Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene

Accounting for the abundance of genetic variation in the face of natural selection remains a central problem of evolutionary biology. Genetic polymorphisms are constantly arising through mutation, and although most are promptly eliminated, polymorphisms in functionally important traits are common. One mechanism that can maintain polymorphisms is negative frequency-dependent selection on alternative alleles, whereby the fitness of each decreases as its frequency increases. Examples of frequency-dependent selection are rare, especially when attempting to describe the genetic basis of the phenotype under selection. Here we show frequency-dependent selection in a well-known natural genetic polymorphism affecting fruitfly foraging behaviour. When raised in low nutrient conditions, both of the naturally occurring alleles of the foraging gene (for(s) and for(R)) have their highest fitness when rare-the hallmark of negative frequency-dependent selection. This effect disappears at higher resources levels, demonstrating the role of larval competition. We are able to confirm the involvement of the foraging gene by showing that a sitter-like mutant allele on a rover background has similar frequency-dependent fitness as the natural sitter allele. Our study represents a clear demonstration of frequency-dependent selection, and we are able to attribute this effect to a single, naturally polymorphic gene known to affect behaviour.     

Cryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme

Cryptic variation is caused by the robustness of phenotypes to mutations. Cryptic variation has no effect on phenotypes in a given genetic or environmental background, but it can have effects after mutations or environmental change. Because evolutionary adaptation by natural selection requires phenotypic variation, phenotypically revealed cryptic genetic variation may facilitate evolutionary adaptation. This is possible if the cryptic variation happens to be pre-adapted, or "exapted", to a new environment, and is thus advantageous once revealed. However, this facilitating role for cryptic variation has not been proven, partly because most pertinent work focuses on complex phenotypes of whole organisms whose genetic basis is incompletely understood. Here we show that populations of RNA enzymes with accumulated cryptic variation adapt more rapidly to a new substrate than a population without cryptic variation. A detailed analysis of our evolving RNA populations in genotype space shows that cryptic variation allows a population to explore new genotypes that become adaptive only in a new environment. Our observations show that cryptic variation contains new genotypes pre-adapted to a changed environment. Our results highlight the positive role that robustness and epistasis can have in adaptive evolution.     

Density cycles and an offspring quantity and quality game driven by natural selection

A long-standing hypothesis posits that natural selection can favour two female strategies when density cycles. At low density, females producing many smaller progeny are favoured when the intrinsic rate of increase, r, governs population growth. At peak density, females producing fewer, high-quality, progeny are favoured when the carrying capacity, K, is exceeded and the population crashes. Here we report on the first example of a genetic r versus K selection game that promotes stable population cycles in lizards. Decade-long fitness studies and game theory demonstrated that two throat-colour morphs were refined by selection in which the strength of natural selection varied with density. Orange-throated females, r strategists, produced many eggs and were favoured at low density. Conversely, yellow-throated females, K strategists, produced large eggs and were favoured at high density. Progeny size should also be under negative frequency-dependent selection in that large progeny will have a survival advantage when rare, but the advantage disappears when they become common. We confirmed this prediction by seeding field plots with rare and common giant hatchlings. Thus, intrinsic causes of frequency- and density-dependent selection promotes an evolutionary game with two-generation oscillations.     

Genetic correlations between morphology and antipredator behaviour in natural populations of the garter snake Thamnophis ordinoides

The genetic coupling of morphology and behaviour means that the evolution of the two types of traits will not be independent: changes in behaviour will result in changes in morphology and vice versa. This might explain nonadaptive differences in morphology through indirect selection on correlated characters of other categories. Genetic correlations between morphology and behaviour are also the basis for some models of sympatric speciation and of the stability of polymorphisms. Morphology and behaviour are often correlated in nature and a genetic basis for such couplings has been demonstrated. I present here evidence that colour pattern and antipredator behaviour are genetically coupled in natural populations of the garter snake Thamnophis ordinoides. Similar phenotypic correlations between pattern and behaviour exist among species of North American snakes, indicating that selection for particular combinations of traits may help to maintain genetic covariances and colour polymorphism in Thamnophis ordinoides.     

Contribution of Distal-less to quantitative variation in butterfly eyespots.

The colour patterns decorating butterfly wings provide ideal material to study the reciprocal interactions between evolution and development. They are visually compelling products of selection, often with a clear adaptive value, and are amenable to a detailed developmental characterization. Research on wing-pattern evolution and development has focused on the eyespots of the tropical butterfly Bicyclus anynana. There is quantitative variation for several features of eyespot morphology but the actual genes contributing to such variation are unknown. On the other hand, studies of gene expression patterns in wing primordia have implicated different developmental pathways in eyespot formation. To link these two sets of information we need to identify which genes within the implicated pathways contribute to the quantitative variation accessible to natural selection. Here we begin to bridge this gap by demonstrating linkage between DNA polymorphisms in the candidate gene Distal-less (Dll) and eyespot size in B. anynana.     

Sexually antagonistic genetic variation for fitness in red deer

Evolutionary theory predicts the depletion of genetic variation in natural populations as a result of the effects of selection, but genetic variation is nevertheless abundant for many traits that are under directional or stabilizing selection. Evolutionary geneticists commonly try to explain this paradox with mechanisms that lead to a balance between mutation and selection. However, theoretical predictions of equilibrium genetic variance under mutation-selection balance are usually lower than the observed values, and the reason for this is unknown. The potential role of sexually antagonistic selection in maintaining genetic variation has received little attention in this debate, surprisingly given its potential ubiquity in dioecious organisms. At fitness-related loci, a given genotype may be selected in opposite directions in the two sexes. Such sexually antagonistic selection will reduce the otherwise-expected positive genetic correlation between male and female fitness. Both theory and experimental data suggest that males and females of the same species may have divergent genetic optima, but supporting data from wild populations are still scarce. Here we present evidence for sexually antagonistic fitness variation in a natural population, using data from a long-term study of red deer (Cervus elaphus). We show that male red deer with relatively high fitness fathered, on average, daughters with relatively low fitness. This was due to a negative genetic correlation between estimates of fitness in males and females. In particular, we show that selection favours males that carry low breeding values for female fitness. Our results demonstrate that sexually antagonistic selection can lead to a trade-off between the optimal genotypes for males and females; this mechanism will have profound effects on the operation of selection and the maintenance of genetic variation in natural populations.     

Accelerated speciation in colour-polymorphic birds

Colour polymorphism exemplifies extreme morphological diversity within populations. It is taxonomically widespread but generally rare. Theory suggests that where colour polymorphism does occur, processes generating and maintaining it can promote speciation but the generality of this claim is unclear. Here we confirm, using species-level molecular phylogenies for five families of non-passerine birds, that colour polymorphism is associated with accelerated speciation rates in the three groups in which polymorphism is most prevalent. In all five groups, colour polymorphism is lost at a significantly greater rate than it is gained. Thus, the general rarity and phylogenetic dispersion of colour polymorphism is accounted for by a combination of higher speciation rate and higher transition rate from polymorphism to monomorphism, consistent with theoretical models where speciation is driven by fixation of one or more morphs. This is corroborated by evidence from a species-level molecular phylogeny of passerines, incorporating 4,128 (66.5%) extant species, that polymorphic species tend to be younger than monomorphic species. Our results provide empirical support for the general proposition, dating from classical evolutionary theory, that colour polymorphism can increase speciation rates.     

The Drosophila melanogaster Genetic Reference Panel

A major challenge of biology is understanding the relationship between molecular genetic variation and variation in quantitative traits, including fitness. This relationship determines our ability to predict phenotypes from genotypes and to understand how evolutionary forces shape variation within and between species. Previous efforts to dissect the genotype-phenotype map were based on incomplete genotypic information. Here, we describe the Drosophila melanogaster Genetic Reference Panel (DGRP), a community resource for analysis of population genomics and quantitative traits. The DGRP consists of fully sequenced inbred lines derived from a natural population. Population genomic analyses reveal reduced polymorphism in centromeric autosomal regions and the X chromosome, evidence for positive and negative selection, and rapid evolution of the X chromosome. Many variants in novel genes, most at low frequency, are associated with quantitative traits and explain a large fraction of the phenotypic variance. The DGRP facilitates genotype-phenotype mapping using the power of Drosophila genetics.     

Mating advantage of rare males in models of sexual selection

Models of sexual selection in polygynous species of animals have been derived on the assumption that some females have preferences to mate with males with particular genotypes. The mating advantage gained by the males is always frequency-dependent because the preferred males take part in the same number of preferential matings when they are rare as when they are common; individually therefore, they mate more often when they are rare. Frequency-dependent sexual selection has been demonstrated in many experiments with Drosophila: rare males take part in a higher proportion of matings than their frequency as available mates. Ehrman and Spiess explained this phenomenon by frequency-dependence either in female preference or in male courtship. This explanation, which is difficult to interpret in behavioural terms, may not be necessary, however, because constant female preferences would entail frequency-dependent selection among the males. I show here that a simple model of constant preferences for particular phenotypes or genotypes is sufficient to explain a large body of data on frequency-dependent sexual selection in Drosophila.     

Host-parasite 'Red Queen' dynamics archived in pond sediment

Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host-parasite coevolution, in particular 'Red Queen' dynamics--in which antagonistic biotic interactions such as host-parasite interactions can lead to reciprocal evolutionary dynamics--is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host-parasite system, corroborated these experimental results. In line with the idea of continuing host-parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.     

Developmental constraints versus flexibility in morphological evolution

Evolutionary developmental biology has encouraged a change of research emphasis from the sorting of phenotypic variation by natural selection to the production of that variation through development. Some morphologies are more readily generated than others, and developmental mechanisms can limit or channel evolutionary change. Such biases determine how readily populations are able to respond to selection, and have been postulated to explain stasis in morphological evolution and unexplored morphologies. There has been much discussion about evolutionary constraints but empirical data testing them directly are sparse. The spectacular diversity in butterfly wing patterns is suggestive of how little constrained morphological evolution can be. However, for wing patterns involving serial repeats of the same element, developmental properties suggest that some directions of evolutionary change might be restricted. Here we show that despite the developmental coupling between different eyespots in the butterfly Bicyclus anynana, there is great potential for independent changes. This flexibility is consistent with the diversity of wing patterns across species and argues for a dominant role of natural selection, rather than internal constraints, in shaping existing variation.     

A yeast prion provides a mechanism for genetic variation and phenotypic diversity

A major enigma in evolutionary biology is that new forms or functions often require the concerted effects of several independent genetic changes. It is unclear how such changes might accumulate when they are likely to be deleterious individually and be lost by selective pressure. The Saccharomyces cerevisiae prion [PSI+] is an epigenetic modifier of the fidelity of translation termination, but its impact on yeast biology has been unclear. Here we show that [PSI+] provides the means to uncover hidden genetic variation and produce new heritable phenotypes. Moreover, in each of the seven genetic backgrounds tested, the constellation of phenotypes produced was unique. We propose that the epigenetic and metastable nature of [PSI+] inheritance allows yeast cells to exploit pre-existing genetic variation to thrive in fluctuating environments. Further, the capacity of [PSI+] to convert previously neutral genetic variation to a non-neutral state may facilitate the evolution of new traits.     

昆虫行为进化中的熵初探

昆虫的行为进化是昆虫学和进化论研究的重要内容。昆虫行为进化与熵有着密切的关系,昆虫行为进化是遗传物质变异基础上,长期自然选择作用下负熵的不断增加过程。自然选择是对昆虫各种行为的综合的、复杂的选择。     

Physical performance and Darwinian fitness in lizards

Strong evidence for a genetic basis of variation in physical performance has accumulated. Considering one of the basic tenets of evolutionary physiology--that physical performance and darwinian fitness are tightly linked--one may expect phenotypes with exceptional physiological capacities to be promoted by natural selection. Why then does physical performance remain considerably variable in human and other animal populations? Our analysis of locomotor performance in the common lizard (Lacerta vivipara) demonstrates that initial endurance (running time to exhaustion measured at birth) is indeed highly heritable, but natural selection in favour of this trait can be unexpectedly weak. A manipulation of dietary conditions unravels a proximate mechanism explaining this pattern. Fully fed individuals experience a marked reversal of performance within only one month after birth: juveniles with low endurance catch up, whereas individuals with high endurance lose their advantage. In contrast, dietary restriction allows highly endurant neonates to retain their locomotor superiority as they age. Thus, the expression of a genetic predisposition to high physical performance strongly depends on the environment experienced early in life.     

Stage-structured cycles promote genetic diversity in a predator-prey system of Daphnia and algae

Competition theory predicts that population fluctuations can promote genetic diversity when combined with density-dependent selection. However, this stabilizing mechanism has rarely been tested, and was recently rejected as an explanation for maintaining diversity in natural populations of the freshwater herbivore Daphnia pulex. The primary limitation of competition theory is its failure to account for the alternative types of population cycles that are caused by size- or stage-dependent population vital rates--even though such structure both explains the fluctuating dynamics of many species and may alter the outcome of competition. Here we provide the first experimental test of whether alternative types of cycles affect natural selection in predator-prey systems. Using competing Daphnia genotypes, we show that internally generated, stage-structured cycles substantially reduce the magnitude of selection (thereby contributing to the maintenance of genetic diversity), whereas externally forced cycles show rapid competitive exclusion. The change in selection is ecologically significant, spanning the observed range in natural populations. We argue that structured cycles reduce selection through a combination of stalled juvenile development and stage-specific mortality. This potentially general fitness-equalizing mechanism may reduce the need for strong stabilizing mechanisms to explain the maintenance of genetic diversity in natural systems.     

Climate-driven population divergence in sex-determining systems

Sex determination is a fundamental biological process, yet its mechanisms are remarkably diverse. In vertebrates, sex can be determined by inherited genetic factors or by the temperature experienced during embryonic development. However, the evolutionary causes of this diversity remain unknown. Here we show that live-bearing lizards at different climatic extremes of the species' distribution differ in their sex-determining mechanisms, with temperature-dependent sex determination in lowlands and genotypic sex determination in highlands. A theoretical model parameterized with field data accurately predicts this divergence in sex-determining systems and the consequence thereof for variation in cohort sex ratios among years. Furthermore, we show that divergent natural selection on sex determination across altitudes is caused by climatic effects on lizard life history and variation in the magnitude of between-year temperature fluctuations. Our results establish an adaptive explanation for intra-specific divergence in sex-determining systems driven by phenotypic plasticity and ecological selection, thereby providing a unifying framework for integrating the developmental, ecological and evolutionary basis for variation in vertebrate sex determination.     

Evolution driven by differential dispersal within a wild bird population

Evolutionary theory predicts that local population divergence will depend on the balance between the diversifying effect of selection and the homogenizing effect of gene flow. However, spatial variation in the expression of genetic variation will also generate differential evolutionary responses. Furthermore, if dispersal is non-random it may actually reinforce, rather than counteract, evolutionary differentiation. Here we document the evolution of differences in body mass within a population of great tits, Parus major, inhabiting a single continuous woodland, over a 36-year period. We show that genetic variance for nestling body mass is spatially variable, that this generates different potential responses to selection, and that this diversifying effect is reinforced by non-random dispersal. Matching the patterns of variation, selection and evolution with population ecological data, we argue that the small-scale differentiation is driven by density-related differences in habitat quality affecting settlement decisions. Our data show that when gene flow is not homogeneous, evolutionary differentiation can be rapid and can occur over surprisingly small spatial scales. Our findings have important implications for questions of the scale of adaptation and speciation, and challenge the usual treatment of dispersal as a force opposing evolutionary differentiation.     

Genetic basis of fitness differences in natural populations

Genomics profoundly influences current biology. One of many exciting consequences of this revolution is the potential for identifying and studying the genetic basis of those traits affecting fitness that are key to natural selection. Recent studies using a multitude of genomic approaches have established such genotype-phenotype relationships in natural populations, giving new insight into the genetic architecture of quantitative variation. In parallel, an emerging understanding of the quantitative genetics of fitness variation in the wild means that we are poised to see a synthesis of ecological and molecular approaches in evolutionary biology.     

Gene flow maintains a large genetic difference in clutch size at a small spatial scale

Understanding the capacity of natural populations to adapt to their local environment is a central topic in evolutionary biology. Phenotypic differences between populations may have a genetic basis, but showing that they reflect different adaptive optima requires the quantification of both gene flow and selection. Good empirical data are rare. Using data on a spatially structured island population of great tits (Parus major), we show here that a persistent difference in mean clutch size between two subpopulations only a few kilometres apart has a major genetic component. We also show that immigrants from outside the island carry genes for large clutches. But gene flow into one subpopulation is low, as a result of a low immigration rate together with strong selection against immigrant genes. This has allowed for adaptation to the island environment and the maintenance of small clutches. In the other area, however, higher gene flow prevents local adaptation and maintains larger clutches. We show that the observed small-scale genetic difference in clutch size is not due to divergent selection on the island, but to different levels of gene flow from outside the island. Our findings illustrate the large effect of immigration on the evolution of local adaptations and on genetic population structure.     

Adaptive Immune Evolutionary Algorithms Based on Immune Network Regulatory Mechanism

Based on immune network regulatory mechanism, a new adaptive immune evolutionary algorithm （AIEA） is proposed to improve the performance of genetic algorithms （GA） in this paper. AIEA adopts novel selection operation according to the stimulation level of each antibody. A memory base for good antibodies is devised simultaneously to raise the convergent rapidity of the algorithm and adaptive adjusting strategy of antibody population is used for preventing the loss of the population adversity. The experiments show AIEA has better convergence performance than standard genetic algorithm and is capable of maintaining the adversity of the population and solving function optimization problems in an efficient and reliable way.