to delineate the conditions necessary for cooperation and altruism to evolve and argue that the models proposed so far can all be classified into four general categories depending on the selective forces at work. These are direct benefits to the Focal Individual (FI) performing a cooperative act, repeated interactions with direct or indirect information on the behaviour of the partner in previous moves, preferential interactions between related individuals and/ or a linkage disequilibrium between genes coding for altruism and phenotypic traits that lead to assortment of individuals bearing altruistic genes (i.e. greenbeard effect). We were extremely pleased to see that authors of 14 of the 15 Commentaries found our framework useful and generally endorsed our views. Doebeli & Fletcher (2006) were the only authors who fundamentally disagreed with our classification. However, their criticisms mostly stem from a misunderstanding of our model and kin selection theory. Several Commentaries raised similar general issues, in particular about the assumptions of our model and/or alleged limitations of Hamilton’s rule. We therefore address these comments in the first four general sections. Following these, we address the criticisms raised by Fletcher and Doebeli (2006). Finally, in the two last sections, we discuss all the other specific comments raised in the Commentaries, and finish with a short conclusion.

Male parentage in army ants

In most social insects workers do not mate, but have retained the ability to produce haploid eggs that can develop into viable male offspring. Under what circumstances this reproductive potential is realized and how the ensuing worker-queen conflict over male production is resolved, is an area of active research in insect sociobiology. Here we present microsatellite data for 176 males from eight colonies of the African army ant Dorylus (Anomma) molestus. Comparison with worker genotypes and inferred queen genotypes from the same colonies show that workers do not or at best very rarely reproduce in the presence of the queen. Queens of D. (A.) molestus are known to be highly multiply mated. This implies that workers are on average more closely related to queen sons than to other workers' sons, so that our results are consistent with predictions from inclusive fitness theory. It remains unknown, however, whether worker sterility is maintained by active worker policing or by self-restraint.

Kin selection is the key to altruism

Kin selection theory, also known as inclusive fitness theory, has been the subject of much debate and misunderstanding. Nevertheless, the idea that relatedness among individuals can drive the evolution of altruism has emerged as a central paradigm in evolutionary biology. Or has it? In two recent articles, E.O. Wilson argues that kin selection should no longer be considered the main explanation for the evolution of altruism in insect societies. Here, we discuss what these articles say about kin selection and how it relates to the theory. We conclude that kin selection remains the key explanation for the evolution of altruism in eusocial insects.

Fitness extraction and the conceptual foundations of political biology

In well known formulations, political science, classical and neoclassical economics, and political economy have recognized as foundational a human impulse toward self-preservation. To employ this concept, modern social-sciences theorists have made simplifying assumptions about human nature and have then built elaborately upon their more incisive simplifications. Advances in biology, including advances in evolutionary theory, notably inclusive-fitness theory, have for decades now encouraged the reconsideration of such assumptions and, more ambitiously, the reconciliation of the social and life sciences. I ask if this reconciliation is feasible and test a path to the unification of politics and biology, called here “political biology.” Two new notions, “fitness extraction” and “fitness exchange,” are defined, then differentiated from each other, and lastly contrasted to cooperative gaming, the putative essential element of economics.

Optimization of inclusive fitness

The first fully explicit argument is given that broadly supports a widespread belief among whole-organism biologists that natural selection tends to lead to organisms acting as if maximizing their inclusive fitness. The use of optimization programs permits a clear statement of what this belief should be understood to mean, in contradistinction to the common mathematical presumption that it should be formalized as some kind of Lyapunov or even potential function. The argument reveals new details and uncovers latent assumptions. A very general genetic architecture is allowed, and there is arbitrary uncertainty. However, frequency dependence of fitnesses is not permitted. The logic of inclusive fitness immediately draws together various kinds of intra-genomic conflict, and the concept of ‘p-family’ is introduced. Inclusive fitness is thus incorporated into the formal Darwinism project, which aims to link the mathematics of motion (difference and differential equations) used to describe gene frequency trajectories with the mathematics of optimization used to describe purpose and design. Important questions remain to be answered in the fundamental theory of inclusive fitness.

Kinship, sex, and fitness in a Caribbean community.

Patterns of human kinship commonly involve preferential treatment of relatives based on lineal descent (lineages) rather than degree of genetic relatedness (kindreds), presenting a challenge for inclusive fitness theory. Here, we examine effects of lineage and kindred characteristics on reproductive success (RS) and number of grandchildren for 130 men and 124 women in a horticultural community on Dominica. Kindreds had little effect on fitness independently of lineage characteristics. Fitness increased with the number of lineal relatives residing in the community but decreased beyond an apparently optimal lineage size, suggesting resource enhancement and competition among kin. Female-biased patrilineage sex ratio was positively associated with men's fitness, while male-biased matrilineage sex ratio was positively associated with women's fitness. Number of brothers in the community was negatively associated with men's, but not women's, fitness. Parents and number of sisters had no effect on either male or female reproduction; however, women with younger sisters had higher RS, suggesting benefits of kin support for childcare. In sum, imposed norms for lineage social organization may enhance lineal ancestors' inclusive fitness at a cost to individual inclusive fitness.

Fitness extraction and the conceptual foundations of political biology

In well known formulations, political science, classical and neoclassical economics, and political economy have recognized as foundational a human impulse toward self-preservation. To employ this concept, modern social-sciences theorists have made simplifying assumptions about human nature and have then built elaborately upon their more incisive simplifications. Advances in biology, including advances in evolutionary theory, notably inclusive-fitness theory, have for decades now encouraged the reconsideration of such assumptions and, more ambitiously, the reconciliation of the social and life sciences. I ask if this reconciliation is feasible and test a path to the unification of politics and biology, called here "political biology." Two new notions, "fitness extraction" and "fitness exchange," are defined, then differentiated from each other, and lastly contrasted to cooperative gaming, the putative essential element of economics.

Why do honey bee workers destroy each other's eggs?

Hamilton’s theory of inclusive fitness predicts that in polyandrous colonies of social Hymenoptera, workers should prevent each other from reproducing and prefer to rear the queen’s sons rather than their nephews. This is because, in polyandrous colonies, unlike in monandrous colonies, workers are expected to be more closely related to their brothers than to their nephews. Honey bees clearly fulfill this expectation – queens mate multiply, worker reproduction is rare and the few eggs laid by workers are usually destroyed by other workers. Such mutual destruction of each other’s eggs by honey bee workers has been called worker policing and has achieved the status of a classic example of kin selection. However, recent evidence indicating that worker-laid eggs may be much less viable than queen-laid eggs opens up the possibility that worker policing may simply be a matter of destroying dead eggs and rearing live ones. If confirmed, this raises serious doubts about the widely accepted relatedness based argument for the evolution of worker policing. A major weakness of the kin selection-based explanation for worker policing is our ignorance of the proximate cues used by worker bees to distinguish between brother eggs and nephew eggs.

Kin influence on female reproductive behavior: the evidence from reconstitution of the Bejsce parish registers, 18th to 20th centuries, Poland.

The phenomenon of kin-oriented help, according to inclusive fitness theory, should be of crucial importance with respect to the process of reproduction. This is due to the fact that the devoted time and resources might indirectly contribute to the reproductive performance of a donor. This study aimed at analyzing the kin effects on fertility in order to check whether help received from kinsmen enhance a recipient's reproduction in terms of parity transition risk, completed fertility, and the number of survivors. The data came from reconstitution of church registers from Bejsce parish, Poland. To estimate the kin effect, regression models for count outcomes and techniques of multilevel event history analysis were applied. The analyses have shown that completed fertility and parity-specific transition risks are strongly influenced by various kin groups. Moreover, a multilevel hazard model revealed differences in the patterns of the kin influence among controlled fertility than among natural fertility birth cohorts. Female reproductive outcome is influenced mainly by the presence of siblings and postreproductive helpers (grandparents). However, there is a negative impact of so-called helpers-at-the-nest (older children in the household) on parity transition risks.