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Gardner A (in press) Inclusive fitness for the conflicted individual. Journal of Evolutionary Biology.

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.

Kam CI, Ruxton GD & Gardner A (in press) The evolution of socially modulated dispersal. Journal of Theoretical Biology. 

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.

Gardner A & Barteškaitė E (2025) Choosy dispersal promotes the evolution of altruism. Biology Letters 21, 20250589.

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.

Twyman KZ & Gardner A (in press) A formal theory of group-level adaptation for obligate eusociality. Journal of Evolutionary Biology.
 

Darwin argued that natural selection leads organisms to appear as if they are striving to maximise their fitness. This idea is readily recognised at the individual cell or body level, but such adaptive design may also manifest at some higher levels of biological organisation. Previous work has formalised 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 conceptualised 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 optimisation—wherein the colony is considered a fitness-maximising 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. (Image: Gemini)

Chokechaipaisarn C & Gardner A (in press) The consequences of constrained sex allocation in diploids and haplodiploids under local mate competition. Journal of Evolutionary Biology https://doi.org/10.1093/jeb/voaf088

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 two-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.

Baird RB, Hitchcock TJ, Ševčik J, Monteith KM, Gardner A, Ross L & Mongue AJ (2025) Faster adaptation but slower divergence of X chromosomes under paternal genome elimination. Nature Communications 16, 5288.

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.

Twyman KZ & Gardner A (in press) The clonality window: relatedness and the group covariance effect in the evolution of division of labour. Evolution. https://doi.org/10.1093/evolut/qpaf093

 

 

Cellular division of labour 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 towards division of labour 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 labour. We recover the covariance effect, revealing that it is a consequence of cells sharing the products of their labours 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 favours 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 labour is favoured by natural selection, such that the ‘clonality window’ is also a prerequisite for division of labour in Michod’s trade-off scenario. (Image: ChatGPT)

Scott TW, Wild G & Gardner A (in press) Kin-discriminating partner choice promotes the evolution of helping. Evolution.

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 towards 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. (Image: ChatGPT)

 

Dong B & Gardner A (2025) Kin competition drives the evolution of earlier metamorphosis. Ecology and Evolution 15, e70806.

Metamorphosis, 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.

 

Chokechaipaisarn C & Gardner A (2024) Density-dependent dispersal reduces conflict over the sex ratio. Biology Letters 20, 20240378.

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.