Selection on female reproductive schedules in the marula fly, Ceratitis cosyra (Diptera: Tephritidae) affects dietary optima for female reproductive traits but not lifespan.

Introduction: A changing environment can select on life-history traits and trade-offs in a myriad of ways. For example, global warming may shift phenology and thus the availability of host-plants. This may alter selection on survival and fertility schedules in herbivorous insects. If selection on life-histories changes, this may in turn select for altered nutrient intake, because the blend of nutrients organisms consume helps determine the expression of life-history traits. However, we lack empirical work testing whether shifts in the timing of oviposition alter nutrient intake and life-history strategies. Methods: We tested in the marula fruit fly, Ceratitis cosyra, how upward-selection on the age of female oviposition, in comparison with laboratory adapted control flies, affects the sex-specific relationship between protein and carbohydrate intake and life-history traits including lifespan, female lifetime egg production and daily egg production. We then determined the macronutrient ratio consumed when flies from each selection line and sex were allowed to self-regulate their intake. Results: Lifespan, lifetime egg production and daily egg production were optimised at similar protein to carbohydrate (P:C) ratios in flies from both selection lines. Likewise, females and males of both lines actively defended similar nutrient intake ratios (control =1:3.6 P:C; upward-selected = 1:3.2 P:C). Discussion: Our results are comparable to those in non-selected C. cosyra, where the optima for each trait and the self-selected protein to carbohydrate ratio observed were nearly identical. The nutrient blend that needs to be ingested for optimal expression of a given trait appeared to be well conserved across laboratory adapted and experimentally selected populations. These results suggest that in C. cosyra, nutritional requirements do not respond to a temporal change in oviposition substrate availability.

A sex skew in life-history research: the problem of missing males.

Life-history strategies are diverse. While understanding this diversity is a fundamental aim of evolutionary biology and biodemography, life-history data for some traits-in particular, age-dependent reproductive investment-are biased towards females. While other authors have highlighted this sex skew, the general scale of this bias has not been quantified and its impact on our understanding of evolutionary ecology has not been discussed. This review summarizes why the sexes can evolve different life-history strategies. The scale of the sex skew is then discussed and its magnitude compared between taxonomic groups, laboratory and field studies, and through time. We discuss the consequences of this sex skew for evolutionary and ecological research. In particular, this sex bias means that we cannot test some core evolutionary theory. Additionally, this skew could obscure or drive trends in data and hinder our ability to develop effective conservation strategies. We finally highlight some ways through which this skew could be addressed to help us better understand broad patterns in life-history strategies.

Oxidative Damage Is Influenced by Diet But Unaffected by Selection for Early Age of Oviposition in the Marula Fly, Ceratitis cosyra (Diptera: Tephritidae).

The expression of life-history traits, such as lifespan or reproductive effort, is tightly correlated with the amount and blend of macronutrients that individuals consume. In a range of herbivorous insects, consuming high protein to carbohydrate ratios (P:C) decreases lifespan but increases female fecundity. In other words, females face a resource-based trade-off between lifespan and fecundity. Redox metabolism may help mediate this trade-off, if oxidative damage is elevated by reproductive investment and if this damage, in turn, reduces lifespan. Here, we test how diets varying in P:C ratio affect oxidative damage and antioxidant protection in female and male of the marula fly, Ceratitis cosyra (Diptera: Tephritidae). We use replicated lines that have been subjected to experimental evolution and differ in their lifespan and reproductive scheduling. We predicted that high fecundity would be associated with high oxidative damage and reduced antioxidant defences, while longer lived flies would show reduced damage and elevated antioxidant defences. However, higher levels of oxidative damage were observed in long-lived control lines than selection lines, but only when fed the diet promoting lifespan. Flies fed diets promoting female fecundity (1:4 and 1:2 P:C) suffered greater oxidative damage to lipids than flies fed the best diet (0:1 P:C) for lifespan. Total antioxidant capacity was not affected by the selection regime or nutrition. Our results reiterate the importance of nutrition in affecting life-history traits, but suggest that in C. cosyra, reactive oxygen species play a minimal role in mediating dietary trade-offs between lifespan and reproduction.

Mapping sex differences in the effects of protein and carbohydrates on lifespan and reproduction in Drosophila melanogaster: is measuring nutrient intake essential?

Understanding how diet affects reproduction and survival is a central aim in evolutionary biology. Although this relationship is likely to differ between the sexes, we lack data relating diet to male reproductive traits. One exception to this general pattern is Drosophila melanogaster, where male dietary intake was quantified using the CApillary FEeder (CAFE) method. However, CAFE feeding reduces D. melanogaster survival and reproduction, so may distort diet-fitness outcomes. Here, we use the Geometric Framework of Nutrition to create nutrient landscapes that map sex-specific relationships between protein, carbohydrate, lifespan and reproduction in D. melanogaster. Rather than creating landscapes with consumption data, we map traits onto the nutrient composition of forty agar-based diets, generating broad coverage of nutrient space. We find that male and female lifespan was maximised on low protein, high carbohydrate blends (~ 1P:15.9C). This nutrient ratio also maximised male reproductive rates, but females required more protein to maximise daily fecundity (1P:1.22C). These results are consistent with CAFE assay outcomes. However, the approach employed here improved female fitness relative to CAFE assays, while effects of agar versus CAFE feeding on male fitness traits depended on the nutrient composition of experimental diets. We suggest that informative nutrient landscapes can be made without measuring individual nutrient intake and that in many cases, this may be preferable to using the CAFE approach. The most appropriate method will depend on the question and species being studied, but the approach adopted here has the advantage of creating nutritional landscapes when dietary intake is hard to quantify.

Complex relationship between amino acids, fitness and food intake in Bombus terrestris.

The ratio of amino acids to carbohydrates (AA:C) that bumble bees consume has been reported to affect their survival. However, it is unknown how dietary AA:C ratio affects other bumble bee fitness traits (e.g., fecundity, condition) and possible trade-offs between them. Moreover, while individual AAs affect phenotype in many species, the effects of AA blend on bumble bee fitness and food intake are unclear. We test how the AA:C ratio that bumble bees (Bombus terrestris) consume affects their condition (abdomen lipid and dry mass), survival following food removal, and ovarian activation. We then compare ovarian activation and food intake in bees fed identical AA:C ratios, but where the blend of AAs in diets differ, i.e., diets contained the same 10 AAs in an equimolar ratio or in the same ratio as in bee collected pollen. We found that AA:C ratio did not significantly affect survival following food removal or ovarian activation; however, high AA intake increased body mass, which is positively correlated with multiple fitness traits in bumble bees. AA blend (i.e., equimolar versus pollen) did not significantly affect overall ovarian activation or consumption of each experimental diet. However, there was an interaction between AA mix and dietary AA:C ratio affecting survival during the feeding experiment, and signs that there may have been weak, interactive effects of AA mix and AA:C ratio on food consumption. These results suggest that the effect of total AA intake on bumble bee phenotype may depend on the blend of individual AAs in experimental diets. We suggest that research exploring how AA blend affects bumble bee performance and dietary intake is warranted, and highlight that comparing research on bee nutrition is complicated by even subtle variation in experimental diet composition.

Herbaceous perennial plants with short generation time have stronger responses to climate anomalies than those with longer generation time.

There is an urgent need to synthesize the state of our knowledge on plant responses to climate. The availability of open-access data provide opportunities to examine quantitative generalizations regarding which biomes and species are most responsive to climate drivers. Here, we synthesize time series of structured population models from 162 populations of 62 plants, mostly herbaceous species from temperate biomes, to link plant population growth rates (λ) to precipitation and temperature drivers. We expect: (1) more pronounced demographic responses to precipitation than temperature, especially in arid biomes; and (2) a higher climate sensitivity in short-lived rather than long-lived species. We find that precipitation anomalies have a nearly three-fold larger effect on λ than temperature. Species with shorter generation time have much stronger absolute responses to climate anomalies. We conclude that key species-level traits can predict plant population responses to climate, and discuss the relevance of this generalization for conservation planning.

Dose-dependent effects of antibiotic intake on Bombus Terrestris (Linnaeus, 1758) dietary intake, survival and parasite infection prevalence.

Diseases may contribute to the widespread declines seen in many bee species. The gut bacteria of bees may serve as one defence against disease, by preventing pathogen colonisation. However, exposure to antibiotics on forage or in the hive may disrupt bee gut bacteria and remove this protective effect. A number of studies show that high antibiotic doses reduce bee health but the effects of field-realistic antibiotic doses remain unclear. Here, we test how Bombus terrestris (Linnaeus, 1758) is affected by multiple field-realistic concentrations of the antibiotic oxytetracycline, which is sometimes used to protect flowering crops from bacterial infections. We measured survival, feeding behaviour and the likelihood of developing infection with the gut parasitic trypanosome Crithidia bombi Lipa & Triggiani, 1988 following oral inoculation with a range of antibiotic doses. Rising antibiotic concentrations were associated with reduced survival and food consumption, and an increased likelihood of becoming infected with C. bombi. These effects were seen at antibiotic concentrations that are applied to crops and so may be encountered by foraging bees in the field. These results support the hypothesis that field-realistic antibiotic doses have lethal and sub-lethal effects on B. terrestris and highlight the importance of improving our understanding of how field-realistic antibiotic doses affect pollinators.

Offspring sex ratios are stable across the life course in Drosophila simulans.

Within populations, adult sex ratios influence population growth and extinction risk, mating behaviours and parental care. Sex ratio adjustment can also have pronounced effects on individual fitness. Accordingly, it is important that we understand how often, and why, offspring sex ratios deviate from parity. In Drosophila melanogaster, females appear to improve their fitness by producing fewer sons when paired with older males. However, facultative sex ratio adjustment in D. melanogaster is controversial, and our understanding of how sex ratio skew affects fitness is hampered by pronounced sexual conflict in this species. Additionally, it is unclear whether maternal age or quality interacts with paternal age to influence offspring sex ratios. Here, we test whether offspring sex ratios vary as a function of maternal quality, and maternal and paternal age in Drosophila simulans, a sister species of D. melanogaster that lacks overt sexual conflict. We find that offspring sex ratios are slightly male-biased overall, but constant across the female life course, and independent of female quality, or paternal age. To really understand if, how and when females skew offspring sex ratios, we need studies linking offspring sex ratios to paternal and maternal phenotypes that are predicted to shift optimal investment in sons and daughters.

Selection on age of female reproduction in the marula fruit fly, Ceratitis cosyra (Walker) (Diptera: Tephritidae), decreases total antioxidant capacity and lipid peroxidation.

The oxidative damage caused to cells by Reactive Oxygen Species (ROS) is one of several factors implicated in causing ageing. Oxidative damage may also be a proximate cost of reproductive effort that mediates the trade-off often observed between reproduction and survival. However, how the balance between oxidative damage and antioxidant protection affects life-history strategies is not fully understood. To improve our understanding, we selected on female reproductive age in the marula fruit fly, Ceratitis cosyra, and quantified the impact of selection on female and male mortality risk, female fecundity, male sperm transfer, calling and mating. Against expectations, upward-selected lines lived shorter lives and experienced some reductions in reproductive performance. Selection affected oxidative damage to lipids and total antioxidant protection, but not in the direction predicted; longer lives were associated with elevated oxidative damage, arguing against the idea that accumulated oxidative damage reduces lifespan. Greater reproductive effort was also associated with elevated oxidative damage, suggesting that oxidative damage may be a cost of reproduction, although one that did not affect survival. Our results add to a body of data showing that the relationship between lifespan, reproduction and oxidative damage is more complex than predicted by existing theories.

Exploring the role of host specialisation and oxidative stress in interspecific lifespan variation in subtropical tephritid flies.

In herbivorous insects, the degree of host specialisation may be one ecological factor that shapes lifespan. Because host specialists can only exploit a limited number of plants, their lifecycle should be synchronised with host phenology to allow reproduction when suitable hosts are available. For species not undergoing diapause or dormancy, one strategy to achieve this could be evolving long lifespans. From a physiological perspective, oxidative stress could explain how lifespan is related to degree of host specialisation. Oxidative stress caused by Reactive Oxygen Species (ROS) might help underpin ageing (the Free Radical Theory of Aging (FRTA)) and mediate differences in lifespan. Here, we investigated how lifespan is shaped by the degree of host specialisation, phylogeny, oxidative damage accumulation and antioxidant protection in eight species of true fruit flies (Diptera: Tephritidae). We found that lifespan was not constrained by species relatedness or oxidative damage (arguing against the FRTA); nevertheless, average lifespan was positively associated with antioxidant protection. There was no lifespan difference between generalist and specialist species, but most of the tephritids studied had long lifespans in comparison with other dipterans. Long lifespan may be a trait under selection in fruit-feeding insects that do not use diapause.

Complex interactions between sperm viability and female fertility.

Sperm viability is a major male fitness component, with higher sperm viability associated with enhanced sperm competitiveness. While many studies have focussed on sperm viability from the male fitness standpoint, its impact on female fitness is less clear. Here we used a panel of 32 isogenic Drosophila simulans lines to test for genetic variation in sperm viability (percentage of viable cells). We then tested whether sperm viability affected female fitness by mating females to males from low or high sperm viability genotypes. We found significant variation in sperm viability among genotypes, and consistent with this, sperm viability was highly repeatable within genotypes. Additionally, females mated to high sperm viability males laid more eggs in the first seven hours after mating, and produced more offspring in total. However, the early increase in oviposition did not result in more offspring in the 8 hours following mating, suggesting that mating with high sperm-viability genotypes leads to egg wastage for females shortly after copulation. Although mating with high sperm-viability males resulted in higher female fitness in the long term, high quality ejaculates would result in a short-term female fitness penalty, or at least lower realised fitness, potentially generating sexual conflict over optimal sperm viability.

Sexual conflict.

Evolutionary conflict arises from differences in the fitness interests of replicating entities and has its roots in relatedness asymmetries. Every replicator is related to itself by 100%, but in most cases is less related to other replicators, which generates selfishness and conflicts of interest. Since this basic condition is the norm at many levels of biological organization, conflict is rife in biological systems. Sexual conflict, on which we focus here, is the evolutionary conflict that occurs between males and females because of their divergent fitness interests. Sexual conflict occurs despite sexual reproduction requiring some level of cooperation between males and females because the fitness interests of the sexes are nevertheless never perfectly aligned. In other words, males and females may agree on where they are going, but not necessarily on how to get there. Sexual conflict is a vast topic with relevance to many areas of biology and so here we restrict our focus to matters we think are of broadest interest.

Wolbachia infection can bias estimates of intralocus sexual conflict.

Males and females share most of their genome and develop many of the same traits. However, each sex frequently has different optimal values for these shared traits, creating intralocus sexual conflict. This conflict has been observed in wild and laboratory populations of insects and affects important evolutionary processes such as sexual selection, the maintenance of genetic variation, and possibly even speciation. Given the broad impacts of intralocus conflict, accurately detecting and measuring it is important. A common way to detect intralocus sexual conflict is to calculate the intersexual genetic correlation for fitness, with negative values suggesting conflict. Here, we highlight a potential confounder of this measure-cytoplasmic incompatibility caused by the intracellular parasite Wolbachia. Infection with Wolbachia can generate negative intersexual genetic correlations for fitness in insects, suggestive of intralocus sexual conflict. This is because cytoplasmic incompatibility reduces the fitness of uninfected females mated to infected males, while uninfected males will not suffer reductions in fitness if they mate with infected females and may even be fitter than infected males. This can lead to strong negative intersexual genetic correlations for fitness, mimicking intralocus conflict. We illustrate this issue using simulations and then present Drosophila simulans data that show how reproductive incompatibilities caused by Wolbachia infection can generate signals of intralocus sexual conflict. Given that Wolbachia infection in insect populations is pervasive, but populations usually contain both infected and uninfected individuals providing scope for cytoplasmic incompatibility, this is an important consideration for sexual conflict research but one which, to date, has been largely underappreciated.

Penis evolution across species: divergence and diversity.

The penis is an incredibly diverse and rapidly evolving structure, such that even in closely related species that otherwise differ very little in their morphology, penis form can be highly differentiated. Penises are also much more complex than their fundamental function - sperm transfer - would seem to require. The rapid divergent evolution of male structures is typically the signature of traits under sexual selection and the current evidence suggests the penis is no different in this regard. Despite the general agreement that sexual selection is the main driver of penis evolution, many questions about penis evolution remain unresolved. Furthermore, the penis might be an ideal characteristic on which to focus in the drive to link phenotype with genotype.

Intralocus sexual conflict can resolve the male-female health-survival paradox.

At any given age, men are more likely to die than women, but women have poorer health at older ages. This is referred to as the "male-female, health-survival paradox", which is not fully understood. Here, we provide a general solution to the paradox that relies on intralocus sexual conflict, where alleles segregating in the population have late-acting positive effects on male fitness, but negative effects on female health. Using an evolutionary modelling framework, we show that male-benefit, female-detriment alleles can spread if they are expressed after female reproduction stops. We provide support for our conflict based solution using experimental Drosophila data. Our results show that selecting for increased late-life male reproductive effort can increase male fitness but have a detrimental effect on female fitness. Furthermore, we show that late-life male fertility is negatively genetically correlated with female health. Our study suggests that intralocus sexual conflict could resolve the health-survival paradox.

The Geometry of Nutrient Space-Based Life-History Trade-Offs: Sex-Specific Effects of Macronutrient Intake on the Trade-Off between Encapsulation Ability and Reproductive Effort in Decorated Crickets.

Life-history theory assumes that traits compete for limited resources, resulting in trade-offs. The most commonly manipulated resource in empirical studies is the quantity or quality of diet. Recent studies using the geometric framework for nutrition, however, suggest that trade-offs are often regulated by the intake of specific nutrients, but a formal approach to identify and quantify the strength of such trade-offs is lacking. We posit that trade-offs occur whenever life-history traits are maximized in different regions of nutrient space, as evidenced by nonoverlapping 95% confidence regions of the global maximum for each trait and large angles (θ) between linear nutritional vectors and Euclidean distances (d) between global maxima. We then examined the effects of protein and carbohydrate intake on the trade-off between reproduction and aspects of immune function in male and female Gryllodes sigillatus. Female encapsulation ability and egg production increased with the intake of both nutrients, whereas male encapsulation ability increased with protein intake but calling effort increased with carbohydrate intake. The trade-offs between traits was therefore larger in males than in females, as demonstrated by significant negative correlations between the traits in males, nonoverlapping 95% confidence regions, and larger estimates of θ and d. Under dietary choice, the sexes had similar regulated intakes, but neither optimally regulated nutrient intake for maximal trait expression. We highlight the fact that greater consideration of specific nutrient intake is needed when examining nutrient space-based trade-offs.

Effects of macronutrient intake on the lifespan and fecundity of the marula fruit fly, Ceratitis cosyra (Tephritidae): Extreme lifespan in a host specialist.

In insects, lifespan and reproduction are strongly associated with nutrition. The ratio and amount of nutrients individuals consume affect their life expectancy and reproductive investment. The geometric framework (GF) enables us to explore how animals regulate their intake of multiple nutrients simultaneously and determine how these nutrients interact to affect life-history traits of interest. Studies using the GF on host-generalist tephritid flies have highlighted trade-offs between longevity and reproductive effort in females, mediated by the protein-to-carbohydrate (P:C) ratio that individuals consume. Here, we tested how P and C intake affect lifespan (LS) in both sexes, and female lifetime (LEP), and daily (DEP) egg production, in Ceratitis cosyra, a host-specialist tephritid fly. We then determined the P:C ratio that C. cosyra defends when offered a choice of foods. Female LS was optimized at a 0:1 P:C ratio, whereas to maximize their fecundity, females needed to consume a higher P:C ratio (LEP = 1:6 P:C; DEP = 1:2.5 P:C). In males, LS was also optimized at a low P:C ratio of 1:10. However, when given the opportunity to regulate their intake, both sexes actively defended a 1:3 P:C ratio, which is closer to the target for DEP than either LS or LEP. Our results show that female C. cosyra experienced a moderate trade-off between LS and fecundity. Moreover, the diets that maximized expression of LEP and DEP were of lower P:C ratio than those required for optimal expression of these traits in host-generalist tephritids or other generalist insects.

Little evidence for intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction in the black field cricket Teleogryllus commodus.

There is often large divergence in the effects of key nutrients on life span (LS) and reproduction in the sexes, yet nutrient intake is regulated in the same way in males and females given dietary choice. This suggests that the sexes are constrained from feeding to their sex-specific nutritional optima for these traits. Here, we examine the potential for intralocus sexual conflict (IASC) over optimal protein and carbohydrate intake for LS and reproduction to constrain the evolution of sex-specific nutrient regulation in the field cricket, Teleogryllus commodus. We show clear sex differences in the effects of protein and carbohydrate intake on LS and reproduction and strong positive genetic correlations between the sexes for the regulated intake of these nutrients. However, the between-sex additive genetic covariance matrix had very little effect on the predicted evolutionary response of nutrient regulation in the sexes. Thus, IASC appears unlikely to act as an evolutionary constraint on sex-specific nutrient regulation in T. commodus. This finding is supported by clear sexual dimorphism in the regulated intake of these nutrients under dietary choice. However, nutrient regulation did not coincide with the nutritional optima for LS or reproduction in either sex, suggesting that IASC is not completely resolved in T. commodus.