The theory of inclusive fitness explains the process and purpose of social adaptation. However, the canonical derivation of inclusive fitness assumes a simple causal relationship between genotype and phenotype. In reality, different components of the genotype may have different impact upon the phenotype and different genetic relatedness to social partners, as for example in the case of parent-of-origin effects that have been implicated in the evolution of genomic imprinting and a diversity of pathological phenotypes. Whilst such scenarios may be framed in terms of a clash of inclusive-fitness interests of different genes or different genetic factions, it remains unclear whether and how an individual's inclusive fitness may be defined in the context of such internal conflicts. Here, I investigate how the derivation of inclusive fitness is affected in the context of an individual suffering from internal conflict between her maternal-origin versus paternal-origin genes. I show that, in relation to a single conflicted trait, the individual's inclusive fitness is given as a weighted average of the interests of the underlying genetic factions, with the power wielded by each faction providing the appropriate weight. This reveals that internal conflict per se does not erode the adaptive integrity of the individual. Rather, it is variation in the underlying balance of power across different traits that leads to a breakdown of the individual's unity of purpose.

Natural selection might favour brightly coloured males and drab females. A male and a female might disagree about whether to mate. Such tensions are often described as 'sexual conflict' of two forms: intralocus and interlocus. However, this framing unites two very different evolutionary processes: genetic constraint and social conflict, in which male and female fitness are linked by shared genetics or by shared social interactions, respectively. We suggest that coupling both under the banner of 'sexual conflict' is not justified and impedes progress. This problem has become acute as researchers explore the mechanistic underpinnings of both phenomena and as conflation emerges in other research. We propose that a conceptual uncoupling of 'sexual conflict' into true sexual conflict and sexual pleiotropy is needed. Here, we (i) clarify the distinction between conflict and pleiotropy, using evolutionary theory; (ii) show how current conceptual coupling has led to faulty predictions, misdirected research efforts and missed opportunities; (iii) detail how interlocus and intralocus terms have added to confusion; and (iv) establish links with other areas of biology. We show the potential scientific advances that can emerge from disentangling conflict and pleiotropy in biodiversity, molecular genetic and ecological research.

Dispersal plays a key role in ecology and evolutionary biology, including as a mechanism that reduces local competition. However, dispersers often suffer a fitness disadvantage relative to nondispersers, which may lead individuals to prefer that others disperse rather than dispersing themselves. Hence, if individuals can force their neighbours to disperse, they may be favoured to do so rather than voluntarily dispersing for the good of others. Besides forcing dispersal, individuals might also improve their neighbours’ ability to disperse. Here, we investigate the evolutionary drivers and consequences of socially modulated dispersal. We find that: (1) there are three possible stable evolutionary outcomes, involving only voluntary dispersal, only socially modulated dispersal, or coexistence of the two; (2) although social modulation that does not improve dispersal success can only be favoured if it is less costly than dispersal itself, social modulation that facilitates dispersal can be favoured even if it is highly expensive for the facilitator; (3) facilitated dispersal may, counterintuitively, lead to a reduced overall level of dispersal; and (4) social modulation can be either welcome or unwelcome from the perspective of the disperser. These predictions emphasise that the evolution of dispersal depends on individuals’ abilities to both disperse and modulate.

Darwin argued that natural selection leads organisms to appear as if they are striving to maximize their fitness. This idea is readily recognized at the individual cell or body level, but such adaptive design may also manifest at some higher levels of biological organization. Previous work has formalized the idea that social groups can be viewed as adaptive individuals in their own right-i.e., "superorganisms"-under the assumptions that within-group selection is absent and that there is no class structure. However, the original and most common biological use of the term "superorganism" is in reference to insect colonies in which members exhibit striking class structure in the form of reproductive division of labour. Accordingly, although obligately eusocial colonies are regularly conceptualized as having the capacity for colony-level adaptation, current formalisms are unable to support this idea. Here, we develop a formal theory of group-level adaptation for obligately eusocial colonies by establishing mathematical correspondences that connect the dynamics of natural selection-as described by Price's equation-to the mathematics of optimization-wherein the colony is considered a fitness-maximizing agent-under a range of assumptions as to which members of the colony control its phenotype and the degree to which they are genetically related.

Altruistic behaviour is evolutionarily favoured through the action of kin selection. A simple mechanism for kin selection is population viscosity, whereby individuals do not move very far over the course of their lives, such that even indiscriminate helping of neighbours is liable to benefit one's genetic relatives. However, population viscosity is also associated with intensified resource competition among kin, which acts to inhibit the evolution of altruism. In standard models of population structure, these opposing effects of viscosity exactly cancel so that the evolutionary potential for altruism is completely invariant with respect to the rate of dispersal. Here, we investigate the consequences of load-balancing dispersal-whereby dispersers exhibit a preference for settling in less-crowded areas-for the evolution of altruism. Using mathematical modelling and individual-based computer simulations, we find that load-balancing dispersal dramatically reduces the kin-competition consequences of altruism, and thereby strongly promotes the evolution of altruism in viscous populations. We discuss other implications of such load-balancing dispersal for social evolution.

ABSTRACTMetamorphosis, the discrete morphological change between postembryonic life stages, is widespread across the animal kingdom. The suggested advantages of metamorphosis have usually been framed in terms of population benefits, i.e., ecological explanations. In contrast, evolutionary explanations concern whether and how metamorphosis spreads through a population owing to individual‐fitness benefits. However, how kin selection modulates evolution of metamorphosis remains to be investigated formally. Here we develop a mathematical model to investigate how kin selection shapes the optimal timing of metamorphosis from foraging, non‐reproductive larva to reproductive adult, when larvae tend to cluster with their genetic relatives. We consider the full range of larval competition intensities—from no competition to full competition—and the full range of relatedness coefficients—from unrelated to clonality. We provide testable predictions as to how kin selection modulates the timing of metamorphosis, as well as a conceptual framework within which empirical observations may be understood.

Cellular division of labor is closely associated with the emergence of organismality in the evolution of obligate multicellularity. Michod has suggested that a trade-off between viability and fecundity may-through a "group covariance effect"-lead to a group's fitness being augmented above the average of its constituents' fitnesses, offering a first step toward division of labor and obligate multicellularity. However, it is difficult to see how a group's fitness could be different from the aggregate of its constituents. Here, we investigate the same fitness trade-off and its consequences for division of labor. We recover the covariance effect, revealing that it is a consequence of cells sharing the products of their labors and clarifying that the group's fitness remains equal to the aggregate of the fitnesses of its constituent cells. We show that the covariance effect imparts an inclusive-fitness benefit for cells that share, but that-all else being equal-natural selection favors sharing only when groupmates are genetically identical, yielding a "clonality window." Lastly, we find that sharing is a critical determinant as to whether division of labor is favored by natural selection, such that the "clonality window" is also a prerequisite for division of labor in Michod's trade-off scenario.

Differences in transmission and ploidy between sex chromosomes and autosomes drive divergent evolutionary trajectories, with sex chromosomes generally evolving faster. Because sex-linked genes are transmitted less frequently, they are under less efficient selection. Conversely, exposure of recessive mutations on haploid sex chromosomes creates more efficient selection. In most systems, these effects occur simultaneously and are confounded. The fly families Sciaridae (fungus gnats) and Cecidomyiidae (gall midges) have X0 sex determination, but males transmit only maternally inherited chromosomes. This phenomenon results in equal transmission of the X and autosomes, allowing the effect of haploid selection to be studied in isolation. We discover that, unlike well-studied systems, X chromosomes diverge more slowly than autosomes in these flies. Using population genomic and expression data, we show that despite the X evolving more adaptively, stronger purifying selection explains slower divergence. Our findings demonstrate the utility of non-Mendelian inheritance systems for understanding fundamental evolutionary processes.

Kin selection theory predicts that individuals should evolve to help relatives, either by helping indiscriminately in a population where they do not move very far from their relatives, or by discriminating kin and conditionally helping them. It has been argued that, because kin discrimination enables individuals to reduce how helpful they are with some social partners as well increase how helpful they are with others, this could lead to an increase or a decrease in the overall level of helping. Specifically, it was argued that kin discrimination would increase the overall level of helping if the function relating the optimal level of help and genetic relatedness is convex, but kin discrimination would decrease the overall level of helping if the function relating the optimal level of help and genetic relatedness is concave. However, this prediction was based on a model in which individuals were not able to choose their social partners but only adjust how helpful they should be toward those social partners they have been allocated. Here, we perform a mathematical analysis showing that being able to choose social partners increases the overall level of helping. Consequently, if kin discriminators are allowed to choose whom they help, kin discrimination is more likely to increase the overall level of helping than previously anticipated. We obtained these results in two complementary theoretical settings: one more general, which makes few demographic assumptions, and the other more specific and concrete, which assumes a patch-structured population with complete dispersal.

Unmated females in haplodiploid populations may enjoy reproductive success but with the constraint that all their offspring-developing from unfertilised eggs-are male. The presence of such females, constrained to produce only male offspring, is expected to lead to a corresponding female bias being favoured among the offspring of unconstrained females. Godfray (J Evol Biol 3, 3-17) derived a mathematical expression for the unbeatable sex allocation strategy for unconstrained females in the context of local mate competition in 2-foundress patches, and concluded that there is negligible impact of the presence of constrained females on the unbeatable sex allocation of unconstrained females. However, Godfray's result assumes diploid-rather than haplodiploid-genetics and his derivation contains a mathematical error. We correct Godfray's error and extend his model to incorporate haplodiploid genetics. This results in a more substantial impact of constrained females on the sex allocation behaviour of unconstrained females under local mate competition.

Haplodiploids—in particular, wasps—are the workhorses of sex-allocation research. This is owing to their unusual system of sex determination, which provides a ready means of sex ratio adjustment. Notably, their sexually asymmetrical mode of genetic inheritance leads mothers and fathers to come into conflict over the sex ratio of their offspring. In the simplest outbreeding scenario, a mother is favoured to employ an even sex ratio while a father prefers that all his mate’s offspring are female. An important modulator of evolutionary conflict between mating partners is genetic relatedness, raising the possibility that this sex ratio conflict is reduced in low-dispersal settings with mating occurring between relatives. However, the impact of population viscosity on sex ratio conflict in haplodiploids remains unknown. Here, we develop and analyse a kin-selection model to investigate how the rate of dispersal modulates sex ratio conflict in a haplodiploid, viscous population setting. We find that population viscosity is associated with a reduction in the extent of sex ratio conflict—the effect being very weak under density-independent dispersal and much stronger under density-dependent dispersal.

Recent years have seen renewed interest in the role of religious systems as drivers of the evolution of cooperation in human societies. One suggestion is that a cultural tradition of ancestor worship might have evolved as a "descendant-leaving strategy" of ancestors by encouraging increased altruism particularly between distant kin. Specifically, Coe and others have suggested a mechanism of cultural transmission exploiting social learning biases, whereby ancestors have been able to establish parental manipulation of kin recognition and perceived relatedness as a traditional behavior, leading to increased altruism among co-descendants and thereby maximizing the ancestor's long-term inclusive fitness. Here, we develop a demographically explicit model in order to quantify the resulting increase in altruism and concomitant "ancestor-descendant conflict", and to determine the evolutionary feasibility of religiously motivated cultural norms that promote altruism among co-descendants. Our analysis reveals that such norms could indeed drive an overall increase in altruism with potential for ancestor-descendant conflict, particularly in low-dispersal settings. Moreover, we find that natural selection can favor traditions encouraging increased altruism towards co-descendants under a range of conditions, with the inclusive-fitness costs of enacting an inappropriately high level of altruism being offset by inclusive-fitness benefits derived from the cultural tradition facilitating kin recognition.

Sex chromosomes differ from autosomes in both their ploidy and transmission genetics. Consequently, selection, mutation, and drift may act differently upon them, driving distinct patterns in genetic divergence, diversity, and gene content. Recently, researchers have begun to consider a wider set of organisms with non-standard inheritance and sex-determination systems, however in many cases we lack theory which extends to such cases. One such example is paternal genome elimination (PGE), an unusual reproductive system which has independently evolved in two fly families, the fungus gnats (Sciaridae) and gall midges (Cecidomyiidae), and one order of springtails (Symphypleona). Under PGE, males receive but do not transmit a paternal genome, such that the autosomes and X chromosomes exhibit the same transmission genetics, but with different somatic ploidy. This makes them uniquely suited to test hypotheses about the role of haploid selection in males. Additionally, repeatedly throughout these groups a novel sex determination system - monogeny - has evolved, whereby females produce broods of exclusively one sex. The genetic basis of monogeny partitions the X chromosome into three segments, all displaying distinct inheritance patterns. Here we develop a series of theoretical models adapted to the genetics of these groups, generating testable predictions as to the relative genetic diversity within populations, and divergence between populations. Our results suggest that these species are excellent systems with which to test many fundamental principles in evolutionary genetics. ### Competing Interest Statement The authors have declared no competing interest.

The frequency of left-handedness in humans is ∼10% worldwide and slightly higher in males than females. Twin and family studies estimate the heritability of human handedness at around 25%. The low but substantial frequency of left-handedness has been suggested to imply negative frequency-dependent selection, e.g. owing to a “surprise” advantage of left-handers in combat against opponents more used to fighting right-handers. Because such game-theoretic hypotheses involve social interaction, here, we perform an analysis of the evolution of handedness based on kin-selection, which is understood to play a major role in the evolution of social behaviour generally. We show that: (1) relatedness modulates the balance of right-handedness versus left-handedness, according to whether left- handedness is marginally selfish versus marginally altruistic; (2) sex differences in relatedness to social partners may drive sex differences in handedness; (3) differential relatedness of parents and offspring may generate parent-offspring conflict and sexual conflict leading to the evolution of maternal and paternal genetic effects in relation to handedness; and (4) differential relatedness of maternal-origin versus paternal-origin genes may generate intragenomic conflict leading to the evolution of parent-of-origin-specific gene effects—such as “genomic imprinting”—and associated maladaptation.