Inclusive Fitness Theory Research Articles

A novel screen for genes associated with pheromone-induced sterility.

For honey bee and other social insect colonies the ‘queen substance’ regulates colony reproduction rendering workers functionally sterile. The evolution of worker reproductive altruism is explained by inclusive fitness theory, but little is known of the genes involved or how they regulate the phenotypic expression of altruism. We previously showed that application of honeybee queen pheromone to virgin fruit flies suppresses fecundity. Here we exploit this finding to identify genes associated with the perception of an ovary-inhibiting social pheromone. Mutational and RNAi approaches in Drosophila reveal that the olfactory co-factor Orco together with receptors Or49b, Or56a and Or98a are potentially involved in the perception of queen pheromone and the suppression of fecundity. One of these, Or98a, is known to mediate female fly mating behaviour, and its predicted ligand is structurally similar to a methyl component of the queen pheromone. Our novel approach to finding genes associated with pheromone-induced sterility implies conserved reproductive regulation between social and pre-social orders, and further helps to identify candidate orthologues from the pheromone-responsive pathway that may regulate honeybee worker sterility.

The Theory of Inclusive FitnessA review of Social Evolution and Inclusive Fitness Theory: An Introduction. By James A. R. Marshall. Princeton (New Jersey): Princeton University Press. $39.95. xix + 195 p.; ill.; index. ISBN: 978-0-691-16156-3. 2015.

Previous articleNext article No AccessThe Theory of Inclusive Fitness A review of Social Evolution and Inclusive Fitness Theory: An Introduction. By James A. R. Marshall. Princeton (New Jersey): Princeton University Press. $39.95. xix + 195 p.; ill.; index. ISBN: 978-0-691-16156-3. 2015.David C. QuellerDavid C. QuellerDepartment of Biology, Washington UniversitySt. Louis, Missouri 63130-4899 USA Search for more articles by this author Department of Biology, Washington UniversitySt. Louis, Missouri 63130-4899 USAe-mail: [email protected]PDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The Quarterly Review of Biology Volume 91, Number 3September 2016 Published in association with Stony Brook University Article DOIhttps://doi.org/10.1086/688099 Views: 289Total views on this site Citations: 3Citations are reported from Crossref For permission to reuse, please contact [email protected]PDF download Crossref reports the following articles citing this article:Toru Miura, Kohei Oguchi, Haruka Yamaguchi, Mayuko Nakamura, Daisuke Sato, Kenta Kobayashi, Nobuyuki Kutsukake, Kyoko Miura, Yoshinobu Hayashi, Masaru Hojo, Kiyoto Maekawa, Shuji Shigenobu, Takeshi Kano, Akio Ishiguro Understanding of superorganisms: collective behavior, differentiation and social organization, Artificial Life and Robotics 27, no.22 (Mar 2022): 204–212.https://doi.org/10.1007/s10015-022-00754-xApril M. Becker The flight of the locus of selection: Some intricate relationships between evolutionary elements, Behavioural Processes 161 (Apr 2019): 31–44.https://doi.org/10.1016/j.beproc.2018.01.002James AR Marshall What is inclusive fitness theory, and what is it for?, Current Opinion in Behavioral Sciences 12 (Dec 2016): 103–108.https://doi.org/10.1016/j.cobeha.2016.09.015

Variation in helper effort among cooperatively breeding bird species is consistent with Hamilton's Rule.

Investment by helpers in cooperative breeding systems is extremely variable among species, but this variation is currently unexplained. Inclusive fitness theory predicts that, all else being equal, cooperative investment should correlate positively with the relatedness of helpers to the recipients of their care. We test this prediction in a comparative analysis of helper investment in 36 cooperatively breeding bird species. We show that species-specific helper contributions to cooperative brood care increase as the mean relatedness between helpers and recipients increases. Helper contributions are also related to the sex ratio of helpers, but neither group size nor the proportion of nests with helpers influence helper effort. Our findings support the hypothesis that variation in helping behaviour among cooperatively breeding birds is consistent with Hamilton's rule, indicating a key role for kin selection in the evolution of cooperative investment in social birds.

Extended inclusive fitness theory: synergy and assortment drives the evolutionary dynamics in biology and economics.

W.D. Hamilton’s Inclusive Fitness Theory explains the conditions that favor the emergence and maintenance of social cooperation. Today we know that these include direct and indirect benefits an agent obtains by its actions, and through interactions with kin and with genetically unrelated individuals. That is, in addition to kin-selection, assortation or homophily, and social synergies drive the evolution of cooperation. An Extended Inclusive Fitness Theory (EIFT) synthesizes the natural selection forces acting on biological evolution and on human economic interactions by assuming that natural selection driven by inclusive fitness produces agents with utility functions that exploit assortation and synergistic opportunities. This formulation allows to estimate sustainable cost/benefit threshold ratios of cooperation among organisms and/or economic agents, using existent analytical tools, illuminating our understanding of the dynamic nature of society, the evolution of cooperation among kin and non-kin, inter-specific cooperation, co-evolution, symbioses, division of labor and social synergies. EIFT helps to promote an interdisciplinary cross fertilization of the understanding of synergy by, for example, allowing to describe the role for division of labor in the emergence of social synergies, providing an integrated framework for the study of both, biological evolution of social behavior and economic market dynamics. Another example is a bio-economic understanding of the motivations of terrorists, which identifies different forms of terrorism.

Evolutionary Roots of Property Rights; The Natural and Cultural Nature of Human Cooperation

Debates about the role of natural and cultural selection in the development of prosocial, antisocial and socially neutral mechanisms and behavior raise questions that touch property rights, cooperation, and conflict. For example, some researchers suggest that cooperation and prosociality evolved by natural selection (Hamilton 1964, Trivers 1971, Axelrod and Hamilton 1981, De Waal 2013, 2014), while others claim that natural selection is insufficient for the evolution of cooperation, which required in addition cultural selection (Sterelny 2013, Bowles and Gintis 2003, Seabright 2013, Norenzayan 2013). Some scholars focus on the complexity and hierarchical nature of the evolution of cooperation as involving different tools associated with lower and the higher levels of competition (Nowak 2006, Okasha 2006); others suggest that humans genetically inherited heuristics that favor prosocial behavior such as generosity, forgiveness or altruistic punishment (Ridley 1996, Bowles and Gintis 2004, Rolls 2005). We argue these mechanisms are not genetically inherited; rather, they are features inherited through cultural selection. To support this view we invoke inclusive fitness theory, which states that individuals tend to maximize their inclusive fitness, rather than maximizing group fitness. We further reject the older notion of natural group selection - as well as more recent versions (West, Mouden, Gardner 2011) – which hold that natural selection favors cooperators within a group (Wynne-Edwards 1962). For Wynne-Edwards, group selection leads to group adaptations; the survival of individuals therefore depends on the survival of the group and a sharing of resources. Individuals who do not cooperate, who are selfish, face extinction due to rapid and over-exploitation of resources.

Context dependent bias in honeybee queen selection: swarm versus emergency queens

Colonies of social Hymenoptera with multiple mated queens comprise of numerous super-sister subfamilies with high within but low between subfamily relatedness. Because fitness gain in workers is indirect and relatedness dependent, inclusive fitness theory predicts that nepotism might be adaptive, particularly with respect to queen rearing and selection of new queens. However, nepotistic queen rearing could not been detected in various eusocial insect species and instead workers preferentially rear queens from rare subfamilies after queen loss. Here, we test, whether this bias can also be observed in queen rearing in preparation for reproductive swarming in the honeybee, Apis mellifera. Colonies reared swarm and subsequently emergency queens. Genotyping of all produced queens as well as worker brood revealed a significant deviation from the expected worker subfamily distribution for emergency queens but not for swarm queens. The preference of rare subfamilies may result from worker control over queen rearing in emergency queen rearing. Based on our results it appears that workers choose a few out of a vast number of worker-destined larvae to select emergency queens at extreme selection intensity. This sets the stage for competition among larvae to compete for queen caste fate, presumably by differentially attracting nurse workers to raise them as queens. During swarm queen production, workers cannot select larvae, because the queen lays eggs into predestined cells, resulting in subfamily distributions among the queens more similar to a random subfamily sample as determined in the worker brood. SIGNIFICANCE STATEMENT: Honeybee queens mate with multiple males resulting in several coexisting subfamilies within a colony favoring nepotism by workers rearing a super-sister as a new queen. Workers feeding queen-destined larvae a special diet and thus, larvae seem to have no influence over their caste fate. Queen rearing happens under different circumstances, conditions for nursing workers to bias queen broods and for larvae to bias their caste fate might differ. We tested for subfamily bias in queen broods reared in preparation for reproductive swarming, when queens provision specific cells with eggs to be reared as queens. Within the same colonies, after dequeening, nursing workers choose from available young larvae individuals to be reared as emergency queens. We detected a subfamily bias under emergency queens, but instead of nepotism, we found evidence for larvae to selfishly bias their own caste fate.

Reproductive concessions between related and unrelated members promote eusociality in bees.

Animal societies exhibit remarkable variation in their breeding strategies. Individuals can maximize their fitness by either reproducing or by helping relatives. Social hymenopterans have been key taxa for the study of Hamilton’s inclusive fitness theory because the haplodiploid sex-determination system results in asymmetric relatedness among breeders producing conflict over the partitioning of reproduction. In small cooperative groups of insects, totipotent individuals may maximize their inclusive fitness by controlling reproduction despotically rather than helping their relatives. Here, we demonstrate that the dominant females of the primitively eusocial bee Euglossa melanotricha (Apidae: Euglossini) control reproduction, but concede part of the reproductive output with their related and unrelated subordinates. As expected, a dominant female capitalizes on the direct reproduction of related subordinates, according to her interests. We found that reproductive skew was positively correlated with relatedness. The concessions were highly reduced in mother-daughter and sibling nests (relatedness r ± s.d. = 0.54 ± 0.02 and 0.79 ± 0.02, respectively) but much more egalitarian in unrelated associations (r = −0.10 ± 0.01). We concluded that reproductive skew in these primitively eusocial bees is strongly related to the genetic structure of associations, and also that females are able to assess pairwise relatedness, either directly or indirectly, and use this information to mediate social contracts.

Genes Underlying Reproductive Division of Labor in Termites, with Comparisons to Social Hymenoptera

All social insects are characterized by a reproductive division of labor. Within a colony only a few individuals reproduce (queens and in termites, also a king) while the large majority (workers and soldiers) forgo reproduction, at least temporarily. The evolution of such reproductive altruism can ultimately be explained by inclusive fitness theory. Here, I will review the proximate genetic mechanisms underlying this altruism in termites. As social cockroaches they evolved eusociality independently from the social Hymenoptera, which makes them interesting test cases to look for common underlying mechanisms of eusociality and lineage specific idiosyncrasies. First, I will provide a summary of the genes and their function that have been identified to underlie reproductive division of labor - so called 'queen genes,' - in the drywood termite Cryptotermes secundus, an emerging model to study termite social evolution. Second, I outline how widespread these queen genes are across the termite phylogeny, using also evidence from recent genome analyses. I will provide hypotheses about the evolutionary origin of these queen genes, aiming to link proximate mechanisms with ultimate functions. Finally, I will draw comparisons to social Hymenoptera to indicate potential common underpinnings that warrant further testing.

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.

Errors in Allen's Review of Social Evolution and Inclusive Fitness Theory: An Introduction

Errors in Allen's Review of Social Evolution and Inclusive Fitness Theory: An Introduction

Evolution of social behaviour in the primitively eusocial wasp Ropalidia marginata: do we need to look beyond kin selection?

Ropalidia marginata is a primitively eusocial wasp widely distributed in peninsular India. Although solitary females found a small proportion of nests, the vast majority of new nests are founded by small groups of females. In such multiple foundress nests, a single dominant female functions as the queen and lays eggs, while the rest function as sterile workers and care for the queen's brood. Previous attempts to understand the evolution of social behaviour and altruism in this species have employed inclusive fitness theory (kin selection) as a guiding framework. Although inclusive fitness theory is quite successful in explaining the high propensity of the wasps to found nests in groups, several features of their social organization suggest that forces other than kin selection may also have played a significant role in the evolution of this species. These features include lowering of genetic relatedness owing to polyandry and serial polygyny, nest foundation by unrelated individuals, acceptance of young non-nest-mates, a combination of well-developed nest-mate recognition and lack of intra-colony kin recognition, a combination of meek and docile queens and a decentralized self-organized work force, long reproductive queues with cryptic heir designates and conflict-free queen succession, all resulting in extreme intra-colony cooperation and inter-colony conflict.

Hamilton's rule, inclusive fitness maximization, and the goal of individual behaviour in symmetric two-player games.

Hamilton's original work on inclusive fitness theory assumed additivity of costs and benefits. Recently, it has been argued that an exact version of Hamilton's rule for the spread of a pro-social allele (rb > c) holds under nonadditive pay-offs, so long as the cost and benefit terms are defined as partial regression coefficients rather than pay-off parameters. This article examines whether one of the key components of Hamilton's original theory can be preserved when the rule is generalized to the nonadditive case in this way, namely that evolved organisms will behave as if trying to maximize their inclusive fitness in social encounters.

Neural, cognitive, and evolutionary foundations of human altruism.

This article considers three forms of altruism from both a psychological and a neural perspective, with an emphasis on homologies that can be observed across species and potentially illuminate altruism's evolutionary origins. Kin-based altruism benefits biological relatives and, according to the theory of inclusive fitness, is ultimately beneficial to the altruist from a genetic standpoint. Kin selection adequately explains some altruistic behavior, but it is not applicable to much human altruism. Little is known about the neural processes that support it, but they may include cortical regions involved in processing autobiographical memory and the identities of familiar others. Reciprocity-based altruism is performed in expectation of future rewards and is supported by dopaminergic cortico-striatal networks that guide behavior according to anticipated rewards. Care-based altruism is aimed at improving the well-being of distressed and vulnerable individuals and is closely linked to empathic concern. This form of altruism is thought to rely on the subcortical neural systems that support parental care, particularly structures densely populated with receptors for the hormones oxytocin and vasopressin, including the amygdala, stria terminalis, and striatum. The amygdala may be a particularly important convergence point for care-based altruism because of its dual role in responding both to cues that signal infantile vulnerability and those that signal distress. Research on altruism continues to converge across disciplines, but more research linking molecular-level neural processes to altruistic behavior in humans and other species is needed, as is research on how various forms of altruism intersect. For further resources related to this article, please visit the WIREs website.

Moment equations in spatial evolutionary ecology

How should we model evolution in spatially structured populations? Here, I review an evolutionary ecology approach based on the technique of spatial moment equations. I first provide a mathematical underpinning to the derivation of equations for the densities of various spatial configurations in network-based models. I then show how this spatial ecological framework can be coupled with an adaptive dynamics approach to compute the invasion fitness of a rare mutant in a resident population at equilibrium. Under the additional assumption that mutations have small phenotypic effects, I show that the selection gradient can be expressed as a function of neutral measures of genetic and demographic structure. I discuss the connections between this approach and inclusive fitness theory, as well as the applicability and limits of this technique. My main message is that spatial moment equations can be used as a means to obtain compact qualitative arguments about the evolution of life-history traits for a variety of life cycles.

'Morals can not be drawn from facts but guidance may be': the early life of W.D. Hamilton's theory of inclusive fitness.

W.D. Hamilton's theory of inclusive fitness saw the evolution of altruism from the point of view of the gene. It was at heart a theory of limits, redefining altruistic behaviours as ultimately selfish. This theory inspired two controversial texts published almost in tandem, E.O. Wilson's Sociobiology: The New Synthesis (1975) and Richard Dawkins's The Selfish Gene (1976). When Wilson and Dawkins were attacked for their evolutionary interpretations of human societies, they claimed a distinction between reporting what is and declaring what ought to be. Can the history of sociobiological theories be so easily separated from its sociopolitical context? This paper draws upon unpublished materials from the 1960s and early 1970s and documents some of the ways in which Hamilton saw his research as contributing to contemporary concerns. It pays special attention to the 1969 Man and Beast Smithsonian Institution symposium in order to explore the extent to which Hamilton intended his theory to be merely descriptive versus prescriptive. From this, we may see that Hamilton was deeply concerned about the political chaos he perceived in the world around him, and hoped to arrive at a level of self-understanding through science that could inform a new social order.

Social Evolution: Uneasy Lies the Head

Inclusive fitness theory explains why workers in insect societies sometimes kill their queen. As the theory predicts, workers in a wasp species are more likely to act matricidally when more highly related to potential worker offspring.

Inclusive Fitness Theory Becomes an End in Itself

Inclusive Fitness Theory Becomes an End in Itself

Kinship reinforces cooperative predator inspection in a cichlid fish.

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.

Social evolution and inclusive fitness theory: an introduction

Social behavior has long puzzled evolutionary biologists, since the classical theory of natural selection maintains that individuals should not sacrifice their own fitness to affect that of others. Social Evolution and Inclusive Fitness Theory argues that a theory first presented in 1963 by William D. Hamilton—inclusive fitness theory—provides the most fundamental and general explanation for the evolution and maintenance of social behavior in the natural world. James Marshall guides readers through the vast and confusing literature on the evolution of social behavior, introducing and explaining the competing theories that claim to provide answers to questions such as why animals evolve to behave altruistically. Using simple statistical language and techniques that practicing biologists will be familiar with, he provides a comprehensive yet easily understandable treatment of key concepts and their repeated misinterpretations. Particular attention is paid to how more realistic features of behavior, such as nonadditivity and conditionality, can complicate analysis. Marshall highlights the general problem of identifying the underlying causes of evolutionary change, and proposes fruitful approaches to doing so in the study of social evolution. Social Evolution and Inclusive Fitness Theory describes how inclusive fitness theory addresses both simple and complex social scenarios, the controversies surrounding the theory, and how experimental work supports the theory as the most powerful explanation for social behavior and its evolution.

Individuality, phenotypic differentiation, dormancy and 'persistence' in culturable bacterial systems: commonalities shared by environmental, laboratory, and clinical microbiology.

For bacteria, replication mainly involves growth by binary fission. However, in a very great many natural environments there are examples of phenotypically dormant, non-growing cells that do not replicate immediately and that are phenotypically 'nonculturable' on media that normally admit their growth. They thereby evade detection by conventional culture-based methods. Such dormant cells may also be observed in laboratory cultures and in clinical microbiology. They are usually more tolerant to stresses such as antibiotics, and in clinical microbiology they are typically referred to as 'persisters'. Bacterial cultures necessarily share a great deal of relatedness, and inclusive fitness theory implies that there are conceptual evolutionary advantages in trading a variation in growth rate against its mean, equivalent to hedging one's bets. There is much evidence that bacteria exploit this strategy widely. We here bring together data that show the commonality of these phenomena across environmental, laboratory and clinical microbiology. Considerable evidence, using methods similar to those common in environmental microbiology, now suggests that many supposedly non-communicable, chronic and inflammatory diseases are exacerbated (if not indeed largely caused) by the presence of dormant or persistent bacteria (the ability of whose components to cause inflammation is well known). This dormancy (and resuscitation therefrom) often reflects the extent of the availability of free iron. Together, these phenomena can provide a ready explanation for the continuing inflammation common to such chronic diseases and its correlation with iron dysregulation. This implies that measures designed to assess and to inhibit or remove such organisms (or their access to iron) might be of much therapeutic benefit.