Adult dietary protein has age- and context-dependent effects on male post-copulatory performance.

The highly conserved effect of dietary protein restriction on lifespan and ageing is observed in both sexes and across a vast range of taxa. This extension of lifespan is frequently accompanied by a reduction in female fecundity, and it has been hypothesized that individuals may reallocate resources away from reproduction and into somatic maintenance. However, effects of dietary protein restriction on male reproduction are less consistent, suggesting that these effects may depend on other environmental parameters. Using the neriid fly, Telostylinus angusticollis, we examined age-specific effects of adult dietary protein restriction on male post-copulatory reproductive performance (fecundity and offspring viability). To explore the context dependence of these effects, we simultaneously manipulated male larval diet and adult mating history. We found that protein-restricted males sired less viable offspring at young ages, but offspring viability increased with paternal age and eventually exceeded that of fully fed males. The number of eggs laid by females was not affected by male dietary protein, whereas egg hatching success was subject to a complex interaction of male adult diet, age, larval diet and mating history. These findings suggest that effects of protein restriction on male reproduction are highly context dependent and cannot be explained by a simple reallocation of resources from reproduction to somatic maintenance. Rather, these effects appear to involve changes in the scheduling of male reproductive investment with age.

Phenotypes optimized for early-life reproduction exhibit faster somatic deterioration with age, revealing a latent cost of high condition.

High condition enables individuals to express a phenotype with greater reproductive potential. However, life-history theory predicts that reproduction will trade off with somatic maintenance and viability, and several studies have reported faster age-related decline in performance in high-condition individuals, suggesting that high condition in early life is associated with accelerated somatic deterioration. This trade-off may be especially pronounced in males, which often express condition-dependent secondary sexual traits that can impose viability costs during development and through damage-inflicting adult sexual behaviours. To test this prediction, we reared larvae of the neriid fly Telostylinus angusticollis on diets of varying nutrient content and quantified somatic deterioration in solitary males, males housed in all-male or mixed-sex groups and immobilized males subjected to mechanical stress. We found that males reared on a nutrient-rich larval diet (high-condition males) suffered a higher rate of somatic deterioration with age, particularly when housed in groups. Perhaps as a result of accelerated somatic deterioration, high-condition males did not outlive low-condition males. In addition, high-condition males housed in all-male groups experienced a greater reduction in escape response with age than males housed in mixed-sex groups, suggesting that male-male combat promotes somatic deterioration. However, even when immobilized, high-condition males were still found to be more susceptible to somatic damage than low-condition males. Our findings suggest that a high-condition male phenotype is more prone to somatic damage, both as a result of associated behaviours such as combat, and because of the inherent fragility of the high-condition body.

Condition dependence of male and female genital structures in the seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae).

Theory predicts that costly secondary sexual traits will evolve heightened condition dependence, and many studies have reported strong condition dependence of signal and weapon traits in a variety of species. However, although genital structures often play key roles in intersexual interactions and appear to be subject to sexual or sexually antagonistic selection, few studies have examined the condition dependence of genital structures, especially in both sexes simultaneously. We investigated the responses of male and female genital structures to manipulation of larval diet quality (new versus once-used mung beans) in the bruchid seed beetle Callosobruchus maculatus. We quantified effects on mean relative size and static allometry of the male aedeagus, aedeagal spines, flap and paramere and the female reproductive tract and bursal spines. None of the male traits showed a significant effect of diet quality. In females, we found that longer bursal spines (relative to body size) were expressed on low-quality diet. Although the function of bursal spines is poorly understood, we suggest that greater bursal spine length in low-condition females may represent a sexually antagonistic adaptation. Overall, we found no evidence that genital traits in C. maculatus are expressed to a greater extent when nutrients are more abundant. This suggests that, even though some genital traits appear to function as secondary sexual traits, genital traits do not exhibit heightened condition dependence in this species. We discuss possible reasons for this finding.

The evolution of genomic imprinting: theories, predictions and empirical tests.

The epigenetic phenomenon of genomic imprinting has motivated the development of numerous theories for its evolutionary origins and genomic distribution. In this review, we examine the three theories that have best withstood theoretical and empirical scrutiny. These are: Haig and colleagues' kinship theory; Day and Bonduriansky's sexual antagonism theory; and Wolf and Hager's maternal-offspring coadaptation theory. These theories have fundamentally different perspectives on the adaptive significance of imprinting. The kinship theory views imprinting as a mechanism to change gene dosage, with imprinting evolving because of the differential effect that gene dosage has on the fitness of matrilineal and patrilineal relatives. The sexual antagonism and maternal-offspring coadaptation theories view genomic imprinting as a mechanism to modify the resemblance of an individual to its two parents, with imprinting evolving to increase the probability of expressing the fitter of the two alleles at a locus. In an effort to stimulate further empirical work on the topic, we carefully detail the logic and assumptions of all three theories, clarify the specific predictions of each and suggest tests to discriminate between these alternative theories for why particular genes are imprinted.

Nongenetic inheritance and the evolution of costly female preference.

In species where males provide neither direct benefits nor paternal care, it is typically assumed that female preferences are maintained by indirect selection reflecting genetic benefits to offspring of preferred males. However, it remains unclear whether populations harbour sufficient genetic variation in fitness to support costly female preferences - a problem called the 'lek paradox'. Here, we ask whether indirect selection on female preferences can be maintained by nongenetic inheritance. We construct a general model that can be used to represent either genetic or nongenetic inheritance, depending on the choice of parameter values. Interestingly, we find that costly preference is most likely to evolve and persist when fitness depends on an environmentally induced factor that can be transmitted over a single generation only, such as an environment-dependent paternal effect. Costly preference can also be supported when fitness depends on a highly mutable factor that can persist over multiple generations, such as an epigenetic mark, but the necessary conditions are more restrictive. Our findings show that nongenetic inheritance provides a plausible hypothesis for the maintenance of costly female preferences in species where males provide no direct benefits to females. Nongenetic paternal inheritance of fitness can occur in species lacking conventional forms of paternal care. Indeed, transmission of paternal condition via sperm-borne nongenetic factors may be more likely to evolve than conventional forms of paternal investment because sperm-borne effects are protected from cuckoldry. Our results furnish a novel example of an interaction between genetic and nongenetic inheritance that can lead to otherwise unexpected evolutionary outcomes.

The relative importance of genetic and nongenetic inheritance in relation to trait plasticity in Callosobruchus maculatus.

A trait's response to natural selection will reflect the nature of the inheritance mechanisms that mediate the transmission of variation across generations. The relative importance of genetic and nongenetic mechanisms of inheritance is predicted to be related to the degree of trait plasticity, with nongenetic inheritance playing a greater role in the cross-generational transmission of more plastic traits. However, this prediction has never been tested. We investigated the influence of genetic effects and nongenetic parental effects in two morphological traits differing in degree of plasticity by manipulating larval diet quality within a cross-generational split-brood experiment using the seed beetle Callososbuchus maculatus. In line with predictions, we found that the more plastic trait (elytron length) is strongly influenced by both maternal and paternal effects whereas genetic variance is undetectable. In contrast, the less plastic trait (first abdominal sternite length) is not influenced by parental effects but exhibits abundant genetic variance. Our findings support the hypothesis that environment-dependent parental effects may play a particularly important role in highly plastic traits and thereby affect the evolutionary response of such traits.

The dissimilar costs of love and war: age-specific mortality as a function of the operational sex ratio.

Lifespan and ageing are strongly affected by many environmental factors, but the effects of social environment on these life-history traits are not well understood. We examined effects of social interaction on age-specific mortality rate in the sexually dimorphic neriid fly Telostylinus angusticollis. We found that although interaction with other individuals reduced longevity of both sexes, the costs associated with variation in operational sex ratio were sex specific: males' early-life mortality rate increased, and lifespan decreased, with increasing male bias in the sex ratio, whereas surprisingly, the presence of males had no effect on early-life mortality or lifespan of females. Intriguingly, early-life (immediate) mortality costs did not covary with late-life (latent) costs. Rather, both sexes aged most rapidly in a social environment dominated by the opposite sex. Our findings suggest that distinct reproductive activities, such as mating and fighting, impose different age-specific patterns of mortality, and that such costs are strongly sex specific.

Condition dependence of developmental stability in the sexually dimorphic fly Telostylinus angusticollis (Diptera: Neriidae).

Developmental stability is widely regarded as a condition-dependent trait, but its relation to genotype and environment, and extent of developmental integration, remain contentious. In Telostylinus angusticollis, the dorsocentral bristles exhibit striking variation in developmental stability, manifested as fluctuating asymmetry (FA) in bristle position ('positional FA') and failure to develop some bristles ('bristle loss'), in natural and laboratory populations. To determine whether this variation reflects condition, I tested for effects of genotype and environment (larval diet quality), and examined covariation with condition-dependent traits. Positional FA was not affected by genotype or environment. However, positional FA covaried negatively with secondary sexual trait expression in males, and with sexual dimorphism in body shape, but covaried positively with body size in females. Bristle loss reflected both genotype and larval diet. Flies reared on poor-quality diet exhibited a similar rate of bristle loss as wild flies. Both positional FA and bristle loss were greater in males. These results suggest that the relation between developmental stability and condition is complex and sex dependent.

Dietary protein and lifespan across the metamorphic boundary: protein-restricted larvae develop into short-lived adults.

Restriction of nutrients in the adult diet extends lifespan across a diverse range of species, but less is known about the long-term effects of developmental dietary restriction. In particular, it is not known whether adult lifespan is influenced by developmental caloric restriction or macronutrient balance. We used the nutritional geometry approach to independently manipulate protein and carbohydrate contents of the larval diet in the neriid fly, Telostylinus angusticollis, and measured adult lifespan. We found that adult male and female lifespan was shortest when larvae were fed a protein restricted diet. Thus, protein restriction in the larval diet has the opposite effect of protein restriction in the adult diet (which prolongs life in this species and across a wide range of taxa). Adult lifespan was unaffected by larval dietary carbohydrate. These patterns persisted after controlling for larval diet effects on adult body size. We propose that larval and adult protein sources are used for distinct metabolic tasks: during development, dietary protein is used to build a durable soma that enhances adult lifespan, although excessive protein consumption partially reverses this effect.

Rethinking heredity, again.

The refutation of 'soft' inheritance and establishment of Mendelian genetics as the exclusive model of heredity is widely portrayed as an iconic success story of scientific progress. Yet, we are witnessing a re-emergence of debate on the role of soft inheritance in heredity and evolution. I argue that this reversal reflects not only the weight of new evidence but also an important conceptual change. I show that the concept of soft inheritance rejected by 20th-century genetics differs fundamentally from the current concept of 'nongenetic inheritance'. Moreover, whereas it has long been assumed that heredity is mediated by a single, universal mechanism, a pluralistic model of heredity is now emerging, based on a recognition of multiple, parallel mechanisms of inheritance.

Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae).

It is widely recognized that maternal phenotype can have important effects on offspring, but paternal phenotype is generally assumed to have no influence in animals lacking paternal care. Nonetheless, selection may favour the transfer of environmentally acquired condition to offspring from both parents. Using a split-brood, cross-generational laboratory design, we manipulated a key environmental determinant of condition - larval diet quality - of parents and their offspring in the fly Telostylinus angusticollis, in which there is no evidence of paternal provisioning. Parental diet did not affect offspring survival, but high-condition mothers produced larger eggs, and their offspring developed more rapidly when on a poor larval diet. Maternal condition had no effect on adult body size of offspring. By contrast, large, high-condition fathers produced larger offspring, and follow-up assays showed that this paternal effect can be sufficient to increase mating success of male offspring and fecundity of female offspring. Our findings suggest that both mothers and fathers transfer their condition to offspring, but with effects on different offspring traits. Moreover, our results suggest that paternal effects can be important even in species lacking conventional forms of paternal care. In such species, the transfer of paternal condition to offspring could contribute to indirect selection on female mate preferences.

Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata).

Little is known about the importance of trade-offs between ageing and other life history traits, or the effects of ageing on sexual selection, particularly in wild populations suffering high extrinsic mortality rates. Life history theory suggests that trade-offs between reproduction and somatic maintenance may constrain individuals with higher initial reproductive rates to deteriorate more rapidly, resulting in reduced sexual selection strength. However, this trade-off may be masked by increased condition dependence of reproductive effort in older individuals. We tested for this trade-off in males in a wild population of antler flies (Protopiophila litigata). High mating rate was associated with reduced longevity, as a result of increased short-term mortality risk or accelerated ageing in traits affecting viability. In contrast, large body size was associated with accelerated ageing in traits affecting mating success, resulting in reduced sexual selection for large body size. Thus, ageing can affect sexual selection and evolution in wild populations.

The evolution of male mate choice in insects: a synthesis of ideas and evidence.

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.