Fluctuating natural selection accounts for the evolution of diversification bet hedging

Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of ‘bet-hedging’ traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination—a model diversification bet-hedging trait—in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing—across 70 intervals throughout five seasons—to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.     

Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants

Understanding the adaptations that allow species to live in temporally variable environments is essential for predicting how they may respond to future environmental change. Variation at the intergenerational scale can allow the evolution of bet-hedging strategies: a novel genotype may be favoured over an alternative with higher arithmetic mean fitness if the new genotype experiences a sufficiently large reduction in temporal fitness variation; the successful genotype is said to have traded off its mean and variance in fitness in order to ‘hedge its evolutionary bets’. We review the evidence for bet-hedging in a range of simple plant systems that have proved particularly tractable for studying bet-hedging under natural conditions. We begin by outlining the essential theory, reiterating the important distinction between conservative and diversified bet-hedging strategies. We then examine the theory and empirical evidence for the canonical example of bet-hedging: diversification via dormant seeds in annual plants. We discuss the complications that arise when moving beyond this simple case to consider more complex life-history traits, such as flowering size in semelparous perennial plants. Finally, we outline a framework for accommodating these complications, emphasizing the central role that model-based approaches can play.     

Experimental evidence for adaptive personalities in a wild passerine bird

Individuals of the same species differ consistently in risky actions. Such ‘animal personality’ variation is intriguing because behavioural flexibility is often assumed to be the norm. Recent theory predicts that between-individual differences in propensity to take risks should evolve if individuals differ in future fitness expectations: individuals with high long-term fitness expectations (i.e. that have much to lose) should behave consistently more cautious than individuals with lower expectations. Consequently, any manipulation of future fitness expectations should result in within-individual changes in risky behaviour in the direction predicted by this adaptive theory. We tested this prediction and confirmed experimentally that individuals indeed adjust their ‘exploration behaviour’, a proxy for risk-taking behaviour, to their future fitness expectations. We show for wild great tits (Parus major) that individuals with experimentally decreased survival probability become faster explorers (i.e. increase risk-taking behaviour) compared to individuals with increased survival probability. We also show, using quantitative genetics approaches, that non-genetic effects (i.e. permanent environment effects) underpin adaptive personality variation in this species. This study thereby confirms a key prediction of adaptive personality theory based on life-history trade-offs, and implies that selection may indeed favour the evolution of personalities in situations where individuals differ in future fitness expectations.     

Bet-hedging as an evolutionary game: the trade-off between egg size and number

Bet-hedging theory addresses how individuals should optimize fitness in varying and unpredictable environments by sacrificing mean fitness to decrease variation in fitness. So far, three main bet-hedging strategies have been described: conservative bet-hedging (play it safe), diversified bet-hedging (don’t put all eggs in one basket) and adaptive coin flipping (choose a strategy at random from a fixed distribution). Within this context, we analyse the trade-off between many small eggs (or seeds) and few large, given an unpredictable environment. Our model is an extension of previous models and allows for any combination of the bet-hedging strategies mentioned above. In our individual-based model (accounting for both ecological and evolutionary forces), the optimal bet-hedging strategy is a combination of conservative and diversified bet-hedging and adaptive coin flipping, which means a variation in egg size both within clutches and between years. Hence, we show how phenotypic variation within a population, often assumed to be due to non-adaptive variation, instead can be the result of females having this mixed strategy. Our results provide a new perspective on bet-hedging and stress the importance of extreme events in life history evolution.     

Genome size correlates with reproductive fitness in seed beetles

The ultimate cause of genome size (GS) evolution in eukaryotes remains a major and unresolved puzzle in evolutionary biology. Large-scale comparative studies have failed to find consistent correlations between GS and organismal properties, resulting in the ‘C-value paradox’. Current hypotheses for the evolution of GS are based either on the balance between mutational events and drift or on natural selection acting upon standing genetic variation in GS. It is, however, currently very difficult to evaluate the role of selection because within-species studies that relate variation in life-history traits to variation in GS are very rare. Here, we report phylogenetic comparative analyses of GS evolution in seed beetles at two distinct taxonomic scales, which combines replicated estimation of GS with experimental assays of life-history traits and reproductive fitness. GS showed rapid and bidirectional evolution across species, but did not show correlated evolution with any of several indices of the relative importance of genetic drift. Within a single species, GS varied by 4–5% across populations and showed positive correlated evolution with independent estimates of male and female reproductive fitness. Collectively, the phylogenetic pattern of GS diversification across and within species in conjunction with the pattern of correlated evolution between GS and fitness provide novel support for the tenet that natural selection plays a key role in shaping GS evolution.     

Mating portfolios: bet-hedging,sexual selection and female multiple mating

Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here, we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most ‘model’ species. In this study, we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.     

Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing

Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The ‘disposable soma’ theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five ‘longevity’ genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.     

The evolution of extreme altruism and inequality in insect societies

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual''s life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.     

Mapping of Candidate Genes Involved in Bud Dormancy and Flowering Time in Sweet Cherry (Prunus avium)

The timing of flowering in perennial plants is crucial for their survival in temperate climates and is regulated by the duration of bud dormancy. Bud dormancy release and bud break depend on the perception of cumulative chilling during endodormancy and heat during the bud development. The objectives of this work were to identify candidate genes involved in dormancy and flowering processes in sweet cherry, their mapping in two mapping progenies ‘Regina’ × ‘Garnet’ and ‘Regina’ × ‘Lapins’, and to select those candidate genes which co-localized with quantitative trait loci (QTLs) associated with temperature requirements for bud dormancy release and flowering. Based on available data on flowering processes in various species, a list of 79 candidate genes was established. The peach and sweet cherry orthologs were identified and primers were designed to amplify sweet cherry candidate gene fragments. Based on the amplified sequences of the three parents of the mapping progenies, SNPs segregations in the progenies were identified. Thirty five candidate genes were genetically mapped in at least one of the two progenies and all were in silico mapped. Co-localization between candidate genes and QTLs associated with temperature requirements and flowering date were identified for the first time in sweet cherry. The allelic composition of the candidate genes located in the major QTL for heat requirements and flowering date located on linkage group 4 have a significant effect on these two traits indicating their potential use for breeding programs in sweet cherry to select new varieties adapted to putative future climatic conditions.     

An inclusive fitness analysis of synergistic interactions in structured populations

We study the evolution of a pair of competing behavioural alleles in a structured population when there are non-additive or ‘synergistic’ fitness effects. Under a form of weak selection and with a simple symmetry condition between a pair of competing alleles, Tarnita et al. provide a surprisingly simple condition for one allele to dominate the other. Their condition can be obtained from an analysis of a corresponding simpler model in which fitness effects are additive. Their result uses an average measure of selective advantage where the average is taken over the long-term—that is, over all possible allele frequencies—and this precludes consideration of any frequency dependence the allelic fitness might exhibit. However, in a considerable body of work with non-additive fitness effects—for example, hawk–dove and prisoner''s dilemma games—frequency dependence plays an essential role in the establishment of conditions for a stable allele-frequency equilibrium. Here, we present a frequency-dependent generalization of their result that provides an expression for allelic fitness at any given allele frequency p. We use an inclusive fitness approach and provide two examples for an infinite structured population. We illustrate our results with an analysis of the hawk–dove game.     

Evaluating the role of reproductive constraints in ant social evolution

The reproductive division of labour is a key feature of eusociality in ants, where queen and worker castes show dramatic differences in the development of their reproductive organs. To understand the developmental and genetic basis underlying this division of labour, we performed a molecular analysis of ovary function and germ cell development in queens and workers. We show that the processes of ovarian development in queens have been highly conserved relative to the fruitfly Drosophila melanogaster. We also identify specific steps during oogenesis and embryogenesis in which ovarian and germ cell development have been evolutionarily modified in the workers. These modifications, which we call ‘reproductive constraints’, are often assumed to represent neutral degenerations that are a consequence of social evolutionary forces. Based on our developmental and functional analysis of these constraints, however, we propose and discuss the alternative hypothesis that reproductive constraints represent adaptive proximate mechanisms or traits for maintaining social harmony in ants. We apply a multi-level selection framework to help understand the role of these constraints in ant social evolution. A complete understanding of how cooperation, conflict and developmental systems evolve in social groups requires a ‘socio-evo-devo’ approach that integrates social evolutionary and developmental biology.     

Bet-hedging via dispersal aids the evolution of plastic responses to unreliable cues

Adaptive plasticity is expected to evolve when informative cues predict environmental variation. However, plastic responses can be maladaptive even when those cues are informative, if prediction mistakes are shared across members of a generation. These fitness costs can constrain the evolution of plasticity when initial plastic mutants use of cues of only moderate reliability. Here, we model the barriers to the evolution of plasticity produced by these constraints and show that dispersal across a metapopulation can overcome them. Constraints are also lessened, though not eliminated, when plastic responses are free to evolve gradually and in concert with increased reliability. Each of these factors be viewed as a form of bet-hedging: by lessening correlations in the fates of relatives, dispersal acts as diversifying bet-hedging, while producing submaximal responses to a cue can be understood as a conservative bet-hedging strategy. While poor information may constrain the evolution of plasticity, the opportunity for bet-hedging may predict when that constraint can be overcome.     

Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable

Female multiple mating (or polyandry) is considered to act as a genetic bet-hedging mechanism, by which females can reduce the assessment error in regard to mates genetic quality when only uncertain information is available. In spite of frequent verbal arguments, no theoretical examination has been carried out to determine the effectiveness of bet-hedging by multiple mating. In the present paper, I show that three factors, female population size, remating costs and environmental fluctuation, all affect the effectiveness of bet-hedging. A mathematical model predicts that bet-hedging effectively works only in small populations, and computer simulations were used to confirm this prediction. The results of simulations differed according to the degree of environmental fluctuation. In relatively stable environments, if there is no remating cost, the fixation probability of a multiple mating strategy is slightly higher than that of a single mating strategy, independent of female population size. However, with very slight fitness costs, multiple mating drastically loses its advantage as population size increases, and almost always becomes extinct within large populations. This means that the evolution of polyandry solely by the mechanism of bet-hedging is unlikely in stable environments. However, in unpredictable environments, or when negative frequency-dependent selection on fitness-related loci is introduced, a multiple mating strategy is sometimes successful against a single mating strategy, even if it entails a small fitness cost. Therefore, female multiple mating may possibly evolve only in these limited conditions. In most cases, some deterministic mechanisms such as postcopulatory sperm selection by multiply mated females (or direct material benefits) are more reasonable as the evolutionary causes of polyandry.     

Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation

An evolutionary response to selection requires genetic variation; however, even if it exists, then the genetic details of the variation can constrain adaptation. In the simplest case, unlinked loci and uncorrelated phenotypes respond directly to multivariate selection and permit unrestricted paths to adaptive peaks. By contrast, ‘antagonistic’ pleiotropic loci may constrain adaptation by affecting variation of many traits and limiting the direction of trait correlations to vectors that are not favoured by selection. However, certain pleiotropic configurations may improve the conditions for adaptive evolution. Here, we present evidence that the Arabidopsis thaliana gene FRI (FRIGIDA) exhibits ‘adaptive’ pleiotropy, producing trait correlations along an axis that results in two adaptive strategies. Derived, low expression FRI alleles confer a ‘drought escape’ strategy owing to fast growth, low water use efficiency and early flowering. By contrast, a dehydration avoidance strategy is conferred by the ancestral phenotype of late flowering, slow growth and efficient water use during photosynthesis. The dehydration avoidant phenotype was recovered when genotypes with null FRI alleles were transformed with functional alleles. Our findings indicate that the well-documented effects of FRI on phenology result from differences in physiology, not only a simple developmental switch.     

Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes

The compositions of bacterial genomes can be changed rapidly and dramatically through a variety of processes including horizontal gene transfer. This form of change is key to bacterial evolution, as it leads to ‘evolution in quantum leaps’. Horizontal gene transfer entails the incorporation of genetic elements transferred from another organism—perhaps in an earlier generation—directly into the genome, where they form ‘genomic islands’, i.e. blocks of DNA with signatures of mobile genetic elements. Genomic islands whose functions increase bacterial fitness, either directly or indirectly, have most likely been positively selected and can be termed ‘fitness islands’. Fitness islands can be divided into several subtypes: ‘ecological islands’ in environmental bacteria and ‘saprophytic islands’, ‘symbiosis islands’ or ‘pathogenicity islands’ (PAIs) in microorganisms that interact with living hosts. Here we discuss ways in which PAIs contribute to the pathogenic potency of bacteria, and the idea that genetic entities similar to genomic islands may also be present in the genomes of eukaryotes.     

Mating tactics determine patterns of condition dependence in a dimorphic horned beetle

The persistence of genetic variability in performance traits such as strength is surprising given the directional selection that such traits experience, which should cause the fixation of the best genetic variants. One possible explanation is ‘genic capture’ which is usually considered as a candidate mechanism for the maintenance of high genetic variability in sexual signalling traits. This states that if a trait is ‘condition dependent’, with expression being strongly influenced by the bearer''s overall viability, then genetic variability can be maintained via mutation-selection balance. Using a species of dimorphic beetle with males that gain matings either by fighting or by ‘sneaking’, we tested the prediction of strong condition dependence for strength, walking speed and testes mass. Strength was strongly condition dependent only in those beetles that fight for access to females. Walking speed, with less of an obvious selective advantage, showed no condition dependence, and testes mass was more condition dependent in sneaks, which engage in higher levels of sperm competition. Within a species, therefore, condition dependent expression varies between morphs, and corresponds to the specific selection pressures experienced by that morph. These results support genic capture as a general explanation for the maintenance of genetic variability in traits under directional selection.     

Divergent allele advantage at MHC-DRB through direct and maternal genotypic effects and its consequences for allele pool composition and mating

It is still debated whether main individual fitness differences in natural populations can be attributed to genome-wide effects or to particular loci of outstanding functional importance such as the major histocompatibility complex (MHC). In a long-term monitoring project on Galápagos sea lions (Zalophus wollebaeki), we collected comprehensive fitness and mating data for a total of 506 individuals. Controlling for genome-wide inbreeding, we find strong associations between the MHC locus and nearly all fitness traits. The effect was mainly attributable to MHC sequence divergence and could be decomposed into contributions of own and maternal genotypes. In consequence, the population seems to have evolved a pool of highly divergent alleles conveying near-optimal MHC divergence even by random mating. Our results demonstrate that a single locus can significantly contribute to fitness in the wild and provide conclusive evidence for the ‘divergent allele advantage’ hypothesis, a special form of balancing selection with interesting evolutionary implications.     

Effects of geographical heterogeneity in species interactions on the evolution of venom genes

Geographical heterogeneity in the composition of biotic interactions can create a mosaic of selection regimes that may drive the differentiation of phenotypes that operate at the interface of these interactions. Nonetheless, little is known about effects of these geographical mosaics on the evolution of genes encoding traits associated with species interactions. Predatory marine snails of the family Conidae use venom, a cocktail of conotoxins, to capture prey. We characterized patterns of geographical variation at five conotoxin genes of a vermivorous species, Conus ebraeus, at Hawaii, Guam and American Samoa, and evaluated how these patterns of variation are associated with geographical heterogeneity in prey utilization. All populations show distinct patterns of prey utilization. Three ‘highly polymorphic’ conotoxin genes showed significant geographical differences in allelic frequency, and appear to be affected by different modes of selection among populations. Two genes exhibited low levels of diversity and a general lack of differentiation among populations. Levels of diversity of ‘highly polymorphic’ genes exhibit a positive relationship with dietary breadth. The different patterns of evolution exhibited by conotoxin genes suggest that these genes play different roles in prey capture, and that some genes are more greatly affected by differences in predator–prey interactions than others. Moreover, differences in dietary breadth appear to have a greater influence on the differentiation of venoms than differences in the species of prey.     

Prospecting and dispersal: their eco-evolutionary dynamics and implications for population patterns

Dispersal is not a blind process, and evidence is accumulating that individual dispersal strategies are informed in most, if not all, organisms. The acquisition and use of information are traits that may evolve across space and time as a function of the balance between costs and benefits of informed dispersal. If information is available, individuals can potentially use it in making better decisions, thereby increasing their fitness. However, prospecting for and using information probably entail costs that may constrain the evolution of informed dispersal, potentially with population-level consequences. By using individual-based, spatially explicit simulations, we detected clear coevolutionary dynamics between prospecting and dispersal movement strategies that differed in sign and magnitude depending on their respective costs. More specifically, we found that informed dispersal strategies evolve when the costs of information acquisition during prospecting are low but only if there are mortality costs associated with dispersal movements. That is, selection favours informed dispersal strategies when the acquisition and use processes themselves were not too expensive. When non-informed dispersal strategies evolve, they do so jointly with the evolution of long dispersal distance because this maximizes the sampling area. In some cases, selection produces dispersal rules different from those that would be ‘optimal’ (i.e. the best possible population performance—in our context quantitatively measured as population density and patch occupancy—among all possible individual movement rules) for the population. That is, on the one hand, informed dispersal strategies led to population performance below its highest possible level. On the other hand, un- and poorly informed individuals nearly optimized population performance, both in terms of density and patch occupancy.     

Social evolution in the shadow of asymmetrical relatedness

The persistence of altruism and spite remains an enduring problem of social evolution. It is well known that selection for these actions depends on the structure of the population—that is, on actors'' genetic relationships to recipients and to the ‘neighbourhood’ upon which the effects of their actions redound. Less appreciated, however, is that population structure can cause genetic asymmetries between partners whereby the relatedness (defined relative to the neighbourhood) of an individual i to a partner j will differ from the relatedness of j to i. Here, we introduce a widespread mechanism of kin recognition to a model of dispersal in subdivided populations. In so doing, we uncover three remarkable consequences of asymmetrical relatedness. First, altruism directed at phenotypically similar partners evolves more easily among migrant than native actors. Second, spite directed at dissimilar partners evolves more easily among native than migrant actors. Third, unlike migrants, natives can evolve to pay costs that far outstrip those they spitefully impose on others. We find that the frequency of natives relative to migrants amplifies the asymmetries between them. Taken together, our results reveal differentiated patterns of ‘phenocentrism’ that readily arise from asymmetries of relatedness.