Quantifying multivariate plasticity: genetic variation in resource acquisition drives plasticity in resource allocation to components of life history

Acquisition and allocation of resources are central to life‐history theory. However, empirical work typically focuses only on allocation despite the fact that relationships between fitness components may be governed by differences in the ability of individuals to acquire resources across environments. Here, we outline a statistical framework to partition the genetic basis of multivariate plasticity into independent axes of genetic variation, and quantify for the first time, the extent to which specific traits drive multitrait genotype–environment interactions. Our framework generalises to analyses of plasticity, growth and ageing. We apply this approach to a unique, large‐scale, multivariate study of acquisition, allocation and plasticity in the life history of the cricket, Gryllus firmus. We demonstrate that resource acquisition and allocation are genetically correlated, and that plasticity in trade‐offs between allocation to components of fitness is 90% dependent on genetic variance for total resource acquisition. These results suggest that genotype–environment effects for resource acquisition can maintain variation in life‐history components that are typically observed in the wild.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

A multivariate test of evolutionary constraints for thermal tolerance in Drosophila melanogaster

Exposure to extreme temperatures is increasingly likely to impose strong selection on many organisms in their natural environments. The ability of organisms to adapt to such selective pressures will be determined by patterns of genetic variation and covariation. Despite increasing interest in thermal adaptation, few studies have examined the extent to which the genetic covariance between traits might constrain thermal responses. Furthermore, it remains unknown whether sex‐specific genetic architectures will constrain responses to climatic selection. We used a paternal half‐sibling breeding design to examine whether sex‐specific genetic architectures and genetic covariances between traits might constrain evolutionary responses to warming climates in a population of Drosophila melanogaster. Our results suggest that the sexes share a common genetic underpinning for heat tolerance as indicated by a strong positive inter‐sexual genetic correlation. Further, we found no evidence in either of the sexes that genetic trade‐offs between heat tolerance and fitness will constrain responses to thermal selection. Our results suggest that neither trade‐offs, nor sex‐specific genetics, will significantly constrain an evolutionary response to climatic warming, at least in this population of D. melanogaster.     

Life‐history trade‐offs promote the evolution of dioecy

Most dioecious plants are perennial and subject to trade‐offs between sexual reproduction and vegetative performance. However, these broader life‐history trade‐offs have not usually been incorporated into theoretical analyses of the evolution of separate sexes. One such analysis has indicated that hermaphroditism is favoured over unisexuality when female and male sex functions involve the allocation of nonoverlapping types of resources to each sex function (e.g. allocations of carbon to female function vs. allocations of nitrogen to male function). However, some dioecious plants appear to conform to this pattern of resource allocation, with different resource types allocated to female vs. male sex functions. Using an evolutionarily stable strategy approach, we show that life‐history trade‐offs between sexual reproduction and vegetative performance enable the evolution of unisexual phenotypes even when there are no direct resource‐based trade‐offs between female and male sex functions. This result might help explain the preponderance of perennial life histories among dioecious plants and why many dioecious plants with annual life histories have indeterminate growth with ongoing trade‐offs between sexual reproduction and vegetative growth.     

Effects of variation in resource acquisition during different stages of the life cycle on life‐history traits and trade‐offs in a burying beetle

Individual variation in resource acquisition should have consequences for life‐history traits and trade‐offs between them because such variation determines how many resources can be allocated to different life‐history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life‐history traits and trade‐offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade‐off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life‐history traits but limited effects on trade‐offs. This suggests that in species that acquire a fixed‐sized resource at the onset of breeding, the size of this resource has larger effects on life‐history trade‐offs than resources acquired at earlier stages.     

When relative allocation depends on total resource acquisition: implication for the analysis of trade‐offs

A central tenet of evolutionary biology states that life‐history traits are linked via trade‐offs, as classically exemplified by the van Noordwijk and de Jong model. This model, however, assumes that the relative resource allocation to a biological function varies independently of the total resource acquisition. Based on current empirical evidence, we first explored the dependency between the total resource acquisition and the relative resource allocation to reproduction and showed that such dependency is the rule rather than the exception. We then derived the expression of the covariance between traits when the assumption of independence is relaxed and used simulations to quantify the importance of such dependency on the detection of trade‐offs between current reproduction and future survival. We found that the dependency between the total energy acquisition and the relative allocation to reproduction can influence the probability to detect trade‐offs between survival and reproduction. As a general rule, a negative dependency between the total energy acquisition and the relative allocation to reproduction should lead to a higher probability of detecting a trade‐off in species with a fast pace of life, whereas a positive dependency should lead to a higher probability of detecting a trade‐off in species with a slow pace of life. In addition to confirming the importance of resource variation to reveal trade‐offs, our finding demonstrates that the covariance between resource allocation and resource acquisition is generally not null and also plays a fundamental role in the detection of trade‐offs.     

Condition‐dependent expression of pre‐ and postcopulatory sexual traits in guppies

Female choice can impose persistent directional selection on male sexually selected traits, yet such traits often exhibit high levels of phenotypic variation. One explanation for this paradox is that if sexually selected traits are costly, only the fittest males are able to acquire and allocate the resources required for their expression. Furthermore, because male condition is dependent on resource allocation, condition dependence in sexual traits is expected to underlie trade‐offs between reproduction and other life‐history functions. In this study we test these ideas by experimentally manipulating diet quality (carotenoid levels) and quantity in the guppy (Poecilia reticulata), a livebearing freshwater fish that is an important model for understanding relationships between pre‐ and post‐copulatory sexually selected traits. Specifically, we test for condition dependence in the expression of pre‐ and postcopulatory sexual traits (behavior, ornamentation, sperm traits) and determine whether diet manipulation mediates relationships among these traits. Consistent with prior work we found a significant effect of diet quantity on the expression of both pre‐ and postcopulatory male traits; diet‐restricted males performed fewer sexual behaviors and exhibited significant reductions in color ornamentation, sperm quality, sperm number, and sperm length than those fed ad libitum. However, contrary to our expectations, we found no significant effect of carotenoid manipulation on the expression of any of these traits, and no evidence for a trade‐off in resource allocation between pre‐ and postcopulatory episodes of sexual selection. Our results further underscore the sensitivity of behavioral, ornamental, and ejaculate traits to dietary stress, and highlight the important role of condition dependence in maintaining the high variability in male sexual traits.     

EVOLUTION OF TRADE-OFFS BETWEEN SEXUAL AND ASEXUAL PHASES AND THE ROLE OF REPRODUCTIVE PLASTICITY IN THE GENETIC ARCHITECTURE OF APHID LIFE HISTORIES

Life‐history theory postulates that evolution is constrained by trade‐offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade‐offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life‐history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry‐oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad‐sense) for all traits and several negative genetic correlations between traits (trade‐offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance–covariance matrices ( G ) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G × E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.     

Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism

Sexual size dimorphism (SSD) describes divergent body sizes of adult males and females. While SSD has traditionally been explained by sexual and fecundity selection, recent advances in physiology and developmental biology emphasize that SSD would occur proximately because of sexual differences in ontogenetic growth trajectories (i.e., growth rate and duration). Notably, these ontogenetic traits are subject to energetic or time constraints and thus traded off with fitness components (e.g., survival and reproduction). To elucidate the importance of such ontogenetic trade‐offs in the evolution of SSD, we developed a new theoretical framework by extending quantitative genetic models for the evolution of sexual dimorphism in which we reinterpret the trait as body size and reformulate sex‐specific fitness in size‐dependent manners. More specifically, we assume that higher growth rate or longer growth duration leads to larger body size and higher reproductive success but incurs the cost of lower survivorship or shorter reproduction period. We illustrate how two sexes would optimize ontogenetic growth trajectories in sex‐specific ways and exhibit divergent body sizes. The present framework provides new insights into the evolutionary theory of SSD and predictions for empirical testing.     

Evolution of male age‐specific reproduction under differential risks and causes of death: males pay the cost of high female fitness

Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high‐condition‐dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex‐specific trade‐offs. Because same life‐history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition‐dependent mortality caused by heat shock leads to evolution of long‐life, decelerated late‐life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early‐life and net reproduction, while mortality rate had no effect. Our results suggest that heat‐shock resistance and associated long‐life trade‐off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.     

Experimental manipulation reveals a trade‐off between weapons and testes

Theory predicts a trade‐off between sexually selected weapons used to secure mates and post‐copulatory traits used to maximize fertilization success. However, individuals that have a greater capacity to acquire resources from the environment may invest more in both pre‐ and post‐copulatory traits, and trade‐offs may not be readily apparent. Here, we manipulate the phenotype of developing individuals to examine allocation trade‐offs between weapons and testes in Mictis profana (Hemiptera: Coreidae), a species where the hind legs are sexually selected weapons used in contests over access to females. We experimentally prevented males from developing weapons by inducing them to autotomize their hind legs before the final moult to adulthood. We compared trait expression in this group to males where autotomy was induced in the mid‐legs, which are presumably not under sexual selection to the same extent. We found males without weapons invested proportionally more in testes mass than those with their mid‐legs removed. Males that developed to adulthood without weapons did not differ from the mid‐leg removal group in other traits potentially under precopulatory sexual selection, other post‐copulatory traits or naturally selected traits. In addition, a sample of adult males from the same population in the wild revealed a positive correlation between investment in testes and weapons. Our study presents a critical contribution to a growing body of literature suggesting the allocation of resources to pre‐ and post‐copulatory sexual traits is influenced by a resource allocation trade‐off and that this trade‐off may only be revealed with experimental manipulation.     

Physiological dynamics,reproduction‐maintenance allocations,and life history evolution

Allocation of resources to competing processes of growth, maintenance, or reproduction is arguably a key process driving the physiology of life history trade‐offs and has been shown to affect immune defenses, the evolution of aging, and the evolutionary ecology of offspring quality. Here, we develop a framework to investigate the evolutionary consequences of physiological dynamics by developing theory linking reproductive cell dynamics and components of fitness associated with costly resource allocation decisions to broader life history consequences. We scale these reproductive cell allocation decisions to population‐level survival and fecundity using a life history approach and explore the effects of investment in reproduction or tissue‐specific repair (somatic or reproductive) on the force of selection, reproductive effort, and resource allocation decisions. At the cellular level, we show that investment in protecting reproductive cells increases fitness when reproductive cell maturation rate is high or reproductive cell death is high. At the population level, life history fitness measures show that cellular protection increases reproductive value by differential investment in somatic or reproductive cells and the optimal allocation of resources to reproduction is moulded by this level of investment. Our model provides a framework to understand the evolutionary consequences of physiological processes underlying trade‐offs and highlights the insights to be gained from considering fitness at multiple levels, from cell dynamics through to population growth.     

Phenotypic constraints and community structure: Linking trade‐offs within and among species

Trade‐offs are central to many topics in biology, from the evolution of life histories to ecological mechanisms of species coexistence. Trade‐offs observed among species may reflect pervasive constraints on phenotypes that are achievable given biophysical and resource limitations. If so, then among‐species trade‐offs should be consistent with trade‐offs within species. Alternatively, trait variation among co‐occurring species may reflect historical contingencies during community assembly rather than within‐species constraints. Here, we test whether a key trade‐off between relative growth rate (RGR) and water‐use efficiency (WUE) among Sonoran Desert winter annual plants is apparent within four species representing different strategies in the system. We grew progeny of maternal families from multiple populations in a greenhouse common garden. One species, Pectocarya recurvata, displayed the expected RGR–WUE trade‐off among families within populations. For other species, although RGR and WUE often varied clinally among populations, among‐family variation within populations was lacking, implicating a role for past selection on these traits. Our results suggest that a combination of limited genetic variation in single traits and negative trait correlations could pose constraints on the evolution of a high‐RGR and high‐WUE phenotype within species, providing a microevolutionary explanation for phenotypes that influence community‐level patterns of abundance and coexistence.     

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.     

Multivariate selection and intersexual genetic constraints in a wild bird population

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra‐ and intersex additive genetic (co)variances and sex‐specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex‐specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex‐specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness that was uncorrelated between the sexes (cross‐sex genetic correlation = ?0.003, 95% CI = ?0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex‐specific effects, was estimated at 50% (95% CI = 13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

Healthier or bigger? Trade‐off mediating male dimorphism in the black scavenger fly Sepsis thoracica (Diptera: Sepsidae)

1. Life history trade‐offs emerge when limited resources are allocated to multiple functions of an organism. Under highly competitive conditions trade‐offs can result in alternative phenotypes that differ morphologically and physiologically. Such is the case in insect species that grow under high densities, where competition for resources but also the risk of disease contagion is high, prompting important adjustments in immune response and melanic cuticular pigmentation, with consequent sacrifices in other fitness‐related traits. 2. In the present study, the potential trade‐offs between total‐ and active phenoloxidase (PO), body size and body pigmentation in Sepsis thoracica black scavenger flies that show alternative male morphs differing in cuticular pigmentation, and body size were evaluated. 3. As expected, small/dark (obsidian) males showed higher total‐PO activity than larger/orange (amber) males. A negative relationship was found between total‐PO activity and body size in females and obsidian but not amber males, suggesting that growth and immunity are more costly for the former. In contrast, density did not affect PO activity, as predicted by the density‐dependent prophylaxis hypothesis, which had not been tested in dipterans before. However, rearing density did affect the body size negatively in females and amber but not obsidian males, showing that male morph is largely determined by condition‐dependent plasticity rather than genes. 4. This study provides good evidence that trade‐offs between different life‐history traits can result in alternative resource allocation strategies, even within one species. These strategies can produce strikingly different alternative phenotypes, evincing that there is not only one optimal solution to address fitness optimisation.     

QUANTITATIVE GENETIC DIVERGENCE AND STANDING GENETIC (CO)VARIANCE IN THERMAL REACTION NORMS ALONG LATITUDE

Although the potential to adapt to warmer climate is constrained by genetic trade‐offs, our understanding of how selection and mutation shape genetic (co)variances in thermal reaction norms is poor. Using 71 isofemale lines of the fly Sepsis punctum, originating from northern, central, and southern European climates, we tested for divergence in juvenile development rate across latitude at five experimental temperatures. To investigate effects of evolutionary history in different climates on standing genetic variation in reaction norms, we further compared genetic (co)variances between regions. Flies were reared on either high or low food resources to explore the role of energy acquisition in determining genetic trade‐offs between different temperatures. Although the latter had only weak effects on the strength and sign of genetic correlations, genetic architecture differed significantly between climatic regions, implying that evolution of reaction norms proceeds via different trajectories at high latitude versus low latitude in this system. Accordingly, regional genetic architecture was correlated to region‐specific differentiation. Moreover, hot development temperatures were associated with low genetic variance and stronger genetic correlations compared to cooler temperatures. We discuss the evolutionary potential of thermal reaction norms in light of their underlying genetic architectures, evolutionary histories, and the materialization of trade‐offs in natural environments.     

Antagonistic pleiotropy in species with separate sexes,and the maintenance of genetic variation in life‐history traits and fitness

Antagonistic pleiotropy (AP)—where alleles of a gene increase some components of fitness at a cost to others—can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex‐specific phenotypic selection estimates—many of which are based on single fitness components.