Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes

Morphological diversification does not proceed evenly across the organism. Some body parts tend to evolve at higher rates than others, and these rate biases are often attributed to sexual and natural selection or to genetic constraints. We hypothesized that variation in the rates of morphological evolution among body parts could also be related to the performance consequences of the functional systems that make up the body. Specifically, we tested the widely held expectation that the rate of evolution for a trait is negatively correlated with the strength of biomechanical trade-offs to which it is exposed. We quantified the magnitude of trade-offs acting on the morphological components of three feeding-related functional systems in four radiations of teleost fishes. After accounting for differences in the rates of morphological evolution between radiations, we found that traits that contribute more to performance trade-offs tend to evolve more rapidly, contrary to the prediction. While ecological and genetic factors are known to have strong effects on rates of phenotypic evolution, this study highlights the role of the biomechanical architecture of functional systems in biasing the rates and direction of trait evolution.     

Hormone-mediated suites as adaptations and evolutionary constraints

Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimental changes in correlated traits. Theory and empirical methods for studying correlated trait evolution have been developed by the field of evolutionary quantitative genetics, and here we suggest that their application to the study of hormone-mediated suites may prove fruitful. We present hypotheses for how selection shapes the evolution of hormone-mediated suites and argue that correlational selection, which arises when traits interact in their effects on fitness, may act to alter or conserve the composition of hormone-mediated suites. Next, we advocate using quantitative genetic methods to assess natural covariation among hormone-mediated traits and to measure the strength of natural selection acting on them. Finally, we present illustrative examples from our own work on the evolution of testosterone-mediated suites in male and female dark-eyed juncos. We conclude that future work on hormone-mediated suites, if motivated by quantitative genetic theory, may provide important insights into their dual roles as adaptations and evolutionary constraints.     

Evolution of quantitative traits in the wild: mind the ecology

Recent advances in the quantitative genetics of traits in wild animal populations have created new interest in whether natural selection, and genetic response to it, can be detected within long-term ecological studies. However, such studies have re-emphasized the fact that ecological heterogeneity can confound our ability to infer selection on genetic variation and detect a population''s response to selection by conventional quantitative genetics approaches. Here, I highlight three manifestations of this issue: counter gradient variation, environmentally induced covariance between traits and the correlated effects of a fluctuating environment. These effects are symptomatic of the oversimplifications and strong assumptions of the breeder''s equation when it is applied to natural populations. In addition, methods to assay genetic change in quantitative traits have overestimated the precision with which change can be measured. In the future, a more conservative approach to inferring quantitative genetic response to selection, or genomic approaches allowing the estimation of selection intensity and responses to selection at known quantitative trait loci, will provide a more precise view of evolution in ecological time.     

Natural genetic variation in Arabidopsis: tools, traits and prospects for evolutionary ecology

BACKGROUND: The model plant Arabidopsis thaliana (Arabidopsis) shows a wide range of genetic and trait variation among wild accessions. Because of its unparalleled biological and genomic resources, the potential of Arabidopsis for molecular genetic analysis of this natural variation has increased dramatically in recent years. SCOPE: Advanced genomics has accelerated molecular phylogenetic analysis and gene identification by quantitative trait loci (QTL) mapping and/or association mapping in Arabidopsis. In particular, QTL mapping utilizing natural accessions is now becoming a major strategy of gene isolation, offering an alternative to artificial mutant lines. Furthermore, the genomic information is used by researchers to uncover the signature of natural selection acting on the genes that contribute to phenotypic variation. The evolutionary significance of such genes has been evaluated in traits such as disease resistance and flowering time. However, although molecular hallmarks of selection have been found for the genes in question, a corresponding ecological scenario of adaptive evolution has been difficult to prove. Ecological strategies, including reciprocal transplant experiments and competition experiments, and utilizing near-isogenic lines of alleles of interest will be a powerful tool to measure the relative fitness of phenotypic and/or allelic variants. CONCLUSIONS: As the plant model organism, Arabidopsis provides a wealth of molecular background information for evolutionary genetics. Because genetic diversity between and within Arabidopsis populations is much higher than anticipated, combining this background information with ecological approaches might well establish Arabidopsis as a model organism for plant evolutionary ecology.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

PLEIOTROPY CAUSES LONG-TERM GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION IN BRASSICA RAPA

Fundamental, long-term genetic trade-offs constrain life-history evolution in wild crucifer populations. I studied patterns of genetic constraint in Brassica rapa by estimating genetic correlations among life-history components by quantitative genetic analyses among ten wild populations, and within four populations. Genetic correlations between age and size at first reproduction were always greater than +0.8 within and among all populations studied. Although quantitative genetics might provide insight about genetic constraints if genetic parameters remain approximately constant, little evidence has been available to determine the constancy of genetic correlations. I found strong and consistent estimates of genetic correlations between life-history components, which were very similar within four natural populations. Population differentiation also showed these same trade-offs, resulting from long-term genetic constraint. For some traits, evolutionary changes among populations were incompatible with a model of genetic drift. Historical patterns of natural selection were inferred from population differentiation, suggesting that correlated response to selection has caused some traits to evolve opposite to the direct forces of natural selection. Comparison with Arabidopsis suggests that these life-history trade-offs are caused by genes that regulate patterns of resource allocation to different components of fitness. Ecological and energetic models may correctly predict these trade-offs because there is little additive genetic variation for rates of resource acquisition, but resource allocation is genetically variable.     

Costs of resistance: genetic correlations and potential trade-offs in an insect immune system

Theory predicts that natural selection will erode additive genetic variation in fitness-related traits. However, numerous studies have found considerable heritable variation in traits related to immune function, which should be closely linked to fitness. This could be due to trade-offs maintaining variation in these traits. We used the Egyptian cotton leafworm, Spodoptera littoralis, as a model system to examine the quantitative genetics of insect immune function. We estimated the heritabilities of several different measures of innate immunity and the genetic correlations between these immune traits and a number of life history traits. Our results provide the first evidence for a potential genetic trade-off within the insect immune system, with antibacterial activity (lysozyme-like) exhibiting a significant negative genetic correlation with haemocyte density, which itself is positively genetically correlated with both haemolymph phenoloxidase activity and cuticular melanization. We speculate on a potential trade-off between defence against parasites and predators, mediated by larval colour, and its role in maintaining genetic variation in traits under natural selection.     

An evolutionary quantitative genetics model for phenotypic (co)variances under limited dispersal,with an application to socially synergistic traits

Darwinian evolution consists of the gradual transformation of heritable traits due to natural selection and the input of random variation by mutation. Here, we use a quantitative genetics approach to investigate the coevolution of multiple quantitative traits under selection, mutation, and limited dispersal. We track the dynamics of trait means and of variance–covariances between traits that experience frequency‐dependent selection. Assuming a multivariate‐normal trait distribution, we recover classical dynamics of quantitative genetics, as well as stability and evolutionary branching conditions of invasion analyses, except that due to limited dispersal, selection depends on indirect fitness effects and relatedness. In particular, correlational selection that associates different traits within‐individuals depends on the fitness effects of such associations between‐individuals. We find that these kin selection effects can be as relevant as pleiotropy for the evolution of correlation between traits. We illustrate this with an example of the coevolution of two social traits whose association within‐individuals is costly but synergistically beneficial between‐individuals. As dispersal becomes limited and relatedness increases, associations between‐traits between‐individuals become increasingly targeted by correlational selection. Consequently, the trait distribution goes from being bimodal with a negative correlation under panmixia to unimodal with a positive correlation under limited dispersal.     

The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids

Genetic correlations among phenotypic characters result when two traits are influenced by the same genes or sets of genes. By reducing the degree to which traits in two environments can evolve independently (e.g., Lande 1979; Via and Lande 1985), such correlations are likely to play a central role in both the evolution of ecological specialization and in its link to speciation. For example, negative genetic correlations between fitness traits in different environments (i.e., genetic trade-offs) are thought to influence the evolution of specialization, while positive genetic correlations between performance and characters influencing assortative mating can accelerate the evolution of reproductive isolation between ecologically specialized populations. We first discuss how the genetic architecture of a suite of traits may affect the evolutionary role of genetic correlations among them and review how the mechanisms of correlations can be analyzed using quantitative trait locus (QTL) mapping. We then consider the implications of such data for understanding the evolution of specialization and its link to speciation. We illustrate this approach with a QTL analysis of key characters in two races of pea aphids that are highly specialized on different host plants and partially reproductively isolated. Our results suggest that antagonism among QTL effects on performance in the two environments leads to a genetic trade-off in this system. We also found evidence for parallel QTL effects on host-plant acceptance and fecundity on the accepted host, which could produce assortative mating. These results suggest that the genetic architecture of traits associated with host use may have played a central role in the evolution of specialization and reproductive isolation in pea aphids.     

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho‐functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro‐ and micro‐evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro‐evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness‐related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex‐specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co‐evolution between morphology and flight behaviour.     

Selection, inheritance, and the evolution of parent-offspring interactions

Very few studies have examined parent-offspring interactions from a quantitative genetic perspective. We used a cross-fostering design and measured genetic correlations and components of social selection arising from two parental and two offspring behaviors in the burying beetle Nicrophorus vespilloides. Genetic correlations were assessed by examining behavior of relatives independent of common social influences. We found positive genetic correlations between all pairs of behaviors, including between parent and offspring behaviors. Patterns of selection were assessed by standardized performance and selection gradients. Parental provisioning had positive effects on offspring performance and fitness, while remaining near the larvae without feeding them had negative effects. Begging had positive effects on offspring performance and fitness, while increased competition among siblings had negative effects. Coadaptations between parenting and offspring behavior appear to be maintained by genetic correlations and functional trade-offs; parents that feed their offspring more also spend more time in the area where they can forage for themselves. Families with high levels of begging have high levels of sibling competition. Integrating information from genetics and selection thus provides a general explanation for why variation persists in seemingly beneficial traits expressed in parent-offspring interactions and illustrates why it is important to measure functionally related suites of behaviors.     

Variation,selection and evolution of function-valued traits

We describe an emerging framework for understanding variation, selection and evolution of phenotypic traits that are mathematical functions. We use one specific empirical example – thermal performance curves (TPCs) for growth rates of caterpillars – to demonstrate how models for function-valued traits are natural extensions of more familiar, multivariate models for correlated, quantitative traits. We emphasize three main points. First, because function-valued traits are continuous functions, there are important constraints on their patterns of variation that are not captured by multivariate models. Phenotypic and genetic variation in function-valued traits can be quantified in terms of variance-covariance functions and their associated eigenfunctions: we illustrate how these are estimated as well as their biological interpretations for TPCs. Second, selection on a function-valued trait is itself a function, defined in terms of selection gradient functions. For TPCs, the selection gradient describes how the relationship between an organism's performance and its fitness varies as a function of its temperature. We show how the form of the selection gradient function for TPCs relates to the frequency distribution of environmental states (caterpillar temperatures) during selection. Third, we can predict evolutionary responses of function-valued traits in terms of the genetic variance-covariance and the selection gradient functions. We illustrate how non-linear evolutionary responses of TPCs may occur even when the mean phenotype and the selection gradient are themselves linear functions of temperature. Finally, we discuss some of the methodological and empirical challenges for future studies of the evolution of function-valued traits.     

The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle

The genetic basis of host plant use by phytophagous insects can provide insight into the evolution of ecological niches, especially phenomena such as specialization and phylogenetic conservatism. We carried out a quantitative genetic analysis of multiple host use traits, estimated on five species of host plants, in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Mean values of all characters varied among host plants, providing evidence that adaptation to plants may require evolution of both behavioral (preference) and post-ingestive physiological (performance) characteristics. Significant additive genetic variation was detected for several characters on several hosts, but not in the capacity to use the two major hosts, a pattern that might be caused by directional selection. No negative genetic correlations across hosts were detected for any 'performance' traits, i.e. we found no evidence of trade-offs in fitness on different plants. Larval consumption was positively genetically correlated across host plants, suggesting that diet generalization might evolve as a distinct trait, rather than by independent evolution of feeding responses to each plant species, but several other traits did not show this pattern. We explored genetic correlations among traits expressed on a given plant species, in a first effort to shed light on the number of independent traits that may evolve in response to selection for host-plant utilization. Most traits were not correlated with each other, implying that adaptation to a novel potential host could be a complex, multidimensional 'character' that might constrain adaptation and contribute to the pronounced ecological specialization and the phylogenetic niche conservatism that characterize many clades of phytophagous insects.     

Multilevel selection 1: Quantitative genetics of inheritance and response to selection

Interaction among individuals is universal, both in animals and in plants, and substantially affects evolution of natural populations and responses to artificial selection in agriculture. Although quantitative genetics has successfully been applied to many traits, it does not provide a general theory accounting for interaction among individuals and selection acting on multiple levels. Consequently, current quantitative genetic theory fails to explain why some traits do not respond to selection among individuals, but respond greatly to selection among groups. Understanding the full impacts of heritable interactions on the outcomes of selection requires a quantitative genetic framework including all levels of selection and relatedness. Here we present such a framework and provide expressions for the response to selection. Results show that interaction among individuals may create substantial heritable variation, which is hidden to classical analyses. Selection acting on higher levels of organization captures this hidden variation and therefore always yields positive response, whereas individual selection may yield response in the opposite direction. Our work provides testable predictions of response to multilevel selection and reduces to classical theory in the absence of interaction. Statistical methodology provided elsewhere enables empirical application of our work to both natural and domestic populations.     

The genetic basis of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats

We used a quantitative trait locus (QTL) approach to study the genetic basis of population differentiation in wild barley, Hordeum spontaneum. Several ecotypes are recognized in this model species, and population genetic studies and reciprocal transplant experiments have indicated the role of local adaptation in shaping population differences. We derived a mapping population from a cross between a coastal Mediterranean population and a steppe inland population from Israel and assessed F3 progeny fitness in the natural growing environments of the two parental populations. Dilution of the local gene pool, estimated as the proportion of native alleles at 96 marker loci in the recombinant lines, negatively affected fitness traits at both sites. QTLs for fitness traits tended to differ in the magnitude but not in the direction of their effects across sites, with beneficial alleles generally conferring a greater fitness advantage at their native site. Several QTLs showed fitness effects at one site only, but no opposite selection on individual QTLs was observed across the sites. In a common-garden experiment, we explored the hypothesis that the two populations have adapted to divergent nutrient availabilities. In the different nutrient environments of this experiment, but not under field conditions, fitness of the F3 progeny lines increased with the number of heterozygous marker loci. Comparison of QTL-effects that underlie genotype x nutrient interaction in the common-garden experiment and genotype x site interaction in the field suggested that population differentiation at the field sites may have been driven by divergent nutrient availabilities to a limited extent. Also in this experiment no QTLs were observed with opposite fitness effects in contrasting environments. Our data are consistent with the view that adaptive differentiation can be based on selection on multiple traits changing gradually along ecological gradients. This can occur without QTLs showing opposite fitness effects in the different environments, that is, in the absence of genetic trade-offs in performance between environments.     

On the transfer of fitness from the cell to the multicellular organism

The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ–soma specialization and the emergence of individuality at the cell group (or organism) level are also consequences of trade-offs between the two basic fitness components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae – which contain both unicellular and multicellular members – to illustrate the principles and conclusions discussed.     

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     

Optimality modelling and quantitative genetics as alternatives to study the evolution of foraging behaviours in insect herbivores.

Summary Although the evolution of large-scale dispersal has received considerable attention, we know very little about how natural selection influences foraging behaviours in herbivorous insects. Host-selection behaviours and within-habitat movements jointly determine foraging behaviours, since host selection affects the allocation of time spent on a particular host versus moving between these hosts. However, host selection is generally a labile trait, whose expression is influenced by the physiological state of the forager and hence, by characteristics of the habitat. We discuss how the quantitative genetic concepts can be used to study the evolution of such labile behaviours. Since host responses depend on the physiological state of the forager, it is argued that the state of the forager must be explicitly considered when estimating the additive genetic basis of host-selection behaviours. The lability of foraging behaviours increases the difficulty of measuring the fitness consequence of variation in the foraging phenotype in specific habitats. Therefore, it may be difficult to rely exclusively on quantitative genetic methods to test hypotheses about adaptive change in foraging behaviours across different habitats. We provide a novel approach based on optimality modelling to calculate the fitness consequence of variation in the foraging phenotype across different habitats. This method, in conjunction with quantitative genetics, can be used to test hypotheses concerning the evolution of foraging behaviours.     

Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations

Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.