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.

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.

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.

The evolution of mate choice: a dialogue between theory and experiment.

Research on the evolution of mate choice has followed three avenues of investigation: (1) theoretical models of the evolution of preference and the preferred trait; (2) proposed models of mate choice; and (3) experiments and observations on mate choice, both in the laboratory and with free-ranging animals. However, there has been relatively little dialogue among these three areas. Most attempts to account for observations of mate choice using theoretical mate-choice models have focused only upon a subset of particular models and have generally failed to consider the difference between probabilistic and deterministic models. In this review, I outline the underlying reasoning of the commonly cited mate-choice models and review the conclusions of the empirical investigations. I present a brief outline of how one might go about testing these models. It remains uncertain if, in general, mate-choice models can be realistically analyzed. Although it is clear that females frequently discriminate among males, data also suggest that females may typically have a very limited number of males from which to choose. The extent to which female choice under natural conditions is relatively random because of limited opportunities remains an open question for the majority of species.

Are we underestimating the genetic variances of dimorphic traits?

Populations often contain discrete classes or morphs (e.g., sexual dimorphisms, wing dimorphisms, trophic dimorphisms) characterized by distinct patterns of trait expression. In quantitative genetic analyses, the different morphs can be considered as different environments within which traits are expressed. Genetic variances and covariances can then be estimated independently for each morph or in a combined analysis. In the latter case, morphs can be considered as separate environments in a bivariate analysis or entered as fixed effects in a univariate analysis. Although a common approach, we demonstrate that the latter produces downwardly biased estimates of additive genetic variance and heritability unless the quantitative genetic architecture of the traits concerned is perfectly correlated between the morphs. This result is derived for four widely used quantitative genetic variance partitioning methods. Given that theory predicts the evolution of genotype-by-environment (morph) interactions as a consequence of selection favoring different trait combinations in each morph, we argue that perfect correlations between the genetic architectures of the different morphs are unlikely. A sampling of the recent literature indicates that the majority of researchers studying traits expressed in different morphs recognize this and do estimate morph-specific quantitative genetic architecture. However, ca. 16% of the studies in our sample utilized only univariate, fixed-effects models. We caution against this approach and recommend that it be used only if supported by evidence that the genetic architectures of the different morphs do not differ.

The evolution of phenotypes and genetic parameters under preferential mating.

This article extends and adds more realism to Lande's analytical model for evolution under mate choice by using individual-based simulations in which females sample a finite number of males and the genetic architecture of the preference and preferred trait evolves. The simulations show that the equilibrium heritabilities of the preference and preferred trait and the genetic correlation between them (r G), depend critically on aspects of the mating system (the preference function, mode of mate choice, choosiness, and number of potential mates sampled), the presence or absence of natural selection on the preferred trait, and the initial genetic parameters. Under some parameter combinations, preferential mating increased the heritability of the preferred trait, providing a possible resolution for the lek paradox. The Kirkpatrick-Barton approximation for r G proved to be biased downward, but the realized genetic correlations were also low, generally <0.2. Such low values of r G indicate that coevolution of the preference and preferred trait is likely to be very slow and subject to significant stochastic variation. Lande's model accurately predicted the incidence of runaway selection in the simulations, except where preferences were relative and the preferred trait was subject to natural selection. In these cases, runaways were over- or underestimated, depending on the number of males sampled. We conclude that rapid coevolution of preferences and preferred traits is unlikely in natural populations, but that the parameter combinations most conducive to it are most likely to occur in lekking species.

Evolutionary optimality in sex differences of longevity and athletic performances.

Many sexual differences are known in human and animals. It is well known that females are superior in longevity, while males in athletic performances. Even though some sexual differences are attributed to the evolutionary tradeoff between survival and reproduction, the aforementioned sex differences are difficult to explain by this tradeoff. Here we show that the evolutionary tradeoff occurs among three components: (1) viability, (2) competitive ability and (3) reproductive effort. The sexual differences in longevity and athletic performances are attributed to the tradeoff between viability (survival) and competitive ability that belongs to the physical makeup of an individual, but not related to the tradeoff between survival and reproduction. This provides a new perspective on sex differences in human and animals: females are superior in longevity and disease recovery, while males are superior in athletic performance.

Fine-tuned bee-flower coevolutionary state hidden within multiple pollination interactions.

Relationships between flowers and pollinators are generally considered cases of mutualism since both agents gain benefits. Fine-tuned adaptations are usually found in the form of strict one-to-one coevolution between species. Many insect pollinators are, however, considered generalists, visiting numerous kinds of flowers, and many flower species (angiosperms) are also considered generalists, visited by many insect pollinators. We here describe a fine-tuned coevolutionary state of a flower-visiting bee that collects both nectar and pollen from an early spring flower visited by multiple pollinators. Detailed morphology of the bee proboscis is shown to be finely adjusted to the floral morphology and nectar production of the flower. Behavioral observations also confirm the precision of this mutualism. Our results suggest that a fine-tuned one-to-one coevolutionary state between a flower species and a pollinator species might be common, but frequently overlooked, in multiple flower-pollinator interactions.

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.

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.

Environmental and genetic controls of soldier caste in a parasitic social wasp.

A larval army caste is found in some parasitic wasps with polyembryonic or clonal proliferation, where many clone larvae emerge from a single egg. In contrast to non-parasitic eusocial Hymenoptera, sterile soldier larvae that protect their clonal reproductives are found in both females and males. Recently, the proportion of soldier larvae has been found to vary radically, depending on the internal conditions of the host, such as multiparasitism by other larval parasites. However, the proportion of male soldier larvae is constant, irrespective of the host internal environment. It is unknown if these traits are heritable. Here we show that a high heritability is found in both sexes, while, in the 6th instar hosts, substantially lower heritability is found in females. These results imply that the structure of the larval caste is determined genetically by both female and male embryonic cells, but more likely modified environmentally in females.

Predicting the response to simultaneous selection: genetic architecture and physiological constraints.

A great deal is known about the evolutionary significance of body size and development time. They are determined by the nonlinear interaction of three physiological traits: two hormonal events and growth rate (GR). In this study we investigate how the genetic architecture of the underlying three physiological traits affects the simultaneous response to selection on the two life-history traits in the hawkmoth Manduca sexta. The genetic architecture suggests that when the two life-history traits are both selected in the same direction (to increase or decrease) the response to selection is primarily determined by the hormonal mechanism. When the life-history traits are selected in opposite directions (one to increase and one to decrease) the response to selection is primarily determined by factors that affect the GR. To determine how the physiological traits affect the response to selection of the life-history traits, we simulated the predicted response to 10 generations of selection. A total of 83% of our predictions were supported by the simulation. The main components of this physiological framework also exist in unicellular organisms, vertebrates, and plants and can thus provide a robust framework for understanding how underlying physiology can determine the simultaneous evolution of life-history traits.

A test of the hypothesis that correlational selection generates genetic correlations.

Theory predicts that correlational selection on two traits will cause the major axis of the bivariate G matrix to orient itself in the same direction as the correlational selection gradient. Two testable predictions follow from this: for a given pair of traits, (1) the sign of correlational selection gradient should be the same as that of the genetic correlation, and (2) the correlational selection gradient should be positively correlated with the value of the genetic correlation. We test this hypothesis with a meta-analysis utilizing empirical estimates of correlational selection gradients and measures of the correlation between the two focal traits. Our results are consistent with both predictions and hence support the underlying hypothesis that correlational selection generates a genetic correlation between the two traits and hence orients the bivariate G matrix.

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.

The evolution of trade-offs under directional and correlational selection.

Using quantitative genetic theory, we develop predictions for the evolution of trade-offs in response to directional and correlational selection. We predict that directional selection favoring an increase in one trait in a trade-off will result in change in the intercept but not the slope of the trade-off function, with the mean value of the selected trait increasing and that of the correlated trait decreasing. Natural selection will generally favor an increase in some combination of trait values, which can be represented as directional selection on an index value. Such selection induces both directional and correlational selection on the component traits. Theory predicts that selection on an index value will also change the intercept but not the slope of the trade-off function but because of correlational selection, the direction of change in component traits may be in the same or opposite directions. We test these predictions using artificial selection on the well-established trade-off between fecundity and flight capability in the cricket, Gryllus firmus and compare the empirical results with a priori predictions made using genetic parameters from a separate half-sibling experiment. Our results support the predictions and illustrate the complexity of trade-off evolution when component traits are subject to both directional and correlational selection.

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.

The evolutionary genetics of acquisition and allocation in the wing dimorphic cricket, Gryllus firmus.

The evolutionary trajectories of trade-offs are ultimately governed by the evolution of the underlying physiological processes of the acquisition and subsequent allocation of resources. In this study, we focused directly on acquisition and allocation as traits and estimated their genetic architecture in the trade-off between flight capability and reproduction in the cricket, Gryllus firmus. To determine the evolutionary genetics of acquisition and allocation both within and between resource environments, we performed a large-scale quantitative genetic breeding experiment in which families were split over several resource levels. Our findings were fourfold: (1) there was substantial genetic variance in acquisition and allocation, (2) contrary to the assumption of independence between acquisition and allocation, there was a significant genetic correlation between them, (3) the genetic covariance between acquisition and allocation was significantly different in the different food environments, (4) the trade-off, as measured by the genetic correlation between flight muscle mass and ovary mass, was only significant in the food restriction environments. However, when measured directly as the genetic correlation between reproductive allocation and flight allocation, we found a consistent strong negative genetic correlation, demonstrating that when allocation is measured independently of acquisition we find evidence for the trade-off.