A temperature shock can lead to trans‐generational immune priming in the Red Flour Beetle,Tribolium castaneum

Trans‐generational immune priming (TGIP) describes the transfer of immune stimulation to the next generation. As stress and immunity are closely connected, we here address the question whether trans‐generational effects on immunity and resistance can also be elicited by a nonpathogen stress treatment of parents. General stressors have been shown to induce immunity to pathogens within individuals. However, to our knowledge, it is as of yet unknown whether stress can also induce trans‐generational effects on immunity and resistance. We exposed a parental generation (mothers, fathers, or both parents) of the red flour beetle Tribolium castaneum, a species where TGIP has been previously been demonstrated, to either a brief heat or cold shock and examined offspring survival after bacterial infection with the entomopathogen Bacillus thuringiensis. We also studied phenoloxidase activity, a key enzyme of the insect innate immune system that has previously been demonstrated to be up‐regulated upon TGIP. We quantified parental fecundity and offspring developmental time to evaluate whether trans‐generational priming might have costs. Offspring resistance was found to be significantly increased when both parents received a cold shock. Offspring phenoloxidase activity was also higher when mothers or both parents were cold‐shocked. By contrast, parental heat shock reduced offspring phenoloxidase activity. Moreover, parental cold or heat shock delayed offspring development. In sum, we conclude that trans‐generational priming for resistance could not only be elicited by pathogens or pathogen‐derived components, but also by more general cues that are indicative of a stressful environment. The interaction between stress responses and the immune system might play an important role also for trans‐generational effects.     

Trans‐generational maternal effect: temperature influences egg size of the offspring in Atlantic salmon Salmo salar

Effect of increased temperature during egg maturation on the mass of single eggs produced by the offspring was investigated experimentally in Atlantic salmon Salmo salar. Mass of eggs produced by next‐generation females was larger when their mothers experienced warmer water during the last two months of egg maturation, relative to those that experienced unheated river water. There was no similar trans‐generational paternal effect on offspring egg mass.     

Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation

The consequences of sexual interactions extend beyond the simple production of offspring. These interactions typically entail direct effects on female fitness, but may also impact the life histories of later generations. Evaluating the cross-generational effects of sexual interactions provides insights into the dynamics of sexual selection and conflict. Such studies can elucidate whether offspring fitness optima diverge across sexes upon heightened levels of sexual interaction among parents. Here, we found that, in Drosophila melanogaster, components of reproductive success in females, but not males, were contingent on the nature of sexual interactions experienced by their mothers. In particular, maternal sexual interactions with non-sires enhanced female fecundity in the following generation. This highlights the importance of non-sire influences of sexual interactions on the expression of offspring life histories.     

The within‐host dynamics of infection in trans‐generationally primed flour beetles

Many taxa exhibit plastic immune responses initiated after primary microbial exposure that provide increased protection against disease‐induced mortality and the fitness costs of infection. In several arthropod species, this protection can even be passed from parents to offspring through a phenomenon called trans‐generational immune priming. Here, we first demonstrate that trans‐generational priming is a repeatable phenomenon in flour beetles (Tribolium castaneum) primed and infected with Bacillus thuringiensis (Bt). We then quantify the within‐host dynamics of microbes and host physiological responses in infected offspring from primed and unprimed mothers by monitoring bacterial density and using mRNA‐seq to profile host gene expression, respectively, over the acute infection period. We find that priming increases inducible resistance against Bt around a critical temporal juncture where host septicaemic trajectories, and consequently survival, may be determined in unprimed individuals. Our results identify a highly differentially expressed biomarker of priming, containing an EIF4‐e domain, in uninfected individuals, as well as several other candidate genes. Moreover, the induction and decay dynamics of gene expression over time suggest a metabolic shift in primed individuals. The identified bacterial and gene expression dynamics are likely to influence patterns of bacterial fitness and disease transmission in natural populations.     

Trans‐generational immune priming is constrained by the maternal immune response in an insect

Immune‐challenged vertebrate and invertebrate females can transfer immunity to their offspring. This trans‐generational immune priming (TGIP) is beneficial for the offspring if the maternal infection risk persists across generations. However, because immunity is costly, fitness consequences of TGIP have been found in primed offspring. Furthermore, transferring immunity to offspring may be costly for immune‐challenged females who are also carrying the costs of their immune response. A negative relationship between levels of immunity between mothers and offspring might therefore be expected. Consistent with this hypothesis, we show that in the insect, Tenebrio molitor, the magnitude of antibacterial immune response of immune‐challenged females negatively correlates with levels of antibacterial activity of their eggs. This negative relationship was only present in small females that are inherently of lower quality. Furthermore, female body size did not affect immune responsiveness to the challenge, indicating that small females favoured their immunity at the expenses of that of their eggs.     

Indirect effects of phytochemicals on offspring performance of Queensland fruit fly,Bactrocera tryoni (Diptera: Tephritidae)

Phytochemical lures such as methyl eugenol (ME) and cue‐lure are used in the management of Bactrocera fruit flies for monitoring and control. These lures are not just attractants, but also trigger physiological changes in males that lead to enhanced mating success. Additionally, in the cue‐lure‐responsive Bactrocera tryoni, females mated with lure‐fed males exhibit changes in fecundity, remating receptivity and longevity. While the lures show current generation effects, no research has been carried out on possible multigenerational effects, although such effects have been hypothesized within a ‘sexy‐son’ sexual selection model. In this study, we test for indirect, cross‐generational effects of lure exposure in F1offspring of B. tryoni females mated with cue‐lure‐fed, zingerone‐fed and lure‐unfed (=control) males. The F1 attributes we recorded were immature development time, immature survival, adult survival and adult male lure foraging. No significant differences were found between treatments for any of the three life‐history measurements, except that the offspring sired by zingerone‐fed males had a longer egg development time than cue‐lure and control offspring. However, indirect exposure to lures significantly enhanced the lure‐foraging ability of F1 adult males. More offspring of cue‐lure‐fed males arrived at a lure source in both large flight cages and small laboratory cages over a 2‐h period than did control males. The offspring of zingerone‐fed males were generally intermediate between cue‐lure and control offspring. This study provides the first evidence of a next generation effect of fruit fly male lures. While the results of this study support a ‘sexy‐son’ sexual selection mechanism for the evolution of lure response in Bactrocera fruit flies, our discussion urges caution in interpreting our results in this way.     

The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket

Trans‐generational immune priming is the transmission of enhanced immunity to offspring following a parental immune challenge. Although within‐generation increased investment into immunity demonstrates clear costs on reproductive investment in a number of taxa, the potential for immune priming to impact on offspring reproductive investment has not been thoroughly investigated. We explored the reproductive costs of immune priming in a field cricket, Teleogryllus oceanicus. To assess the relative importance of maternal and paternal immune status, mothers and fathers were immune‐challenged with live bacteria or a control solution and assigned to one of four treatments in which one parent, neither or both parents were immune‐challenged. Families of offspring were reared to adulthood under a food‐restricted diet, and approximately 10 offspring in each family were assayed for two measures of immunocompetence. We additionally quantified offspring reproductive investment using sperm viability for males and ovary mass for females. We demonstrate that parental immune challenge has significant consequences for the immunocompetence and, in turn, reproductive investment of their male offspring. A complex interaction between maternal and paternal immune status increased the antibacterial immune response of male offspring. This increased immune response was associated with a reduction in son's sperm viability, implicating a trans‐generational resource trade‐off between investment into immunocompetence and reproduction. Our data also show that these costs are sexually dimorphic, as daughters did not demonstrate a similar increase in immunity, despite showing a reduction in ovary mass.     

An experimental test for body size‐dependent effects of male harassment and an elevated copulation rate on female lifetime fecundity and offspring performance

Many studies investigate the benefits of polyandry, but repeated interactions with males can lower female reproductive success. Interacting with males might even decrease offspring performance if it reduces a female's ability to transfer maternal resources. Male presence can be detrimental for females in two ways: by forcing females to mate at a higher rate and through costs associated with resisting male mating attempts. Teasing apart the relative costs of elevated mating rates from those of greater male harassment is critical to understand the evolution of mating strategies. Furthermore, it is important to test whether a male's phenotype, notably body size, has differential effects on female reproductive success versus the performance of offspring, and whether this is due to male body size affecting the costs of harassment or the actual mating rate. In the eastern mosquitofish Gambusia holbrooki, males vary greatly in body size and continually attempt to inseminate females. We experimentally manipulated male presence (i.e., harassment), male body size and whether males could copulate. Exposure to males had strong detrimental effects on female reproductive output, growth and immune response, independent of male size or whether males could copulate. In contrast, there was a little evidence of a cross‐generational effect of male harassment or mating rate on offspring performance. Our results suggest that females housed with males pay direct costs due to reduced condition and offspring production and that these costs are not a consequence of increased mating rates. Furthermore, exposure to males does not affect offspring reproductive traits.     

Brood conspicuousness and clutch viability in male‐caring assassin bugs (Rhinocoris tristis)

Abstract 1. Conspicuousness to mates can bring benefits to both males (increased mating success) and females (reduced search costs), but also brings costs (e.g. increased predation and parasitism). Assassin bugs, Rhinocoris tristis, lay egg clutches either on exposed stems or hidden under leaves. Males guard eggs against parasitoids. Guarding males are attractive to females who add subsequent clutches to the brood. This is an excellent opportunity to study the effects of conspicuousness on the fitness of males and females. 2. Using viable eggs in a multi‐clutch brood as a correlate of fitness, the present study examined whether laying eggs on stems affected (1) female fitness, through exposure to parasitism and cannibalism, and (2) male fitness, through attracting further females. 3. Stem broods were more parasitised. However, males on stems accumulated more mates and more eggs, a net benefit even accounting for parasitism. The eggs gained from being on a stem were cannibalised. By contrast, higher mortality on stems suggests that females should gain by ovipositing on leaves. To the extent that egg viability represents fitness, male and female interests may therefore differ. This suggests a potential for sexual conflict that may affect other species with male care. 4. Despite higher costs, females actually initiated more broods, and subsequently added bigger clutches to broods, on stems than under leaves. This suggests either that viable eggs do not reflect fitness, or that females laid in unfavourable locations. The key is now to address lifetime fitness, since unmeasured factors may affect offspring viability post‐hatching, and to investigate who controls the location of oviposition in R. tristis.     

Evaluating the existence and benefit of major histocompatibility complex‐based mate choice in an isolated owl population

How mate preferences evolve in the first place has been a major conundrum for sexual selection. Some hypotheses explaining this assume fitness benefit derived from subsequent generations. Major histocompatibility complex (MHC)‐based mate choice is a representative example of the mate choice that is associated with such trans‐generational mechanisms. To provide evidences for fitness benefit of MHC‐based mate choice, previous studies assessed the association between own MHC genotype and own fitness components. However, the association between MHC‐based mate choice in the parental generation and fitness components in the resultant offspring generation has only rarely been measured in wild populations. Focusing on the isolated population of the monogamous Ryukyu Scops Owl (Otus elegans interpositus) on Minami‐daito Island, Japan, we found evidence of MHC‐based mate choice. However, we found no evidence of MHC‐based mate choice increasing own reproductive success or offspring survival. This is a rare case study that directly examines the existence of the trans‐generational indirect benefit of MHC‐based mate choice for genetic compatibility from trans‐generational data in a wild bird population. By investigating the fitness benefits of mate choice, this study serves to facilitate our understanding of the evolution of MHC‐based mate choice.     

Fear and lethality in snowshoe hares: the deadly effects of non‐consumptive predation risk

Predators play a critical, top–down role in shaping ecosystems, driving prey population and community dynamics. Traditionally, studies of predator‐prey interactions have focused on direct effects of predators, namely the killing of prey. More recently, the non‐consumptive effects of predation risk are being appreciated; e.g. the ‘ecology of fear’. Prey responses to predation risk can be morphological, behavioural, and physiological, and are assumed to come at a cost to prey fitness. However, few studies have examined the relationship between predation risk and survival in wild animals. We tested the hypothesis that predation risk itself could reduce survival in wild‐caught snowshoe hares. We exposed female snowshoe hares to a simulated predator (a trained dog) during gestation only, and measured adult survival and, in surviving females, their ability to successfully wean offspring. We show for the first time in a wild mammal that the risk of predation can itself be lethal. Predation risk reduced adult female survival by 30%, and had trans‐generational effects, reducing offspring survival to weaning by over 85% – even though the period of risk ended at birth. As a consequence of these effects the predator‐exposed group experienced a decrease in number, while the control group substantially increased. Challenges remain in determining the importance of risk‐induced mortality in natural field settings; however, our findings show that non‐lethal predator encounters can influence survival of both adults and offspring. Future work is needed to test these effects in free‐living animals.     

Reproductive senescence and parental effects in an indeterminate grower

Reproductive senescence is the decrease of reproductive performance with increasing age and can potentially include trans‐generational effects as the offspring produced by old parents might have a lower fitness than those produced by young parents. This negative effect may be caused either by the age of the father, mother or the interaction between the ages of both parents. Using the common woodlouse Armadillidium vulgare, an indeterminate grower, as a biological model, we tested for the existence of a deleterious effect of parental age on fitness components. Contrary to previous findings reported from vertebrate studies, old parents produced both a higher number and larger offspring than young parents. However, their offspring had lower fitness components (by surviving less, producing a smaller number of clutches or not reproducing at all) than offspring born to young parents. Our findings strongly support the existence of trans‐generational senescence in woodlice and contradict the belief that old individuals in indeterminate growers contribute the most to recruitment and correspond thereby to the key life stage for population dynamics. Our work also provides rare evidence that the trans‐generational effect of senescence can be stronger than direct reproductive senescence in indeterminate growers.     

Females avoid manipulative males and live longer

Abstract Female mate choice has been demonstrated in a wide variety of species and is now accepted as an important factor in sexual selection. One of the remaining questions, however, is why females prefer specific males. Do females or their offspring benefit from their choice? Or do females choose mates to minimize costs of mating? Here we show that, in the ovoviviparous cockroach Nauphoeta cinerea, where sexual selection has been well documented, females chose mates to avoid costly male manipulation. Females were partnered with preferred or nonpreferred mates, and fitness of the females measured. We found that females lived longer when they mated with preferred males. Female lifespan depended on the rate at which offspring developed from egg to parturition: slower development led to longer life. We manipulated the male pheromone and showed that the component of the pheromone blend that makes males attractive to females also delayed parturition. Thus, like other aspects of sexual conflict in this species, offspring development and thereby the mother's lifespan depended on exposure of females to specific components of the male pheromone. Males benefit from manipulating offspring development because females with accelerated parturition remained unreceptive whereas females with slower developing offspring readily remated after giving birth to their offspring. Our results suggest a hormone‐like role for the male pheromone in N. cinerea and provide the first direct evidence of mate choice to avoid male manipulation. This study shows that dominant males may not be preferred males if they are manipulating females, why multiple components with contrasting effects can exist in a sexual signal, and emphasizes the complex fitness relationships that can arise in species with sexual conflict.     

COSTLY INFIDELITY: LOW LIFETIME FITNESS OF EXTRA‐PAIR OFFSPRING IN A PASSERINE BIRD

Extra‐pair copulation (EPC) is widespread in socially monogamous species, but its evolutionary benefits remain controversial. Indirect genetic benefit hypotheses postulate that females engage in EPC to produce higher quality extra‐pair offspring (EPO) than within‐pair offspring (WPO). In contrast, the sexual conflict hypothesis posits that EPC is beneficial to males but not to females. Thus, under the sexual conflict hypothesis, EPO are predicted to be no fitter than WPO. We tested these two hypotheses in a 12‐year dataset with complete life‐history and pedigree information from an isolated island population of house sparrows (Passer domesticus). We compared fitness components of EPO and two types of WPO: (1) WPO from genetically polyandrous “unfaithful” mothers, and (2) WPO from genetically monogamous mothers. We found that all three groups of offspring had similar probabilities of hatching and nestling survival. Unexpectedly, EPO had the lowest probability of recruiting into the breeding population and the lowest lifetime reproductive output. Our results indicate that EPO incurred indirect genetic costs, rather than benefits, which is contrary to indirect benefit models. Importantly, the indirect costs we observed are also underappreciated in current sexual conflict models. Our results call for improved theoretical frameworks that incorporate indirect costs by extending current sexual conflict models.     

Sexual conflict is not counterbalanced by good genes in the laboratory Drosophila melanogaster model system

Sexual conflict theory is based on the observation that females of many species are harmed through their interactions with males. Direct harm to females, however, can potentially be counterbalanced by indirect genetic benefits, where females make up for a reduction in offspring quantity by an increase in offspring quality through a generic increase in offspring fitness (good genes) and/or one restricted to the context of sexual selection (sexy sons). Here, we quantify the magnitude of the good genes mechanism of indirect benefits in a laboratory-adapted population of Drosophila melanogaster. We find that despite high-standing genetic variance for fitness, females gain at most only a modest benefit through the good genes form of indirect benefits--far too little to counterbalance the direct cost of male-induced harm.     

Maternal effects are long‐lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live‐bearing fish. Fry from mothers reared on two different nutritional diets (HQ = high quality and LQ = low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long‐lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low‐quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

REMATING IN DROSOPHILA MELANOGASTER: ARE INDIRECT BENEFITS CONDITION DEPENDENT?

By measuring the direct and indirect fitness costs and benefits of sexual interactions, the feasibility of alternate explanations for polyandry can be experimentally assessed. This approach becomes more complicated when the relative magnitude of the costs and/or benefits associated with multiple mating (i.e., remating with different males) vary with female condition, as this may influence the strength and direction of sexual selection. Here, using the model organism Drosophila melanogaster, we test whether the indirect benefits that a nonvirgin female gains by remating (“trading‐up”) are influenced by her condition (body size). We found that remating by small‐bodied, low‐fecundity females resulted in the production of daughters of relatively higher fecundity, whereas the opposite pattern was observed for large‐bodied females. In contrast, remating had no measurable effect on the relative reproductive success of sons from dams of either body size. These results are consistent with a hypothesis based on sexually antagonistic genetic variation. The implications of these results to our understanding of the evolution and consequences of polyandry are discussed.     

Trans‐generational effects on ageing in a wild bird population

Ageing, long thought to be too infrequent to study effectively in natural populations, has recently been shown to be ubiquitous, even in the wild. A major challenge now is to explain variation in the rates of ageing within populations. Here, using 49 years of data from a population of great tits (Parus major), we show that offspring life‐history trajectories vary with maternal age. Offspring hatched from older mothers perform better early in life, but suffer from an earlier onset, and stronger rate, of reproductive senescence later in life. Offspring reproductive lifespan is, however, unaffected by maternal age, and the different life‐history trajectories result in a similar fitness payoff, measured as lifetime reproductive success. This study therefore identifies maternal age as a new factor underlying variation in rates of ageing, and, given the delayed trans‐generational nature of this effect, poses the question as to proximate mechanisms linking age‐effects across generations.