Drift on holey landscapes as a dominant evolutionary process.

An organism's phenotype has been shaped by evolution but the specific processes have to be indirectly inferred for most species. For example, correlations among traits imply the historical action of correlated selection and, more generally, the expression and distribution of traits is expected to be reflective of the adaptive landscapes that have shaped a population. However, our expectations about how quantitative traits-like most behaviors, physiological processes, and life-history traits-should be distributed under different evolutionary processes are not clear. Here, we show that genetic variation in quantitative traits is not distributed as would be expected under dominant evolutionary models. Instead, we found that genetic variation in quantitative traits across six phyla and 60 species (including both Plantae and Animalia) is consistent with evolution across high-dimensional "holey landscapes." This suggests that the leading conceptualizations and modeling of the evolution of trait integration fail to capture how phenotypes are shaped and that traits are integrated in a manner contrary to predictions of dominant evolutionary theory. Our results demonstrate that our understanding of how evolution has shaped phenotypes remains incomplete and these results provide a starting point for reassessing the relevance of existing evolutionary models.

Tests for associations between sexual dimorphism and patterns of quantitative genetic variation in the water strider, Aquarius remigis.

The evolution of sexual dimorphisms requires divergence between sexes in the evolutionary trajectories of the traits involved. Discerning how genetic architecture could facilitate such divergence has proven challenging because of the difficulty in estimating non-additive and sex-linked genetic variances using traditional quantitative genetic designs. Here we use a three-generation, double-first-cousin pedigree design to estimate additive, sex-linked and dominance (co)variances for 12 traits in the water strider, Aquarius remigis. Comparisons among these traits, which have size ratios ranging from 1 to 5 (larger/smaller), allow us to ask if sexual dimorphisms are associated with characteristic patterns of quantitative genetic variation. We frame our analysis around three main questions, derived from existing theory and empirical evidence: Are sexual dimorphisms associated with (1) lower additive inter-sex genetic correlations, (2) higher proportions of sex-linked variance, or (3) differences between sexes in autosomal additive and dominance genetic variances? For questions (1) and (2), we find weak and non-significant trends in the expected directions, which preclude definitive conclusions. However, in answer to question (3), we find strong evidence for a positive relationship between sexual dimorphism and differences between sexes in proportions of autosomal dominance variance. We also find strong interactions among the three genetic components indicating that their relative influence differs among traits and between sexes. These results highlight the need to include all three components of genetic (co)variance in both theoretical evolutionary models and empirical estimations of the genetic architecture of dimorphic traits.

Evolutionary potential of thermal preference and heat tolerance in Drosophila subobscura.

Evolutionary change of thermal traits (i.e., heat tolerance and behavioural thermoregulation) is one of the most important mechanisms exhibited by organisms to respond to global warming. However, the evolutionary potential of heat tolerance, estimated as narrow-sense heritability, depends on the methodology employed. An alternative adaptive mechanism to buffer extreme temperatures is behavioural thermoregulation, although the association between heat tolerance and thermal preference is not clearly understood. We suspect that methodological effects associated with the duration of heat stress during thermal tolerance assays are responsible for missing this genetic association. To test this hypothesis, we estimated the heritabilities and genetic correlations for thermal traits in Drosophila subobscura, using high-temperature static and slow ramping assays. We found that heritability for heat tolerance was higher in static assays (h2  = 0.134) than in slow ramping assays (h2  = 0.084), suggesting that fast assays may provide a more precise estimation of the genetic variation of heat tolerance. In addition, thermal preference exhibited a low heritability (h2  = 0.066), suggesting a reduced evolutionary response for this trait. We also found that the different estimates of heat tolerance and thermal preference were not genetically correlated, regardless of how heat tolerance was estimated. In conclusion, our data suggest that these thermal traits can evolve independently in this species. In agreement with previous evidence, these results indicate that methodology may have an important impact on genetic estimates of heat tolerance and that fast assays are more likely to detect the genetic component of heat tolerance.

Testing the aerobic model for the evolution of endothermy: implications of using present correlations to infer past evolution.

The evolution of endothermy is one of the most puzzling events in vertebrate evolution, for which several hypotheses have been proposed. The most accepted model is the aerobic model, which assumes the existence of a genetic correlation between resting metabolic rate (RMR) and maximum aerobic capacity (whose standard measure is maximum metabolic rate, MMR). This model posits that directional selection acted on maximum aerobic capacity and resting metabolic rate increased as a correlated response, in turn increasing body temperature. To test this hypothesis we implemented a simple two-trait quantitative genetic model in which RMR and MMR are initially independent of each other and subject to stabilizing selection to two separate optima. We show mutations that arise that affect both traits can lead to the evolution of a genetic correlation between the traits without any significant shifting of the two trait means. Thus, the presence of a genetic correlation between RMR and MMR in living animals provides no support in and of itself for the past elevation of metabolic rate via selection on aerobic capacity. This result calls into question the testability of the hypothesis that RMR increased as a correlated response to directional selection on MMR, in turn increasing body temperature, using quantitative genetics. Given the difficulty in studying ancient physiological processes, we suggest that approaches such as this model are a valuable alternative for analyzing possible mechanisms of endothermy evolution.

The deleterious effects of high inbreeding on male Drosophila melanogaster attractiveness are observed under competitive but not under non-competitive conditions.

In order for the male courtship traits to honestly signal quality they need to be condition-dependent. Moreover, if these traits capture genetic variation in condition they should resemble life-history traits in being subject to strong directional selection and, consequently, suffer strong inbreeding depression. In this study we investigated the effect of high inbreeding on male attractiveness by assessing mating success, mating speed and copulation duration of inbred, outbred and crossbred (constructed by crossing separate, randomly chosen inbred lines) males of Drosophila melanogaster. When set to compete against a standardized competitor and compared to the success rate of the crossbred lines, inbreeding significantly reduced male mating success. Under competition, outbred males initiated copulation significantly sooner than crossbred and inbred males. Under non-competitive conditions, no effect of inbreeding was found on either mating speed or copulation duration. Both mating success and mating speed showed much higher inbreeding depression than male size.

Extracting the underlying physiological determinants of resource-based trade-offs: a principal components approach.

The relationship between traits that compete for resources is influenced by variance in the acquisition and allocation of resources. The difficulty of accurately measuring these underlying physiological processes has hampered studies of resource-based trade-offs. Here, we explore the ability of principal components analysis (PCA) to extract axes corresponding to acquisition and allocation in a bivariate trade-off by comparing these axes to estimates obtained using physiological measurements. We validate the method using simulations and then test it using empirical data for the well-characterized trade-off between flight capability and reproduction in female sand crickets, Gryllus firmus. We find a high correspondence between our physiological estimates and the estimates obtained using PCA. Our results demonstrate that PCA provides a robust and efficient method for estimating acquisition and allocation directly from the traits involved in a resource-based trade-off.

Analysis of the effects of inbreeding on lifespan and starvation resistance in Drosophila melanogaster.

Because of their decreased overall fitness and genetic variability inbred individuals are expected to show reduced survival and lifespan under most environmental conditions as compared with outbred individuals. Whereas evidence for the deleterious effects of inbreeding on lifespan has been previously provided, only a few studies have investigated effects of inbreeding on survival under starved conditions. In the present study we compared the abilities of inbred and outbred adult Drosophila melanogaster to survive under starved and fed conditions. We found that inbreeding reduced lifespan but had no effect on starvation resistance. The results indicate highly trait specific consequences of inbreeding. Possible mechanisms behind the observed results are discussed.

Effects of inbreeding on potential and realized immune responses in Tenebrio molitor.

Although numerous studies on vertebrates suggest that inbreeding reduces their resistance against parasites and pathogens, studies in insects have found contradictory evidence. In this study we tested the effect of 1 generation of brother-sister mating (inbreeding) on potential and realized immune responses and other life-history traits in Tenebrio molitor. We found that inbreeding reduced adult mass, pre-adult survival and increased development time, suggesting that inbreeding reduced the condition of the adults and thus potentially made them more susceptible to physiological stress. However, we found no significant effect of inbreeding on the potential immune response (encapsulation response), but inbreeding reduced the realized immune response (resistance against the entomopathogenic fungi, Beauveria bassiana). There was a significant family effect on encapsulation response, but no family effect on the resistance against the entomopathogenic fungi. Given that this latter trait showed significant inbreeding depression and that the sample size for the family-effect analysis was small it is likely that the lack of a significant family effect is due to reduced statistical power, rather than the lack of a heritable basis to the trait. Our study highlights the importance of using pathogens and parasites in immunoecological studies.

Effects of shape variations on the energy metabolism of the sand cricket Gryllus firmus: a geometric morphometric analysis.

Respiration and energy metabolism are key processes in animals, which are severely constrained by the design of physical structures, such as respiratory structures. Insects have very particular respiratory systems, based on gas diffusion across tracheae. Since the efficiency of the tracheal respiratory system is highly dependent on body shape, the pattern of morphological variation during ontogeny could have important metabolic consequences. We studied this problem combining through-flow respirometry and geometric morphometrics in 88 nymphs of the sand cricket, Gryllus firmus. After measuring production in each individual, we took digital photographs and defined eight landmarks for geometric morphometric analysis. The analysis suggested that ontogenic deformations were mostly related to enlargement of the abdomen, compared to thorax and head. We found that (controlling for body size) metabolic variables and especially resting metabolism are positively correlated with a shape-component associated to an elongation of the abdomen. Our results are in agreement with the mechanics of tracheal ventilation in orthopterans, as gas circulation occurs by changes in abdominal pressures due to abdominal contractions and expansions along the longitudinal axis.

Modeling the evolution of phenotypic plasticity in resource allocation in wing-dimorphic insects.

In nature, resource availability varies spatially and temporally both within and across generations, leading to variation in the amount of energy available to individuals. The optimal allocation strategy can change, depending on the amount of resources available to allocate to life-history functions. If so, selection should favor the evolution of allocation strategies that can respond to variation in environmental resource levels. We address this issue by using two quantitative genetic simulation models in a model system for studying trade-offs, wing-dimorphic insects. Wing dimorphic insects typically exhibit a trade-off in the allocation of resources between migratory ability and reproduction. In our models, we focus on allocation as a genetic trait and model the evolution of phenotypic plasticity in this trait in response to spatiotemporal variation in resource availability. We show that the evolved allocation strategy depends on the predictability of resource levels across time. Specifically, selection favors higher investment in flight under poor conditions in predictable environments and lower investment in unpredictable environments.

Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology.

Predation plays a central role in evolutionary processes, but little is known about how predators affect the expression of heritable variation, restricting our ability to predict evolutionary effects of predation. We reared families of three-spined stickleback Gasterosteus aculeatus from two populations-one with a history of fish predation (predator sympatric) and one without (predator naive)-and experimentally manipulated experience of predators during ontogeny. For a suite of ecologically relevant behavioural ('personality') and morphological traits, we then estimated two key variance components, additive genetic variance (VA) and residual variance (VR), that jointly shape narrow-sense heritability (h2=VA/(VA+VR)). Both population and treatment differentially affected VA versus VR, hence h2, but only for certain traits. The predator-naive population generally had lower VA and h2 values than the predator-sympatric population for personality behaviours, but not morphological traits. Values of VR and h2 were increased for some, but decreased for other personality traits in the predator-exposed treatment. For some personality traits, VA and h2 values were affected by treatment in the predator-naive population, but not in the predator-sympatric population, implying that the latter harboured less genetic variation for behavioural plasticity. Replication and experimental manipulation of predation regime are now needed to confirm that these population differences were related to variation in predator-induced selection. Cross-environment genetic correlations (rA) were tight for most traits, suggesting that predator-induced selection can affect the evolution of the same trait expressed in the absence of predators. The treatment effects on variance components imply that predators can affect evolution, not only by acting directly as selective agents, but also by influencing the expression of heritable variation.

Defining fitness in evolutionary models.

The analysis of evolutionary models requires an appropriate definition for fitness. In this paper, I review such definitions in relation to the five major dimensions by which models may be described, namely (i) finite versus infinite (or very large) population size, (ii) type of environment (constant, fixed length, temporally stochastic, temporally predictable, spatially stochastic, spatially predictable and social environment), (iii) density-independent or density-dependent, (iv) inherent population dynamics (equilibrium, cyclical and chaotic), and (v) frequency dependent or independent. In simple models, the Malthusian parameter 'r' or the net reproductive rate R(0) may be satisfactory, but once density-dependence or complex population dynamics is introduced the invasion exponent should be used. Defining fitness in a social environment or when there is frequency-dependence requires special consideration.

Four types of vibration behaviors in a mole cricket.

Vibrational communication is known in some subterranean insects. Except for their use in sexual signaling, vibration behavior has rarely been reported. We report here four distinct types of substrate-based vibration behaviors in the mole cricket, Gryllotalpa orientalis, which are not associated with sexual signaling because of the occurrence of these behaviors in nymphs: (1) scraping with the forelegs; (2) foreleg taps (tapping with the forelegs); (3) palpal taps (tapping with the maxillary palpi); and (4) tremulation (back-and-forth movement of the whole body). Scraping is hypothesized to be used for the inspection of borrows. Foreleg taps are possibly informing nearby individuals of their presence, because it is never observed in solitary conditions. Palpal taps are rarely observed and its function is unknown. Tremulation is possibly related to avoidance of conspecific individual approaching and touching. The combination of the four vibration behaviors in the mole cricket may be unique among insects.

A centennial celebration for quantitative genetics.

Quantitative genetics is at or is fast approaching its centennial. In this perspective I consider five current issues pertinent to the application of quantitative genetics to evolutionary theory. First, I discuss the utility of a quantitative genetic perspective in describing genetic variation at two very different levels of resolution, (1) in natural, free-ranging populations and (2) to describe variation at the level of DNA transcription. Whereas quantitative genetics can serve as a very useful descriptor of genetic variation, its greater usefulness is in predicting evolutionary change, particularly when used in the first instance (wild populations). Second, I review the contributions of Quantitative trait loci (QLT) analysis in determining the number of loci and distribution of their genetic effects, the possible importance of identifying specific genes, and the ability of the multivariate breeder's equation to predict the results of bivariate selection experiments. QLT analyses appear to indicate that genetic effects are skewed, that at least 20 loci are generally involved, with an unknown number of alleles, and that a few loci have major effects. However, epistatic effects are common, which means that such loci might not have population-wide major effects: this question waits upon (QTL) analyses conducted on more than a few inbred lines. Third, I examine the importance of research into the action of specific genes on traits. Although great progress has been made in identifying specific genes contributing to trait variation, the high level of gene interactions underlying quantitative traits makes it unlikely that in the near future we will have mechanistic models for such traits, or that these would have greater predictive power than quantitative genetic models. In the fourth section I present evidence that the results of bivariate selection experiments when selection is antagonistic to the genetic covariance are frequently not well predicted by the multivariate breeder's equation. Bivariate experiments that combine both selection and functional analyses are urgently needed. Finally, I discuss the importance of gaining more insight, both theoretical and empirical, on the evolution of the G and P matrices.

Laboratory evolution of the migratory polymorphism in the sand cricket: combining physiology with quantitative genetics.

Predicting evolutionary change is the central goal of evolutionary biology because it is the primary means by which we can test evolutionary hypotheses. In this article, we analyze the pattern of evolutionary change in a laboratory population of the wing-dimorphic sand cricket Gryllus firmus resulting from relaxation of selection favoring the migratory (long-winged) morph. Based on a well-characterized trade-off between fecundity and flight capability, we predict that evolution in the laboratory environment should result in a reduction in the proportion of long-winged morphs. We also predict increased fecundity and reduced functionality and weight of the major flight muscles in long-winged females but little change in short-winged (flightless) females. Based on quantitative genetic theory, we predict that the regression equation describing the trade-off between ovary weight and weight of the major flight muscles will show a change in its intercept but not in its slope. Comparisons across generations verify all of these predictions. Further, using values of genetic parameters estimated from previous studies, we show that a quantitative genetic simulation model can account for not only the qualitative changes but also the evolutionary trajectory. These results demonstrate the power of combining quantitative genetic and physiological approaches for understanding the evolution of complex traits.

Epistasis and dominance: evidence for differential effects in life-history versus morphological traits.

Dominance and epistatic effects are predicted to be larger in life-history than in morphological traits. We test these predictions using published results from line cross analyses. We find that dominance is found in more than 95% of traits, regardless of the type of trait, but that the magnitude of the effect in relation to the additive effect is much greater in life-history than in morphological traits. Epistatic effects were detected more often in life-history than in morphological traits (79% and 67%, respectively). We also test for a difference in the magnitude of the effects by comparing the ratio of the nonadditive components separately to the additive component. For both dominance and epistatic components, the ratio of the nonadditive component to additive effects in life-history traits is approximately twice as large as that for morphological traits.

Co-occurrence of ecologically equivalent cryptic species of spider wasps.

Many cryptic species have been discovered in various taxonomic groups based on molecular phylogenetic analyses and mating experiments. Some sympatric cryptic species share equivalent resources, which contradicts the competitive exclusion principle. Two major theories have been proposed to explain the apparent lack of competitive exclusion, i.e. niche-based coexistence and neutral model, but a conclusive explanation is lacking. Here, we report the co-occurrence of cryptic spider wasp species appearing to be ecologically equivalent. Molecular phylogenetic analyses and mating experiments revealed that three phylogenetically closely related species are found sympatrically in Japan. These species share the same resources for larval food, and two of the species have the same niche for nesting sites, indicating a lack of competitive exclusion. This evidence may suggest that ecologically equivalent species can co-occur stably if their shared resources are sufficiently abundant that they cannot be over-exploited.

Dissecting the variance-covariance structure in insect physiology: the multivariate association between metabolism and morphology in the nymphs of the sand cricket (Gryllus firmus).

Energy metabolism in animals has been largely studied in relation to exogenous sources of variation. However, because they give insight into the relationship between whole metabolism and lower organizational levels such as organs and tissues, examination of endogenous determinants of metabolism other than body mass is itself very important. We studied the multivariate association of body parts and several aspects of energy metabolism in an insect, the nymphs of the sand cricket, Gryllus firmus. By using a variety of both univariate and multivariate techniques, we explored the resultant variance-covariance matrix to build a path diagram with latent variables. After controlling for body mass, we found a significant canonical correlation between metabolism and morphology. According to the factor loadings and path coefficients, the most important contributions of morphology to the correlation were thorax and abdomen size measures, whereas the most important metabolic contribution was resting metabolism. Activity metabolism was mostly explained by body mass rather than body parts, which could be a result of resting rates being chronic consequences of the functioning of the metabolic machinery that the insect must maintain.