More on the genetical theory of multilevel selection

In my article The genetical theory of multilevel selection, I provided a synthesis of the theory of multilevel selection (MLS) and the theory of natural selection in class‐structured populations. I framed this synthesis within Fisher's genetical paradigm, taking a strictly genetical approach to traits and fitness. I showed that this resolves a number of long‐standing conceptual problems that have plagued the MLS literature, including the issues of ‘aggregate’ vs. ‘emergent’ group traits, ‘collective fitness₁’ vs. ‘collective fitness₂’ and ‘MLS1’ vs. ‘MLS2 ‘. In his commentary, Goodnight suggests this theoretical and conceptual synthesis is flawed in several respects. Here, I show this is incorrect, by: reiterating the theoretical and conceptual goals of my synthesis; clarifying that my genetical approach to traits is necessary for a proper analysis of the action of MLS independently of non‐Darwinian factors; emphasizing that the Price–Hamilton approach to MLS provides a consistent, useful and conceptually superior theoretical framework; and explaining the role of reproductive value in the study of natural selection in class‐structured populations. I also show that Goodnight's contextual analysis treatment of MLS in a class‐structured population is mathematically, biologically and conceptually inadequate.     

The genetical theory of multilevel selection

The theory of multilevel selection (MLS) is beset with conceptual difficulties. Although it is widely agreed that covariance between group trait and group fitness may arise in the natural world and drive a response to ‘group selection’, ambiguity exists over the precise meaning of group trait and group fitness and as to whether group selection should be defined according to changes in frequencies of different types of individual or different types of group. Moreover, the theory of MLS has failed to properly engage with the problem of class structure, which greatly limits its empirical application to, for example, social insects whose colonies are structured into separate age, sex, caste and ploidy classes. Here, I develop a genetical theory of MLS, to address these problems. I show that taking a genetical approach facilitates a decomposition of group‐level traits – including reproductive success – into the separate contributions made by each constituent individual, even in the context of so‐called emergence. However, I uncover a novel problem with the group‐oriented approach: in many scenarios, it may not be possible to express a meaningful covariance between trait and fitness at the level of the social group, because the group's constituents belong to separate, irreconcilable classes.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter?

There has been a long‐standing conceptual debate over the legitimacy of assigning components of offspring fitness to parents for purposes of evolutionary analysis. The benefits and risks inherent in assigning fitness of offspring to parents have been given primarily as verbal arguments and no explicit theoretical analyses have examined quantitatively how the assignment of fitness can affect evolutionary inferences. Using a simple quantitative genetic model, we contrast the conclusions drawn about how selection acts on a maternal character when components of offspring fitness (such as early survival) are assigned to parents vs. when they are assigned directly to the individual offspring. We find that there are potential shortcomings of both possible assignments of fitness. In general, whenever there is a genetic correlation between the parental and direct effects on offspring fitness, assigning components of offspring fitness to parents yields incorrect dynamical equations and may even lead to incorrect conclusions about the direction of evolution. Assignment of offspring fitness to parents may also produce incorrect estimates of selection whenever environmental variation contributes to variance of the maternal trait. Whereas assignment of offspring fitness to the offspring avoids these potential problems, it introduces the possible problem of missing components of kin selection provided by the mother, which may not be detected in selection analyses. There are also certain conditions where either model can be appropriate because assignment of offspring fitness to parents may yield the same dynamical equations as assigning offspring fitness directly to offspring. We discuss these implications of the alternative assignments of fitness for modelling, selection analysis and experimentation in evolutionary biology.     

Inclusive fitness,asymmetric competition and kin selection in plants

The findings that some plants alter their competitive phenotype in response to genetic relatedness of its conspecific neighbour (and presumed competitor) has spurred an increasing interest in plant kin‐interactions. This phenotypic response suggests the ability to assess the genetic relatedness of conspecific competitors, proposing kin selection as a process that can influence plant competitive interactions. Kin selection can favour restrained competitive growth towards kin, if the fitness loss from reducing own growth is compensated by increased fitness in the related neighbour. This may lead to positive frequency dependency among related conspecifics with important ecological consequences for species assemblage and coexistence. However, kin selection in plants is still controversial. First, many studies documenting a plastic response to neighbour relatedness do not estimate fitness consequences of the individual that responds, and when estimated, fitness of individuals grown in competition with kin did not necessarily exceed that of individuals grown in non‐kin groups. Although higher fitness in kin groups could be consistent with kin selection, this could also arise from mechanisms like asymmetric competition in the non‐kin groups. Here we outline the main challenges for studying kin selection in plants taking genetic variation for competitive ability into account. We emphasize the need to measure inclusive fitness in order to assess whether kin selection occurs, and show under which circumstances kin selected responses can be expected. We also illustrate why direct fitness estimates of a focal plant, and group fitness estimates are not suitable for documenting kin selection. Importantly, natural selection occurs at the individual level and it is the inclusive fitness of an individual plant – not the mean fitness of the group – that can capture if a differential response to neighbour relatedness is favoured by kin selection.     

植物的亲缘选择

亲缘选择是指在一个随机交配群体中的个体基于亲缘关系而以一种非随机性的方式相互作用,其作用结果是亲缘个体得到更大的广义适合度。综述了亲缘选择和亲缘竞争两种观点以及各自的试验支持证据;分析了导致亲缘选择试验结果出现分歧的原因,认为这主要是由于对亲缘选择理解上的模糊以及试验设计的不严谨所致。植物间的亲缘选择研究不仅相对较少,对亲缘选择的机制研究更为欠缺,这就造成了目前对此问题在科学认识上出现不少盲点。综合前期研究,提出今后对亲缘选择的研究应该首先界定"亲缘"程度,同时改良试验设计方案,选择多种不同生境下的物种对亲缘选择进行深入研究,并且考虑环境因子对植物亲缘选择的影响。同时,对植物亲缘识别机制的研究应该从生理生化方面出发,通过定性定量地分析探索植物根系分泌物在植物亲缘识别中的作用和作用途径。     

The unity that does not exist – a review of A. Burt & R. Trivers 2006: Genes in Conflict

Organisms harbour several genetic elements with the potential to act selfishly, and thus undermine the fitness of the organism as a whole. In their book ‘Genes in conflict’, Austin Burt and Robert Trivers thoroughly review evolution and molecular biology of such selfish genetics elements, and set them in a kin selection framework. In this review I set their views in a larger multi‐level selection framework, and consider potential problems in the study of selfish genetics elements.     

Darwin's ‘one special difficulty’: celebrating Darwin 200

Darwin identified eusocial evolution, especially of complex insect societies, as a particular challenge to his theory of natural selection. A century later, Hamilton provided a framework for selection on inclusive fitness. Hamilton''s rule is robust and fertile, having generated multiple subdisciplines over the past 45 years. His suggestion that eusociality can be explained via kin selection, however, remains contentious. I review the continuing debate on the role of kin selection in eusocial evolution and suggest some lines of research that should resolve that debate.     

Can natural selection favour altruism between species?

Darwin suggested that the discovery of altruism between species would annihilate his theory of natural selection. However, it has not been formally shown whether between‐species altruism can evolve by natural selection, or why this could never happen. Here, we develop a spatial population genetic model of two interacting species, showing that indiscriminate between species helping can be favoured by natural selection. We then ask if this helping behaviour constitutes altruism between species, using a linear‐regression analysis to separate the total action of natural selection into its direct and indirect (kin selected) components. We show that our model can be interpreted in two ways, as either altruism within species, or altruism between species. This ambiguity arises depending on whether or not we treat genes in the other species as predictors of an individual's fitness, which is equivalent to treating these individuals as agents (actors or recipients). Our formal analysis, which focuses upon evolutionary dynamics rather than agents and their agendas, cannot resolve which is the better approach. Nonetheless, because a within‐species altruism interpretation is always possible, our analysis supports Darwin's suggestion that natural selection does not favour traits that provide benefits exclusively to individuals of other species.     

Relatedness in spatially structured populations with empty sites: An approach based on spatial moment equations

Taking into account the interplay between spatial ecological dynamics and selection is a major challenge in evolutionary ecology. Although inclusive fitness theory has proven to be a very useful tool to unravel the interactions between spatial genetic structuring and selection, applications of the theory usually rely on simplifying demographic assumptions. In this paper, I attempt to bridge the gap between spatial demographic models and kin selection models by providing a method to compute approximations for relatedness coefficients in a spatial model with empty sites. Using spatial moment equations, I provide an approximation of nearest-neighbour relatedness on random regular networks, and show that this approximation performs much better than the ordinary pair approximation. I discuss the connection between the relatedness coefficients I define and those used in population genetics, and sketch some potential extensions of the theory.     

The genetic consequences of selection in natural populations

The selection coefficient, s, quantifies the strength of selection acting on a genetic variant. Despite this parameter's central importance to population genetic models, until recently we have known relatively little about the value of s in natural populations. With the development of molecular genetic techniques in the late 20th century and the sequencing technologies that followed, biologists are now able to identify genetic variants and directly relate them to organismal fitness. We reviewed the literature for published estimates of natural selection acting at the genetic level and found over 3000 estimates of selection coefficients from 79 studies. Selection coefficients were roughly exponentially distributed, suggesting that the impact of selection at the genetic level is generally weak but can occasionally be quite strong. We used both nonparametric statistics and formal random‐effects meta‐analysis to determine how selection varies across biological and methodological categories. Selection was stronger when measured over shorter timescales, with the mean magnitude of s greatest for studies that measured selection within a single generation. Our analyses found conflicting trends when considering how selection varies with the genetic scale (e.g., SNPs or haplotypes) at which it is measured, suggesting a need for further research. Besides these quantitative conclusions, we highlight key issues in the calculation, interpretation, and reporting of selection coefficients and provide recommendations for future research.     

Fisher’s fundamental theorem of inclusive fitness and the change in fitness due to natural selection when conspecifics interact

Competition and cooperation is fundamental to evolution by natural selection, both in animals and plants. Here, I investigate the consequences of such interactions for response in fitness due to natural selection. I provide quantitative genetic expressions for heritable variance and response in fitness due to natural selection when conspecifics interact. Results show that interactions among conspecifics generate extra heritable variance in fitness, and that interacting with kin is the key to evolutionary success because it translates the extra heritable variance into response in fitness. This work also unifies Fisher’s fundamental theorem of natural selection (FTNS) and Hamilton’s inclusive fitness (IF). The FTNS implies that natural selection maximizes fitness, whereas Hamilton proposed maximization of IF. This work shows that the FTNS describes the increase in IF, rather than direct fitness, at a rate equal to the additive genetic variance in fitness. Thus, Hamilton’s IF and Fisher’s FTNS both describe the maximization of IF.     

THE COMPONENTS OF KIN COMPETITION

It is well known that competition among kin alters the rate and often the direction of evolution in subdivided populations. Yet much remains unclear about the ecological and demographic causes of kin competition, or what role life cycle plays in promoting or ameliorating its effects. Using the multilevel Price equation, I derive a general equation for evolution in structured populations under an arbitrary intensity of kin competition. This equation partitions the effects of selection and demography, and recovers numerous previous models as special cases. I quantify the degree of kin competition, α, which explicitly depends on life cycle. I show how life cycle and demographic assumptions can be incorporated into kin selection models via α, revealing life cycles that are more or less permissive of altruism. As an example, I give closed‐form results for Hamilton's rule in a three‐stage life cycle. Although results are sensitive to life cycle in general, I identify three demographic conditions that give life cycle invariant results. Under the infinite island model, α is a function of the scale of density regulation and dispersal rate, effectively disentangling these two phenomena. Population viscosity per se does not impede kin selection.     

A gene's eye view of epistasis,selection and speciation

In this mini‐review, I discuss the effects of gene interaction or epistasis from a `gene's eye view.' By a `gene's eye view' of epistasis, I mean that I will consider a single, bi‐allelic locus, A , whose effects on fitness result only from its interactions with alleles of another, unknown locus, X . I will show how changes in the frequencies of alleles at the background locus affect the relationship of alleles at the A ‐locus to fitness. Changing the genetic background changes the fundamental characteristics of the A ‐locus, such as the magnitude and sign of allelic effects on fitness, and, consequently, it changes the strength and pattern of selection. I consider each of the four kinds of pair–wise interactions between two loci and show that some kinds of epistasis are more sensitive than others to population genetic subdivision. Lastly, I show that some kinds of epistasis are more likely than others to affect the process of speciation and contribute to or be responsible for general genetic features of interspecific hybrids, such as Haldane's rule.     

The danger of applying the breeder's equation in observational studies of natural populations

The breeder's equation, which predicts evolutionary change when a phenotypic covariance exists between a heritable trait and fitness, has provided a key conceptual framework for studies of adaptive microevolution in nature. However, its application requires strong assumptions to be made about the causation of fitness variation. In its univariate form, the breeder's equation assumes that the trait of interest is not correlated with other traits having causal effects on fitness. In its multivariate form, the validity of predicted change rests on the assumption that all such correlated traits have been measured and incorporated into the analysis. Here, we (i) highlight why these assumptions are likely to be seriously violated in studies of natural, rather than artificial, selection and (ii) advocate wider use of the Robertson–Price identity as a more robust, and less assumption‐laden, alternative to the breeder's equation for applications in evolutionary ecology.     

Cryptic Kin Selection: Kin Structure in Vertebrate Populations and Opportunities for Kin‐Directed Cooperation

Animal societies of varying complexity have been the favoured testing ground for inclusive fitness theory, and there is now abundant evidence that kin selection has played a critical role in the evolution of cooperative behaviour. One of the key theoretical and empirical findings underlying this conclusion is that cooperative systems have a degree of kin structure, often the product of delayed dispersal, that facilitates interactions with relatives. However, recent population genetic studies have revealed that many non‐cooperative animals also have kin‐structured populations, providing more cryptic opportunities for kin selection to operate. In this article, I first review the evidence that kin structure is widespread among non‐cooperative vertebrates, and then consider the various contexts in which kin selection may occur in such taxa, including: leks, brood parasitism, crèches, breeding associations, territoriality and population dynamics, foraging and predator deterrence. I describe the evidence that kin‐selected benefits arise from interacting with kin in each of these contexts, notwithstanding the potential costs of kin competition and inbreeding. I conclude that as the tools required to determine population genetic structure are readily available, measurement of kin structure and the potential for kin selection on a routine basis is likely to reveal that this process has been an important driver of evolutionary adaptation in many non‐cooperative as well as cooperative species.     

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.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.     

Sex‐biased dispersal,kin selection and the evolution of sexual conflict

There is growing interest in resolving the curious disconnect between the fields of kin selection and sexual selection. Rankin's (2011, J. Evol. Biol. 24 , 71–81) theoretical study of the impact of kin selection on the evolution of sexual conflict in viscous populations has been particularly valuable in stimulating empirical research in this area. An important goal of that study was to understand the impact of sex‐specific rates of dispersal upon the coevolution of male‐harm and female‐resistance behaviours. But the fitness functions derived in Rankin's study do not flow from his model's assumptions and, in particular, are not consistent with sex‐biased dispersal. Here, we develop new fitness functions that do logically flow from the model's assumptions, to determine the impact of sex‐specific patterns of dispersal on the evolution of sexual conflict. Although Rankin's study suggested that increasing male dispersal always promotes the evolution of male harm and that increasing female dispersal always inhibits the evolution of male harm, we find that the opposite can also be true, depending upon parameter values.     

Consequences of genetic linkage for the maintenance of sexually antagonistic polymorphism in hermaphrodites

When selection differs between males and females, pleiotropic effects among genes expressed by both sexes can result in sexually antagonistic selection (SA), where beneficial alleles for one sex are deleterious for the other. For hermaphrodites, alleles with opposing fitness effects through each sex function represent analogous genetic constraints on fitness. Recent theory based on single‐locus models predicts that the maintenance of SA genetic variation should be greatly reduced in partially selfing populations. However, selfing also reduces the effective rate of recombination, which should facilitate selection on linked allelic combinations and expand opportunities for balancing selection in a multilocus context. Here, I develop a two‐locus model of SA selection for simultaneous hermaphrodites, and explore the joint influence of linkage, self‐fertilization, and dominance on the maintainance of SA polymorphism. I find that the effective reduction in recombination caused by selfing significantly expands the parameter space where SA polymorphism can be maintained relative to single‐locus models. In particular, linkage facilitates the invasion of male‐beneficial alleles, partially compensating for the “female‐bias” in the net direction of selection created by selfing. I discuss the implications of accounting for linkage among SA loci for the maintenance of SA genetic variation and mixed mating systems in hermaphrodites.