How to balance the offspring quality–quantity tradeoff when environmental cues are unreliable

Maternal effects on offspring size can have a strong effect on fitness, as larger offspring often survive better under harsh environmental conditions. Selection should hence favour mothers that find an optimal solution to the offspring size versus number tradeoff. If environmental conditions are variable, there will not be a single optimal offspring size, as predicted in a constant environment, but plastic responses can be favoured. To be able to adjust offspring size in an adaptive manner, mothers have to use environmental cues to predict offspring environmental conditions. Cues can be unreliable, however, particularly in species where individuals occupy different niches at different life stages. Here we model the evolution of plasticity of offspring size when the environmental cues mothers use to predict the conditions experienced by their offspring are not perfectly reliable. Our results show that plastic strategies are likely to be superior to fixed strategies in a stochastically varying environment when the environmental cues are at least moderately reliable, with the threshold depending on plasticity costs and the difference of resources available to mothers. Plasticity is more likely to occur if resource availability is not too different between environments. For any given scenario, plasticity in offspring size is favoured if offspring survival varies greatly between environmental states. Whenever plastic strategies are optimal, the occurring switches performed by mothers between small and large offspring are predicted to be substantial, as small adjustments are unlikely to reap fitness benefits great enough to overcome the costs of plasticity.     

Coevolutionary dynamics of polyandry and sex‐linked meiotic drive

Segregation distorters located on sex chromosomes are predicted to sweep to fixation and cause extinction via a shortage of one sex, but in nature they are often found at low, stable frequencies. One potential resolution to this longstanding puzzle involves female multiple mating (polyandry). Because many meiotic drivers severely reduce the sperm competitive ability of their male carriers, females are predicted to evolve more frequent polyandry and thereby promote sperm competition when a meiotic driver invades. Consequently, the driving chromosome's relative fitness should decline, halting or reversing its spread. We used formal modeling to show that this initially appealing hypothesis cannot resolve the puzzle alone: other selective pressures (e.g., low fitness of drive homozygotes) are required to establish a stable meiotic drive polymorphism. However, polyandry and meiotic drive can strongly affect one another's frequency, and polyandrous populations may be resistant to the invasion of rare drive mutants.     

Bet-hedging--a triple trade-off between means, variances and correlations

In unpredictably varying environments, strategies that have a reduced variance in fitness can invade a population consisting of individuals that on average do better. Such strategies 'hedge their evolutionary bets' against the variability of the environment. The idea of bet-hedging arises from the fact that appropriate measure of long-term fitness is sensitive to variance, leading to the potential for strategies with a reduced mean fitness to invade and increase in frequency. Our aim is to review the conceptual foundation of bet-hedging as a mechanism that influences short- and long-term evolutionary processes. We do so by presenting a general model showing how evolutionary changes are affected by variance in fitness and how genotypic variance in fitness can be separated into variance in fitness at the level of the individuals and correlations in fitness among them. By breaking down genotypic fitness variance in this way the traditional divisions between conservative and diversified strategies are more easily intuited, and it is also shown that this division can be considered a false dichotomy, and is better viewed as two extreme points on a continuum. The model also sheds light on the ideas of within- and between-generation bet-hedging, which can also be generalized to be seen as two ends of a different continuum. We use a simple example to illustrate the virtues of our general model, as well as discuss the implications for systems where bet-hedging has been invoked as an explanation.     

The opportunity to be misled in studies of sexual selection

It is a challenge to measure sexual selection because both stochastic events (chance) and deterministic factors (selection) generate variation in individuals' reproductive success. Most researchers realize that random events ('noise') make it difficult to detect a relationship between a trait and mating success (i.e. the presence of sexual selection). There is, however, less appreciation of the dangers that arise if stochastic events vary systematically. Systematic variation makes variance-based approaches to measuring the role of selection problematic. This is why measuring the opportunity for sexual selection (I(s) and I(mates)) is so vulnerable to misinterpretation. Although I(s) does not measure actual sexual selection (because it includes stochastic variation in mating/fertilization success) it is often implicitly assumed that it will be correlated with the actual strength of sexual selection. The hidden assumption is that random noise is randomly distributed across populations, species or the sexes. Here we present a simple numerical example showing why this practice is worrisome. Specifically, we show that chance variation in mating success is higher when there are fewer potential mates per individual of the focal sex [i.e. when the operational sex ratio (OSR), is more biased]. This will lead to the OSR covarying with I(s) even when the strength of sexual selection is unaffected by the OSR. This can generate false confidence in identifying factors that determine variation in the strength of sexual selection. We emphasize that in nature, even when sexual selection is strong, chance variation in mating success is still inevitable because the number of mates per individual is a discrete number. We hope that our worked example will clarify a recent debate about how best to measure sexual selection.     

Mate limitation causes sexes to coevolve towards more similar dispersal kernels

Sex‐specific dispersal behavior has been documented in a wide range of different species. Avoidance of inbreeding and kin competition as well as different benefits of philopatry have been invoked as explanations for these patterns. All of these factors have, however, focused on explaining why dispersal behavior differs between the sexes. In this paper, we make the case that dispersal causes an increase in spatial variability in the sex ratio which can reduce the local availability of mates, and thus feed back to influence the evolution of sex‐specific dispersal and lead to more, rather than less, similar dispersal behavior in the sexes. We investigate this mechanism in two different models, first in a conceptually simple case showing why the coevolutionary effect arises, second in an individual‐based model where we model a population in explicit space with dispersal implemented as dispersal kernels. While our mechanism is not expected to completely remove sex‐bias in dispersal, it can act alongside other selection pressures to reduce such biases. Our model thus shows that dispersal of one sex can have an effect on the selective pressures on the opposite sex, without implementing inbreeding avoidance or differential benefits or costs of dispersal.     

Female choice selects for lifetime lekking performance in black grouse males

''Good genes'' models assume that females can use a signal such as mating effort to assess a male''s lifetime fitness. Inferring long-term performance from short-term behavioural observations can be unreliable, and repeated sampling may be needed for more accurate assessment of males. Additionally, if sexual advertisement is viewed as a life-history trait subject to trade-offs, reliable comparison of mates should yield information on all life-history components rather than on one trait value in one season. We show that in the lekking black grouse (Tetrao tetrix), a male''s success is best explained by assuming that females are informed of the past history of males up to the beginning of the study (eight years). Much of this extremely lasting ''memory'' can be attributed to females observing long-term outcomes of male–male competition: current territory position is the only momentarily observable variable that has high power in predicting female choice, and it correlates to a male''s past lekking effort on a cumulative lifetime scale. We conclude that females can use territory position as a signal that conveys information of a male''s lifetime performance that combines lekking effort and longevity. Females may thus overcome the problem of male allocations varying in time, without the need to pay costs associated with repeated sampling.     

The hawk–dove game in a sexually reproducing species explains a colourful polymorphism of an endangered bird

The hawk–dove game famously introduced strategic game theory thinking into biology and forms the basis of arguments for limited aggression in animal populations. However, aggressive ‘hawks’ and peaceful ‘doves’, with strategies inherited in a discrete manner, have never been documented in a real animal population. Thus, the applicability of game-theoretic arguments to real populations might be contested. Here, we show that the head-colour polymorphism of red and black Gouldian finches (Erythrura gouldiae) provides a real-life example. The aggressive red morph is behaviourally dominant and successfully invades black populations, but when red ‘hawks’ become too common, their fitness is severely compromised (via decreased parental ability). We also investigate the effects of real-life deviations, particularly sexual reproduction, from the simple original game, which assumed asexual reproduction. A protected polymorphism requires mate choice to be sufficiently assortative. Assortative mating is adaptive for individuals because of genetic incompatibilities affecting hybrid offspring fitness, but by allowing red ‘hawks’ to persist, it also leads to significantly reduced population sizes. Because reductions in male contributions to parental care are generally known to lead to lower population productivity in birds, we expect zero-sum competition to often have wide ranging population consequences.     

Mate‐sampling costs and sexy sons

Costly female mating preferences for purely Fisherian male traits (i.e. sexual ornaments that are genetically uncorrelated with inherent viability) are not expected to persist at equilibrium. The indirect benefit of producing ‘sexy sons’ (Fisher process) disappears: in some models, the male trait becomes fixed; in others, a range of male trait values persist, but a larger trait confers no net fitness advantage because it lowers survival. Insufficient indirect selection to counter the direct cost of producing fewer offspring means that preferences are lost. The only well‐cited exception assumes biased mutation on male traits. The above findings generally assume constant direct selection against female preferences (i.e. fixed costs). We show that if mate‐sampling costs are instead derived based on an explicit account of how females acquire mates, an initially costly mating preference can coevolve with a male trait so that both persist in the presence or absence of biased mutation. Our models predict that empirically detecting selection at equilibrium will be difficult, even if selection was responsible for the location of the current equilibrium. In general, it appears useful to integrate mate sampling theory with models of genetic consequences of mating preferences: being explicit about the process by which individuals select mates can alter equilibria.