What is genetic quality?

Mate choice is favored by indirect selection if choosy females mate with males of high genetic quality. We believe, however, that testing hypotheses about indirect selection has been constrained by how we conceptualize and therefore empirically measure male genetic quality. Here, we argue that genetic quality is the breeding value of an individual for total fitness. We can therefore learn little about genetic quality from measures of only a few fitness components. We explain breeding value for total fitness, drawing on concepts from life-history theory and quantitative genetics, and suggest how approaches incorporating these insights might result in empirical progress.     

Mitochondrial DNA effects on fitness in Drosophila subobscura

We tested different fitness components on a series of conspecific mtDNA haplotypes, detected by RFLPs in Drosophila subobscura. Additionally, haplotype VIII, endemic to the Canary Islands, was tested upon its own native nuclear DNA background and upon that of the rest of mtDNAs tested herein. We found that both nuclear and mitochondrial DNA can have a significant effect upon their hosts' fitness, and that negative selection is one of the mechanisms that can intervene in this species' mtDNA haplotype pattern. We discuss the importance of this mechanism in relation to genetic drift, in the form of periodic population bottlenecks, and how the latter can enhance the former. We also detected a significant positive effect of haplotype VIII upon fitness that could explain in part the dominance of this endemic haplotype on some of the Canary Islands, and a mitochondrial heterosis involving this haplotype when on a foreign nuclear DNA background.     

The fitness of filamentous fungi

Fitness is a common currency in comparative biology. Without data on fitness, hypotheses about the adaptive significance of phenotypes or basic mechanisms of evolution, for example natural selection, remain speculative. Experiments with fungi can address questions specific to fungi or questions with a broader significance. Fungi can challenge the generality of fundamental evolutionary principles, yet there are no standard measures of fungal fitness. We argue that focusing on a single aspect of a complex life cycle, or a single measure of fitness (e.g. the number of asexual spores) is appropriate. Choosing which aspect of fitness to measure can be facilitated by an understanding of how fitness measures are correlated. Choices can also be based on the ecology of a species, for example whether a fungus is semelparous and reproduces once, or iteroparous and reproduces multiple times.     

Distributions of beneficial fitness effects in RNA

Beneficial mutations are the driving force of evolution by natural selection. Yet, relatively little is known about the distribution of the fitness effects of beneficial mutations in populations. Recent work of Gillespie and Orr suggested some of the first generalizations for the distributions of beneficial fitness effects and, surprisingly, they depend only weakly on biological details. In particular, the theory suggests that beneficial mutations obey an exponential distribution of fitness effects, with the same exponential parameter across different regions of genotype space, provided only that few possible beneficial mutations are available to that genotype. Here we tested this hypothesis with a quasi-empirical model of RNA evolution in which fitness is based on the secondary structures of molecules and their thermodynamic stabilities. The fitnesses of randomly selected genotypes appeared to follow a Gumbel-type distribution and thus conform to a basic assumption of adaptation theory. However, the observed distributions of beneficial fitness effects conflict with specific predictions of the theory. In particular, the distributions of beneficial fitness effects appeared exponential only when the vast majority of small-effect beneficial mutations were ignored. Additionally, the distribution of beneficial fitness effects varied with the fitness of the parent genotype. We believe that correlation of the fitness values among similar genotypes is likely the cause of the departure from the predictions of recent adaptation theory. Although in conflict with the current theory, these results suggest that more complex statistical generalizations about beneficial mutations may be possible.     

Toward a more trait-centered approach to diffuse (co)evolution

How species evolve depends on the communities in which they are embedded. Here, we briefly review the ideas underlying concepts of diffuse coevolution, evolution, and selection. We discuss criteria to identify when evolution will be diffuse. We advocate a more explicitly trait-oriented approach to diffuse (co)evolution, and discuss how considering effects of interacting species on fitness alone tells us little about evolution. We endorse the view that diffuse evolution occurs whenever the response to selection by one interacting species on a given trait is altered by the presence of a second interacting species. Building on the work of others, we clarify and expand the criteria for diffuse evolution and present a simple experimental design that will allow the detection of diffuse selection. We argue that a greater focus on selection on specific traits and the evolutionary response to that selection will improve our conceptual understanding of how communities affect the evolution of species embedded within them.     

The cost of an immune response: vaccination reduces parental effort

A fundamental assumption of theories of the ecology and evolution of inducible defences is that protective responses to attacks by parasites or predators should not only have benefits, but also costs. The vertebrate immune system is by far the best studied example of an inducible defence, yet little is known about the costs of an immune response, especially in natural populations. To test if an immune response per se is costly, we induced an antibody response in female blue tits, Parus caeruleus , by immunising them with human diphtheria–tetanus vaccine, and compared their nestling-feeding rate with that of saline-injected controls. We found that vaccinated females reduced their nestling feeding rate, thus demonstrating a cost of the immune response in the currency of parental effort.     

Strategy maps: Generalised giving-up densities for optimal foraging

Finding a common currency for benefits and hazards is a major challenge in optimal foraging theory, often requiring complex computational methods. We present a new analytic approach that builds on the Marginal Value Theorem and giving-up densities while incorporating the nonlinear effect of predation risk. We map the space of all possible environments into strategy regions, each corresponding to a discrete optimal strategy. This provides a generalised quantitative measure of the trade-off between foraging rewards and hazards. This extends a classic optimal diet choice rule-of-thumb to incorporate the hazard of waiting for better resources to appear. We compare the dynamics of optimal decision-making for three foraging life-history strategies: One in which fitness accrues instantly, and two with delays before fitness benefit is accrued. Foragers with delayed-benefit strategies are more sensitive to predation risk than resource quality, as they stand to lose more fitness from a predation event than instant-accrual foragers.     

INFERRING FITNESS LANDSCAPES

Since 1983, study of natural selection has relied heavily on multiple regression of fitness on the values for a set of traits via ordinary least squares (OLSs), as proposed by Lande and Arnold, to obtain an estimate of the quadratic relationship between fitness and the traits, the fitness surface. However, well‐known statistical problems with this approach can affect inferences about selection. One key concern is that measures of lifetime fitness do not conform to a normal or any other standard sampling distribution, as needed to justify the usual statistical tests. Another is that OLS may yield an estimate of the sign of the fitness function's curvature that is opposite to the truth. We here show that the recently developed aster modeling approach, which explicitly models the components of fitness as the basis for inferences about lifetime fitness, eliminates these problems. We illustrate selection analysis via aster using simulated datasets involving five fitness components expressed in each of four years. We demonstrate that aster analysis yields accurate estimates of the fitness function in cases in which OLS misleads, as well as accurate confidence regions for directional selection gradients. Further, to evaluate selection when many traits are under consideration, we recommend model selection by information criteria and frequentist model averaging.     

Sesquiterpene lactone stereochemistry influences herbivore resistance and plant fitness in the field

Background and Aims

Stereochemical variation is widely known to influence the bioactivity of compounds in the context of pharmacology and pesticide science, but our understanding of its importance in mediating plant–herbivore interactions is limited, particularly in field settings. Similarly, sesquiterpene lactones are a broadly distributed class of putative defensive compounds, but little is known about their activities in the field.

Methods

Natural variation in sesquiterpene lactones of the common cocklebur, Xanthium strumarium (Asteraceae), was used in conjunction with a series of common garden experiments to examine relationships between stereochemical variation, herbivore damage and plant fitness.

Key Results

The stereochemistry of sesquiterpene lactone ring junctions helped to explain variation in plant herbivore resistance. Plants producing cis-fused sesquiterpene lactones experienced significantly higher damage than plants producing trans-fused sesquiterpene lactones. Experiments manipulating herbivore damage above and below ambient levels found that herbivore damage was negatively correlated with plant fitness. This pattern translated into significant fitness differences between chemotypes under ambient levels of herbivore attack, but not when attack was experimentally reduced via pesticide.

Conclusions

To our knowledge, this work represents only the second study to examine sesquiterpene lactones as defensive compounds in the field, the first to document herbivore-mediated natural selection on sesquiterpene lactone variation and the first to investigate the ecological significance of the stereochemistry of the lactone ring junction. The results indicate that subtle differences in stereochemistry may be a major determinant of the protective role of secondary metabolites and thus of plant fitness. As stereochemical variation is widespread in many groups of secondary metabolites, these findings suggest the possibility of dynamic evolutionary histories within the Asteraceae and other plant families showing extensive stereochemical variation.     

Kinship reinforces cooperative predator inspection in a cichlid fish

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.     

The genetics of speciation: Insights from Fisher's geometric model

Research in speciation genetics has uncovered many robust patterns in intrinsic reproductive isolation, and fitness landscape models have been useful in interpreting these patterns. Here, we examine fitness landscapes based on Fisher's geometric model. Such landscapes are analogous to models of optimizing selection acting on quantitative traits, and have been widely used to study adaptation and the distribution of mutational effects. We show that, with a few modifications, Fisher's model can generate all of the major findings of introgression studies (including “speciation genes” with strong deleterious effects, complex epistasis and asymmetry), and the major patterns in overall hybrid fitnesses (including Haldane's Rule, the speciation clock, heterosis, hybrid breakdown, and male–female asymmetry in the F1). We compare our approach to alternative modeling frameworks that assign fitnesses to genotypes by identifying combinations of incompatible alleles. In some cases, the predictions are importantly different. For example, Fisher's model can explain conflicting empirical results about the rate at which incompatibilities accumulate with genetic divergence. In other cases, the predictions are identical. For example, the quality of reproductive isolation is little affected by the manner in which populations diverge.     

Function-valued adaptive dynamics and optimal control theory

In this article we further develop the theory of adaptive dynamics of function-valued traits. Previous work has concentrated on models for which invasion fitness can be written as an integral in which the integrand for each argument value is a function of the strategy value at that argument value only. For this type of models of direct effect, singular strategies can be found using the calculus of variations, with singular strategies needing to satisfy Euler’s equation with environmental feedback. In a broader, more mechanistically oriented class of models, the function-valued strategy affects a process described by differential equations, and fitness can be expressed as an integral in which the integrand for each argument value depends both on the strategy and on process variables at that argument value. In general, the calculus of variations cannot help analyzing this much broader class of models. Here we explain how to find singular strategies in this class of process-mediated models using optimal control theory. In particular, we show that singular strategies need to satisfy Pontryagin’s maximum principle with environmental feedback. We demonstrate the utility of this approach by studying the evolution of strategies determining seasonal flowering schedules.     

There is no fitness but fitness,and the lineage is its bearer

Inclusive fitness has been the cornerstone of social evolution theory for more than a half-century and has matured as a mathematical theory in the past 20 years. Yet surprisingly for a theory so central to an entire field, some of its connections to evolutionary theory more broadly remain contentious or underappreciated. In this paper, we aim to emphasize the connection between inclusive fitness and modern evolutionary theory through the following fact: inclusive fitness is simply classical Darwinian fitness, averaged over social, environmental and demographic states that members of a gene lineage experience. Therefore, inclusive fitness is neither a generalization of classical fitness, nor does it belong exclusively to the individual. Rather, the lineage perspective emphasizes that evolutionary success is determined by the effect of selection on all biological and environmental contexts that a lineage may experience. We argue that this understanding of inclusive fitness based on gene lineages provides the most illuminating and accurate picture and avoids pitfalls in interpretation and empirical applications of inclusive fitness theory.     

Emergent properties of conspecific attraction in fragmented landscapes

Attraction to conspecifics may have wide-ranging implications for habitat selection and metapopulation theory, yet little is known about the process of attraction and its effects relative to other habitat selection strategies. Using individual-based simulations, I investigated the emergent properties of conspecific attraction during habitat selection on survival, fecundity, short-term fitness (survival x fecundity), and distributions in fragmented landscapes. I simulated conspecific attraction during searching and settlement decisions and compared attraction with random, habitat-based (searching for the presence of habitat), and habitat quality sampling strategies (searching for and settling in high-quality habitat). Conspecific attraction during searching or settlement decisions had different consequences for animals: attraction while searching increased survival by decreasing time spent in nonsuitable habitat, whereas attraction during settlement increased fecundity by aggregating animals in high-quality habitats. Habitat-based sampling did not improve fitness over attraction, but directly sampling habitat quality resulted in the highest short-term fitness among strategies. These results suggest that attraction can improve fitness when animals cannot directly assess habitat quality. Interestingly, conspecific attraction influenced distributions by generating patch size effects and weak edge effects, highlighting that attraction is one potential, yet previously unappreciated, mechanism to explain the widespread patterns of animal sensitivity to habitat fragmentation.     

SEXUAL IMPRINTING: WHAT STRATEGIES SHOULD WE EXPECT TO SEE IN NATURE?

Sexual imprinting occurs when juveniles learn mate preferences by observing the phenotypes of other members of their populations, and it is ubiquitous in nature. Imprinting strategies, that is which individuals and phenotypes are observed and how strong preferences become, vary among species. Imprinting can affect trait evolution and the probability of speciation, and different imprinting strategies are expected to have different effects. However, little is known about how and why different imprinting strategies evolve, or which strategies we should expect to see in nature. We used a mathematical model to study how the evolution of sexual imprinting depends on (1) imprinting costs and (2) the sex‐specific fitness effects of the phenotype on which individuals imprint. We found that even small fixed costs prevent the evolution of sexual imprinting, but small relative costs do not. When imprinting does evolve, we identified the conditions under which females should evolve to imprint on their fathers, their mothers, or on other members of their populations. Our results provide testable hypotheses for empirical work and help to explain the conditions under which sexual imprinting might evolve to promote speciation.     

Population genetics and sociobiology: conflicting views of evolution

This article explores the tension between the population genetics and sociobiological approaches to the study of evolution. Whereas population geneticists, like Stanford's Marc Feldman, insist that the genetic complexities of organisms cannot be overlooked, sociobiologists (many of whom now prefer to call themselves "behavioral ecologists") rely on optimization models that are based on the simplest possible genetics.These optimization approaches have their roots in the classical result known as the fundamental theorem of natural selection, formulated by R. A. Fisher in 1930. From the start there was great uncertainty over the proper interpretation of Fisher's theorem, which became confused with Sewall Wright's immensely influential adaptive landscape concept. In the 1960s, a new generation of mathematical biologists proved that Fisher's theorem did not hold when fitness depended on more than one locus. Similar reasoning was used to attack W. D. Hamilton's inclusive fitness theory. A new theory, known as the theory of long-term evolution, attempts to reconcile the rigorous population genetics approach with the long-standing sociobiological view that natural selection acts to increase the fitness of organisms.     

Drivers and consequences of partial migration in an alpine bird species

1. Partial migration, where a portion of the population migrates between winter and summer (breeding) areas and the rest remain year‐round resident, is a common phenomenon across several taxonomic groups. Several hypotheses have been put forward to explain why some individuals migrate while others stay resident, as well as the fitness consequences of the different strategies. Yet, the drivers and consequences of the decision to migrate or not are poorly understood.
2. We used data from radio‐tagged female (n = 73) willow ptarmigan Lagopus lagopus in an alpine study area in Central Norway to test if (i) the decision to migrate was dependent on individual state variables (age and body weight), (ii) individuals repeated migratory decisions between seasons, and (iii) the choice of migratory strategy was related to reproductive success.
3. Partially supporting our prediction that migratory strategy depends on individual state, we found that juvenile birds with small body sizes were more likely to migrate, whereas large juveniles remained resident. For adult females, we found no relationship between the decision to migrate or stay resident and body weight. We found evidence for high individual repeatability of migratory decision between seasons. Migratory strategy did not explain variation in clutch size or nest fate among individuals, suggesting no direct influence of the chosen strategy on reproductive success.
4. Our results indicate that partial migration in willow ptarmigan is related to juvenile body weight, and that migratory behavior becomes a part of the individual life history as a fixed strategy. Nesting success was not affected by migratory strategy in our study population, but future studies should assess other traits to further test potential fitness consequences.

     

Individual adaptations in stochastic environments

Summary Many natural populations undergo radical and unpredictable fluctuations, associated with stochastic environmental conditions. Under such circumstances, fitness of a genotype (or strategy) is defined as the geometric mean of the intergenerational genotypic population growth ratel(t). Unfortunately, this population-level criterion has proved difficult to apply at the level of individual organisms.After developing a formula for the variance ofl as the sum of developmental and environmental variance, we discuss several models of individual adaptations, involving clutch size, progeny size and number, and foraging behaviour under risk of predation, based on the geometric-mean fitness concept. We then show how the method of dynamic programming can be extended to deal with facultative behaviour in stochastic environments. Finally we discuss the concept of an evolutionarily stable strategy in a stochastic environment.Our analysis suggests several novel interpretations of field and laboratory observations. Under the geometric mean criterion behaviour may be determined primarily by the worst likely environment; behaviour may appear suboptimal if observed only under normal or average conditions. For example,except under extreme environmental conditions, avian clutches larger than those that are observed might result in increased fecundity, with little if any cost of reproduction in terms of parental survival; however, in unusually bad years such large clutches might be disastrous, in terms of parental survival. This consideration may help explain some recently reported experimental clutch-size manipulation results. Similarly, our analysis indicates that the known phenomenon of seasonal reduction in seed size may constitute a double bet-hedging strategy, determined by parental mortality risk and future seed survival probability. We also discuss circumstances in which phenotypic polymorphism is an adaptation to environmental uncertainty. Thus almost any individual life history or behavioural adaptation may be affected by environmental stochasticity.     

Plant traits and ecosystem effects of clonality: a new research agenda

Background

Clonal plants spread laterally by spacers between their ramets (shoot–root units); these spacers can transport and store resources. While much is known about how clonality promotes plant fitness, we know little about how different clonal plants influence ecosystem functions related to carbon, nutrient and water cycling.

Approach

The response–effect trait framework is used to formulate hypotheses about the impact of clonality on ecosystems. Central to this framework is the degree of correspondence between interspecific variation in clonal ‘response traits’ that promote plant fitness and interspecific variation in ‘effect traits’, which define a plant''s potential effect on ecosystem functions. The main example presented to illustrate this concept concerns clonal traits of vascular plant species that determine their lateral extension patterns. In combination with the different degrees of decomposability of litter derived from their spacers, leaves, roots and stems, these clonal traits should determine associated spatial and temporal patterns in soil organic matter accumulation, nutrient availability and water retention.

Conclusions

This review gives some concrete pointers as to how to implement this new research agenda through a combination of (1) standardized screening of predominant species in ecosystems for clonal response traits and for effect traits related to carbon, nutrient and water cycling; (2) analysing the overlap between variation in these response traits and effect traits across species; (3) linking spatial and temporal patterns of clonal species in the field to those for soil properties related to carbon, nutrient and water stocks and dynamics; and (4) studying the effects of biotic interactions and feedbacks between resource heterogeneity and clonality. Linking these to environmental changes may help us to better understand and predict the role of clonal plants in modulating impacts of climate change and human activities on ecosystem functions.     

Have Genetic Trade-Offs in Host Use been Overlooked in Arthropods?

A popular hypothesis to explain the high degree of host specialisation observed among mites and insects is the existence of host-associated fitness trade-offs. According to this theory, adaptation to a host results in a relatively poorer performance on alternative hosts due to the antagonistic pleiotropic action of one or more genes. Evidence in favour of the genetic trade-off hypothesis is however scarce. Recent ecological work has shown that the optimisation of adult performance drives the evolution of host choice in at least some phytophagous insects. Yet, most ecological and evolutionary studies on host choice assume that females maximise their fitness by optimising offspring performance. In this paper, we investigate whether a general lack of attention for the role of adult performance in host choice may have diminished the chance of detecting genetic trade-offs. We reviewed the literature on genetic trade-offs and showed that most studies neglected host specific variation in adult performance. Moreover, studies that considered both adult and offspring performance had a higher chance of detecting genetic fitness trade-offs. Our results also suggested that studies on asexual reproducing species tend to detect trade-offs more often than studies on obligate sexual reproducing species. We argue that future studies on genetic trade-offs should take all fitness parameters into account in order to be conclusive. This approach may reveal (i) that genetic trade-offs are more common than hitherto reported and/or (ii) that genetic trade-offs are more common, or more easily detected among asexual reproducing species like mites and aphids. Co-ordinating editor: Dr. F. Stuefer