Abstract Population genetic models excel at identifying the conditions for polymorphisms based on balancing selection but typically disregard the ecological processes that yield particular values of selection coefficients. We model a system that combines antagonistic pleiotropy, dominance reversal and heterozygote advantage: the wood tiger moth Arctia plantaginis , where alternative haplotypes at a major-effect locus determine male hindwing coloration. Yellow offers better protection against predators, while white is often associated with better mating success. The effects of mortality and reproductive success overlap in time because protandrous males can mate as long as they are alive, but they need to avoid predation for several days before the bulk of females emerge. We show that protandry aids polymorphism maintenance whenever the second-fittest genotype (after the heterozygote) is the poorly surviving but mating advantaged homozygote, while increased protandry harms polymorphism when the second-best fitness is that of the survival advantaged morph. Ecologically plausible protandry times predict that dominance reversal does not have to be strong for polymorphism to be maintained. Our study highlights the importance of timing traits in maintaining polymorphisms in Lepidoptera and showcases the benefits of deriving fitness explicitly in place of abstract selection coefficients that lack temporal components within the life cycle.

Many species of Colias butterflies show a female-limited colour polymorphism where the dominant Alba allele leads to white wings, faster development and higher fecundity (hypothesized to arise from not allocating resources to pteridine pigment production), while orange females are more attractive to males. Attractiveness can benefit females because males provide nutrient-rich spermatophores. Despite decades of research and a long-standing understanding of the associated life-history trade-off, earlier modelling work has been unable to show how this trade-off could generate frequency-dependent selection. We construct a model that shows the importance of phenology for this polymorphism's stability. When generations are non-overlapping or partially overlapping, and there is an eclosion order where males precede Alba females that precede orange females, females use partially distinct temporal niches. Theory on temporal niches, however, is known not to automatically guarantee coexistence; translated to our case, Alba monopolization of males early in the season might simply deplete mate availability for late-eclosing orange females. However, with sufficiently high male ability to replenish spermatophores, we find negative frequency-dependence where competition intensifies mainly within a morph if it becomes common. In summary, given realistic assumptions, the trade-off between development time and attractiveness can maintain a stable polymorphism in Colias butterflies. This article is part of the theme issue 'Exploring negative frequency dependent selection across levels: from genetics to ecology and back again'.

Host dispersal influences how frequently a parasite encounters new susceptible hosts, which translates into potential conflict between parasite and host interests regarding dispersal. In vertically transmitted parasites, the impact of host dispersal on parasite spread appears limited. Here, it is less intuitive whether parasites can benefit by manipulating host dispersal and, if so, whether they would evolve to increase or decrease host dispersal. We examine host-parasite conflict over dispersal using the case of the African monarch butterfly (Danaus chrysippus) and the male-killing Spiroplasma as inspiration. Male-killing endosymbionts transmit vertically from host females to their offspring and infected male offspring die. We contrast spread of a male-killing endosymbiont with a hypothetical scenario in which the parasite can additionally manipulate host dispersal. We show that a dispersal-manipulating male killer can switch the system from an overall male-biased dispersal pattern to a female-biased one. Interestingly, while infected females disperse most, the strongest evolutionary response occurs in uninfected females, which evolve towards philopatry (relative to a scenario where parasites cannot manipulate hosts). Our work thus uncovers a novel context where the phenotypic effect of parasitism is strongest in individuals that are not at risk of ever being parasitized.

Multi-level selection and senescence do not at first sight have much in common. Here, we demonstrate that the emergent mortality patterns generated by demographic senescence can be understood as the product of multi-level selection. We formulate a two-level Moran type process and use its scaling limits to illustrate that a simple mathematical framework that models multi-level selection in group-structured populations also models damage accumulation patterns and resultant mortality curves in ageing organisms. To verbally make the connection, observe that defectors spread within a group consisting of cooperators and defectors; when groups compete against each other, defector-rich groups suffer, and between-group selection causes such groups to be systematically under-represented. Exactly analogously, senescing individuals accumulate damage to physiological sub-systems, and `damage begets damage'; individuals who are more damaged are more likely to die, hence damage-rich individuals are systematically under-represented in later age classes. Thus, emergent senescence patterns in complex, integrated organisms are formally equivalent to the patterns generated by a within-generation multi-level selection process in which intra-organismal sub-systems play the role of particles, organisms play the role of collectives, and selective disappearance plays the role of group selection.

The universality of the trade-off between fecundity and longevity in life-history theory is sometimes contested. Social insects present the arguably strongest challenge, as (i) queens not only monopolize reproduction, but also live much longer than workers, and (ii) within a caste, those individuals that lay more eggs are also observed to live longer. Positive fecundity-longevity relationships can appear in observational data even though an underlying trade-off exists, as individual variation in resource acquisition (e.g., variation in habitat quality) can mask the trade-off. Here, we demonstrate theoretically that the fecundity-longevity trade-off in social insects can be easily masked even without differences in individual quality. Demographic stochasticity, caused by variable worker lifespans, leads to self-reinforcing dynamics (equivalent to the well-known Matthew effect), where "lucky" colonies exhibit healthy growth and long-lived, productive queens, while "unlucky" colonies show the opposite combination of traits. Allocation variation between individual queens, if present, can unmask the trade-off in principle, but the trade-off remains commonly concealed not only when measuring fecundity as a cumulative total (a strongly confounded measure as longer-lived queens have more time to produce eggs), but also when measuring fecundity as a rate. Our results help align superorganismal fitness components with general life-history principles, and highlight the necessity of experimental manipulations when making statements regarding trade-offs or the lack thereof.

Genetic trade-offs-which occur when variants that are beneficial in some contexts of natural selection are harmful in others-can influence a wide range of evolutionary phenomena, from the maintenance of genetic variation to the evolution of aging and sex differences. An extensive body of evolutionary theory has focused on the consequences of such trade-offs, and recent analyses of Fisher's geometric model have further quantified the expected proportion of new mutations that exhibit trade-offs. However, the theory remains silent regarding the prevalence of trade-offs among the variants that contribute to adaptation. Here, we extend Fisher's geometric model to predict the prevalence of trade-offs among the adaptive mutations that become established or fixed in a population. We consider trade-offs between sexes, habitats, fitness components, and temporally fluctuating environments. In all 4 scenarios, trade-off alleles are consistently under-represented among established relative to new beneficial mutations-an effect that arises from the greater susceptibility of trade-off alleles to genetic drift. Adaptation during a population size decline exacerbates this deficit of trade-offs among established mutations, whereas population expansions dampen it. Consequently, threatened populations should primarily adapt using unconditionally beneficial alleles, while invasive populations are more prone to adaptation using variants that exhibit trade-offs.

A large proportion of arthropod species are infected with endosymbionts, some of which selfishly alter host reproduction. The currently known forms of parasitic reproductive manipulations are male-killing, feminization, cytoplasmic incompatibility, parthenogenesis induction and distortion of sex allocation. While all of these phenomena represent adaptations that enhance parasite spread, they differ in the mechanisms involved and the consequent infection dynamics. We focus here on the latter aspect, summarizing existing theoretical literature on infection dynamics of all known reproductive manipulation types, and completing the remaining knowledge gaps where dynamics have not been modelled yet. Our unified framework includes the minimal model components required to describe the effects of each manipulation. We establish invasion criteria for all potential combinations of manipulative endosymbionts, yielding predictions for an endosymbiont's increase from rarity within a host population that is initially either uninfected or infected with a different symbiont strain. We consider diplodiploid and haplodiploid hosts, as the mechanisms as well as the infection dynamics of reproductive manipulations can differ between them. Our framework reveals that endosymbionts that a priori have the best invasion prospects are not necessarily the most commonly found ones in nature; priority effects play a role too, and cytoplasmic incompatibility excels in this regard. As a whole, considerations of the ease with which a symbiont spreads have to be complemented with knowledge of how easy it is to achieve a particular manipulation, and with factors influencing the probability that interspecific host switching occurs and succeeds.

Our understanding of sex-biased helping has progressed from a historical emphasis on relatedness differences caused by haplodiploidy to an understanding of the role played by the rarer-sex effect. Theory to date typically assumes that offspring help their mother. We show that an alternative, peer-to-peer cooperation can shed light on the interaction of helpers and the recipients of help. In pine sawfly (Diprion pini) larvae, larval peer-to-peer cooperation takes the form of collective, and individually costly, anti-predator behaviour. Larvae typically occur in mixed-sex groups, but females can lay unfertilized eggs that develop into haploid males, which produce male-only broods. Female-biased sex ratios typically select for female-biased helping, and our model here matches empirical findings. Alternative scenarios provide insight too: (i) if genetic constraints permit no sex-specificity in behaviour beyond haploid males expressing all alleles while helping in females can be recessive or dominant, then the sex difference in helping simply reflects the effects of dominance and (ii) female-biased helping can also emerge under male-biased sex ratios, if males are mostly produced in single-sex broods by unmated mothers. While this last example remains hypothetical for D. pini, it highlights an underappreciated point: the rarer-sex effect impacts solutions not only by modifying fitness prospects of the helper, but also of the recipient of help.

Temporal niches do not automatically promote coexistence. We combine field data on the marine midge Clunio marinus with a model. In Roscoff (Brittany, France) sympatric C. marinus timing strains emerge at full moon (FM strain) or just before new moon (NM strain). We show that NM individuals reproduce and lay eggs when the water level is higher than during FM strain reproduction, and that this shift partially segregates larvae according to elevation. Modelling the underlying dynamics shows that the causality from temporal to spatial niches is crucial for coexistence: for hypothetical strains which differ in the temporal niche used for reproduction so that they use equivalently low water levels for egg-laying, the dynamics show priority effects, not coexistence. While general theory on temporal niches is rather complex, we highlight the understudied possibility that timing traits cause differences in space use, and coexistence is unproblematic as it results from spatial niches.

While niche differences aid coexistence, the role of temporal niches is complex. A recent study (Stump & Vasseur, 2023) casts doubt on the idea that species coexist easily if they partition abiotic niches that vary in time. The storage effect, which aids coexistence, requires that species differ in what is a 'good year', and that the benefits that the currently common species can draw from its own good year become limited due to intraspecific competition. The recent re-evaluation of temporal niches considered Allee effects only fleetingly. We complement their work by providing a case study of the marine midge Clunio marinus, where coexistence appears to occur in nature, is associated with a strong difference in timing traits, and also features Allee effects because rare timing phenotypes emerge with limited mating opportunities. The larvae develop in the sea, and adults emerge and mate during the lowest low tides. These tides coincide with either the full or the new moon, and genetically determined strains use either one of them, or both, for emergence. A 'good year' in this system translates into a particular low tide. Allee effects create strain-specific good tides if the risk of hybridization is greater for the currently rare strain, which mates more often with another strain, than the currently common strain. We are able to investigate this effect by varying the effects of hybridization in our model of Clunio biology. Temporal niches, mate-finding Allee effects, hybridization possibilities and a potential growth-survival tradeoff do not easily combine to yield stable coexistence. Most factors instead promote positive frequency dependence, leading to priority effects. Ontogenetic niche shifts among larvae deviate from this result: if suitably timed, they are able to concentrate competition in a coexistence-promoting manner. Our study thus complements and strengthens Stump and Vasseur's conclusion that a finding of temporal niche differentiation should not be straightforwardly assumed to be an explanation for the coexistence of two or more morphs or species. We encourage linking temporal niche studies with those of priority effects, as well as the study of other coexistence mechanisms that may operate within systems that feature temporal niches.

Ubiquity of cancer across the tree of life yields opportunities to understand variation in cancer defences across species. Peto's paradox, the finding that large-bodied species do not suffer from more cancer despite having more cells at risk of oncogenic mutations compared to small species, can be explained if large size selects for better cancer defences. Since birds live longer than non-flying mammals of equivalent size, and are descendants of moderate-sized dinosaurs, we ask whether ancestral cancer defences are retained if body size shrinks in a lineage. Our model derives selection coefficients and fixation events for changes in cancer defences over macroevolutionary time, based on known relationships between body size, cancer risk, extrinsic mortality, metabolic rate, and effective population size. We show that, if mutation rate is sufficiently high and cancer defences are costly, we expect birds to have lower cancer defences than their dinosaurian ancestors. However, if the evolution of cancer suppression is mutation limited, due to e.g. pleiotropy, birds may have kept excessive dinosaurian cancer defences, possibly explaining their low cancer risk. Counterintuitively, birds can then be 'too robust' for their own good, if excessive cancer suppression requires compromising reproductive rates. Yet, evolutionary innovations such as flight can increase longevity and keep selection for cancer suppression intact in birds, even if flight requires small body size. Retaining dinosaur-level cancer defences can then be adaptive, particularly if the evolution of flight is accompanied by an increase in cancer risk due to metabolic scaling. Overall, our study suggests that studying cancer suppression in birds can reveal alternative mechanisms to those found in mammals, possibly inherited from birds' dinosaurian ancestors.

Sex ratio theory usually assumes obligate sex; rare exceptions with facultative sex typically consider idiosyncratic cases of cyclic parthenogens. Here, we construct a general theoretical framework for facultative parthenogens. We show that facultative parthenogenesis selects for female-biased sex ratios by elevating the class reproductive value of females. The degree of this bias depends on the future rate of parthenogenesis. This complicates calculations for cyclic parthenogens, but in stable environments (with stable rates of parthenogenesis), the optimal sex ratio can result automatically from constraints caused by preexisting sex chromosomes: if sexually produced offspring retain unbiased sex ratios while parthenogenetically produced offspring are female (example: stick insects), optimality is achieved for any rate of parthenogenesis. Conversely, in birds and haplodiploids, parthenogenesis produces males, resulting in suboptimal sex ratios. Nevertheless, male-producing parthenogenesis can invade and reach an equilibrium frequency, if the reproductive value of parthenogenetically produced brood is compromised by less than 50%. We argue that this condition is not met in birds due to inviable WW and homozygous ZZ offspring. For haplodiploids, on the other hand, our work resurrects a somewhat forgotten idea by Bull (1981) that haplodiploidy in Hymenoptera evolved from a diplodiploid ancestor with complementary sex determination.

Dispersal is a well-recognized driver of ecological and evolutionary dynamics, and simultaneously an evolving trait. Dispersal evolution has traditionally been studied in single-species metapopulations so that it remains unclear how dispersal evolves in metacommunities and metafoodwebs, which are characterized by a multitude of species interactions. Since most natural systems are both species-rich and spatially structured, this knowledge gap should be bridged. Here, we discuss whether knowledge from dispersal evolutionary ecology established in single-species systems holds in metacommunities and metafoodwebs and we highlight generally valid and fundamental principles. Most biotic interactions form the backdrop to the ecological theatre for the evolutionary dispersal play because interactions mediate patterns of fitness expectations across space and time. While this allows for a simple transposition of certain known principles to a multispecies context, other drivers may require more complex transpositions, or might not be transferred. We discuss an important quantitative modulator of dispersal evolution-increased trait dimensionality of biodiverse meta-systems-and an additional driver: co-dispersal. We speculate that scale and selection pressure mismatches owing to co-dispersal, together with increased trait dimensionality, may lead to a slower and more 'diffuse' evolution in biodiverse meta-systems. Open questions and potential consequences in both ecological and evolutionary terms call for more investigation. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Immunocompetence evolution can involve a "resistance is futile" scenario if parasite encounter rates are so high that high investment in resistance only marginally delays infection. Here, we investigate two understudied aspects of "futility": the mode of immunocompetence and sexual selection. First, immunocompetence is usefully categorized as reducing the rate of becoming infected (resistance) or reducing the negative fitness consequences of infection once it happened (tolerance). We compare the prospects of futility for resistance, tolerance, and their joint occurrence, showing that resistance futility arises with respect to parasite encounter rates, while tolerance futility arises with respect to parasite virulence. However, if the same host trait improves pleiotropically both resistance and tolerance, futility disappears altogether and immunity investment remains profitable when increasing parasite encounter rates, virulence, or both. Second, we examine how sexual selection strength impacts these findings. If one sex (typically males) is near the faster end of a fast-slow continuum of life histories, then life history patterns reflecting futility can evolve sex-specificity. The solutions often feature sexual dimorphism in immunocompetence, but not always in the direction of strong sexual selection yielding low immunity: sexual selection can select for faster and "sicker" lives, but if sexual selection also favors traits that impact parasite encounter rates, the results are strongly dependent on whether futility (along any axis) plays a role. Intuition suggests that investment in immunity is higher when hosts frequently encounter parasites. While there are examples that confirm this, in other cases, hosts have been shown to abandon immune defenses under high parasite pressure. We reconcile these findings by modeling the optimal host resource allocation towards immunity under varying parasite pressure and strength of sexual selection. Our results show two axes along which immunity investments are futile and should therefore be abandoned in favor of investing in reproduction: resisting infection becomes futile under high parasite abundance, while tolerating the harmful effects of infection is not beneficial under ever increasing parasitic virulence. However, investments of organisms that are capable of both resistance and tolerance mechanisms yield fitness payoffs also when parasites are highly virulent and abundant. This work highlights the impact of parasites and immune defenses on optimal immunity investment levels in hosts, an insight which also complements theory on sex-specific immunity.

Antagonistic co-evolution can be asymmetric, where one species lags behind another. Asymmetry in a predator-prey context is expressed by the 'life-dinner principle', a classic informal model predicting that prey should be in some sense ahead in this arms race, since prey are running for their lives, while predators lag as they only run for their dinner. The model has undergone surprisingly little theoretical scrutiny. We derive analytical models that show coevolutionary outcomes do not always align with the life-dinner principle. Our results show that other important asymmetries can easily reverse the outcome, especially the rare-enemy principle: predators are usually outnumbered by their prey, sometimes substantially (trophic asymmetry), which can make selection on prey relatively weak. We additionally show that the antagonists typically exhibit different evolutionary responses to a situation where both predator and prey start out as equally fast runners. Although predators sometimes become so efficient that attacks always succeed, attack success often reaches a stable intermediate value. We conclude that the life-dinner principle has some validity as a metaphor, but its effect is of an 'all else being equal' type, which is surprisingly easily overridden by other features of the evolutionary dynamics.

Game theory is frequently used to study conflicting interests between the two sexes. Males often benefit from a higher mating rate than females do. A temporal component of this conflict has rarely been modelled: females' interest in mating may depend on when females become fertile. This sets conditions for male–female coevolution, where females may develop fertility signals, and males may obey the signal, such that they only target signalling females. Modelling this temporal aspect to sexual conflict yields two equilibria: (i) a trivial equilibrium without signals and with males targeting all females, and (ii) a signalling equilibrium where all females signal before ovulation, and where either some, or all, males obey the signal. The ‘all males obey the signal’ equilibrium is more likely if we assume that discriminating males have an advantage in postcopulatory sperm competition, while in the absence of this benefit, we find the ‘some males obey the signal’ equilibrium. The history of game-theoretic models of sex differences often portrays one sex as the 'winner' and the opposite sex as the ‘loser’. From early models emphasizing ‘battle of the sexes’-style terminology, we recommend moving on to describe the situation as non-signalling equilibria having stronger unresolved sexual conflict than signalling equilibria. This article is part of the theme issue ‘Half a century of evolutionary games: a synthesis of theory, application and future directions’.

In seasonal environments, competition among males can drive males to emerge before females. Females, simultaneously, should avoid emerging at times after sufficient male availability. We show that the consequent sexual conflict over timing traits can produce arms races toward ever earlier emergence, if low mate-search efficiency or sperm limitation elevate the latter risk for females. In reality, however, arms races over timing cannot proceed indefinitely as this ignores the relevant ecological context for phenology: the temporal niche of resource availability for offspring development. We model the interaction of natural and sexual selection to predict the sexual conflict load, i.e., the loss of population fitness caused by sexual conflict. We show that selection to avoid matelessness can exacerbate another problem of maladaptation: a temporal mismatch between the organism (e.g., insect) and its resource (e.g., host plant). Load frequently associates with protandry if males can mate multiply, yet lack of multiple mating does not imply zero load. A temporal mismatch can still evolve, where both sexes emerge and mate suboptimally early with respect to the seasonal resource peak, because monogamy does not guarantee that every individual finds one mate, and selection favors early individuals in mate-finding contexts.

Do environments or species traits that lower the mortality of individuals create selection for delaying senescence? Reading the literature creates an impression that mathematically oriented biologists cannot agree on the validity of George Williams' prediction (who claimed 'yes'). The abundance of models and opinions may bewilder those that are new to the field. Here we provide heuristics as well as simple models that outline when the Williams prediction holds, why there is a ‘null model’ where extrinsic mortality does not change the evolution of senescence at all, and why it is also possible to expect the opposite of William’s prediction, where increased extrinsic mortality favours slower senescence. We hope to offer intuition by quantifying how much delaying the ‘placement’ of an offspring into the population reduces its expected contribution to the gene pool of the future. Our first example shows why sometimes increased extrinsic mortality has no effect (the null result), and why density dependence can change that. Thereafter, a model with ten different choices for population regulation shows that high extrinsic mortality favours fast life histories (Williams) if increasing density harms the production of juveniles or their chances to recruit into the population. If instead increasing density harms the survival of older individuals in a population, then high extrinsic mortality favours slow life histories (anti-Williams). We discuss the possibility that empirically found Williams-like patterns provide indirect evidence for population regulation operating via harming the production or fitness prospects of juveniles, as opposed to the survival of established breeders.