Rising temperatures threaten pollinators of fig trees-Keystone resources of tropical forests.

Pollinating insects are decreasing worldwide in abundance, biomass, and species richness, affecting the plants that rely on pollinators for fruit production and seed set. Insects are often sensitive to high temperatures. The projected temperature increases may therefore severely affect plants that rely on insect pollinators. Highly specialized mutualisms are expected to be particularly vulnerable to change because they have fewer partner options should one partner become unavailable. In the highly specialized mutualism between fig trees and their pollinating fig wasp, each fig species is pollinated by only one or a few wasp species. Because of their year-round fruit production, fig trees are considered a keystone resource for tropical forests. However, to produce fruits, wild fig trees need to be pollinated by fig wasps that typically travel a long one-way trip from the tree donating pollen to the tree receiving pollen. In a few previous studies from China and Australia, increasing temperatures dramatically decreased fig wasp lifespan. Are these grim results generalizable to fig mutualisms globally? Here, we use survival experiments to determine the effect of increasing temperature on the lifespan of Neotropical fig wasps associated with five common Panamanian Ficus species. Experimental temperatures were based on the current daytime mean temperature of 26.8°C (2SD: 21.6-31.7°C) and the predicted local temperature increase of 1-4°C by the end of the 21st century. We found that all tested pollinator wasp species had a significantly shorter lifespan in 30, 32, 34, and 36°C compared to the current diurnal mean temperature of 26°C. At 36°C pollinator median lifespan decreased to merely 2-10 h (6%-19% of their median lifespan at 26°C). Unless wasps can adapt, such a dramatic reduction in lifespan is expected to reduce the number of pollinators that successfully disperse to flowering fig trees, and may therefore jeopardize both fruit set and eventually survival of the mutualism.

Beneficial cumulative effects of old parental age on offspring fitness.

Old parental age is commonly associated with negative effects on offspring life-history traits. Such parental senescence effects are predicted to have a cumulative detrimental effect over successive generations. However, old parents may benefit from producing higher quality offspring when these compete for seasonal resources. Thus, old parents may choose to increase investment in their offspring, thereby producing fewer but larger and more competitive progeny. We show that Caenorhabditis elegans hermaphrodites increase parental investment with advancing age, resulting in fitter offspring who reach their reproductive peak earlier. Remarkably, these effects increased over six successive generations of breeding from old parents and were subsequently reversed following a single generation of breeding from a young parent. Our findings support the hypothesis that offspring of old parents receive more resources and convert them into increasingly faster life histories. These results contradict the theory that old parents transfer a cumulative detrimental 'ageing factor' to their offspring.

Should females prefer old males?

Whether females should prefer to mate with old males is controversial. Old males may sire offspring of low quality because of an aging germline, but their proven ability to reach an old age can also be an excellent indicator of superior genetic quality, especially in natural populations. These genetic effects are, however, hard to study in nature, because they are often confounded with direct benefits offered by old males to the female, such as experience and high territory quality. We, therefore, used naturally occurring extra-pair young to disentangle different aspects of male age on female fitness in a natural population of collared flycatchers because any difference between within- and extra-pair young within a nest should be caused by paternal genetic effects only. Based on 18 years of long-term data, we found that females paired with older males as social partners experienced an overall reproductive advantage. However, offspring sired by old males were of lower quality as compared to their extra-pair half-siblings, whereas the opposite was found in nests attended by young males. These results imply a negative genetic effect of old paternal age, given that extra-pair males are competitive middle-age males. Thus, offspring may benefit from being sired by young males but raised by old males, to maximize both genetic and direct effects. Our results show that direct and genetic benefits from pairing with old males may act in opposing directions and that the quality of the germline may deteriorate before other signs of senescence become obvious.

Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing.

Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The 'disposable soma' theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five 'longevity' genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.

Environmental variation mediates the evolution of anticipatory parental effects.

Theory maintains that when future environment is predictable, parents should adjust the phenotype of their offspring to match the anticipated environment. The plausibility of positive anticipatory parental effects is hotly debated and the experimental evidence for the evolution of such effects is currently lacking. We experimentally investigated the evolution of anticipatory maternal effects in a range of environments that differ drastically in how predictable they are. Populations of the nematode Caenorhabditis remanei, adapted to 20°C, were exposed to a novel temperature (25°C) for 30 generations with either positive or zero correlation between parent and offspring environment. We found that populations evolving in novel environments that were predictable across generations evolved a positive anticipatory maternal effect, because they required maternal exposure to 25°C to achieve maximum reproduction in that temperature. In contrast, populations evolving under zero environmental correlation had lost this anticipatory maternal effect. Similar but weaker patterns were found if instead rate-sensitive population growth was used as a fitness measure. These findings demonstrate that anticipatory parental effects evolve in response to environmental change so that ill-fitting parental effects can be rapidly lost. Evolution of positive anticipatory parental effects can aid population viability in rapidly changing but predictable environments.

Parental effects influence life history traits and covary with an environmental cline in common frog populations.

Across latitudinal clines, the juvenile developmental rates of ectotherms often covary with the length of the growing season, due to life-history trade-offs imposed by the time-constrained environments. However, as the start of the growing season often varies substantially across years, adaptive parental effects on juvenile developmental rates may mediate the costs of a delayed season. By employing a meta-analysis, we tested whether larval developmental rates across a latitudinal cline of the common frog (Rana temporaria) are affected by fluctuating onsets of breeding, across years. We predicted that larval developmental rate will be inversely related to the onset of breeding, and that northern populations will be more prone to shorten their developmental rate in response to late breeding, as the costs of delayed metamorphosis should be highest in areas with a shorter growing season. We found that the larval period of both northern and southern populations responded to parental environmental conditions to a similar degree in absolute terms, but in different directions. In northern populations, a late season start correlated with decreased development time, suggesting that the evolution of parental effects aids population persistence in time-constrained environments. In southern populations, late season start correlated with increased development time, which could potentially be explained as a predator avoidance strategy. Our findings suggest that local ecological variables can induce adaptive parental effects, but responses are complex, and likely trade-off with other ecological factors.

Silver-spoon upbringing improves early-life fitness but promotes reproductive ageing in a wild bird.

Early-life conditions can have long-lasting effects and organisms that experience a poor start in life are often expected to age at a faster rate. Alternatively, individuals raised in high-quality environments can overinvest in early-reproduction resulting in rapid ageing. Here we use a long-term experimental manipulation of early-life conditions in a natural population of collared flycatchers (Ficedula albicollis), to show that females raised in a low-competition environment (artificially reduced broods) have higher early-life reproduction but lower late-life reproduction than females raised in high-competition environment (artificially increased broods). Reproductive success of high-competition females peaked in late-life, when low-competition females were already in steep reproductive decline and suffered from a higher mortality rate. Our results demonstrate that 'silver-spoon' natal conditions increase female early-life performance at the cost of faster reproductive ageing and increased late-life mortality. These findings demonstrate experimentally that natal environment shapes individual variation in reproductive and actuarial ageing in nature.

Dietary Restriction Improves Fitness of Aging Parents But Reduces Fitness of Their Offspring in Nematodes.

Dietary restriction (DR) is a well-established intervention to extend lifespan across taxa. Recent studies suggest that DR-driven lifespan extension can be cost-free, calling into question a central tenant of the evolutionary theory of aging. Nevertheless, boosting parental longevity can reduce offspring fitness. Such intergenerational trade-offs are often ignored but can account for the "missing costs" of longevity. Here, we use the nematode Caenorhabditis remanei to test for effects of DR by fasting on fitness of females and their offspring. Females deprived of food for 6 days indeed had increased fecundity, survival, and stress resistance after re-exposure to food compared with their counterparts with constant food access. However, offspring of DR mothers had reduced early and lifetime fecundity, slower growth rate, and smaller body size at sexual maturity. These findings support the direct trade-off between investment in soma and gametes challenging the hypothesis that increased somatic maintenance and impaired reproduction can be decoupled.

Kin but less than kind: within-group male relatedness does not increase female fitness in seed beetles.

Theory maintains within-group male relatedness can mediate sexual conflict by reducing male-male competition and collateral harm to females. We tested whether male relatedness can lessen female harm in the seed beetle Callosobruchus maculatus. Male relatedness did not influence female lifetime reproductive success or individual fitness across two different ecologically relevant scenarios of mating competition. However, male relatedness marginally improved female survival. Because male relatedness improved female survival in late life when C. maculatus females are no longer producing offspring, our results do not provide support for the role of within-group male relatedness in mediating sexual conflict. The fact that male relatedness improves the post-reproductive part of the female life cycle strongly suggests that the effect is non-adaptive. We discuss adaptive and non-adaptive mechanisms that could result in reduced female harm in this and previous studies, and suggest that cognitive error is a likely explanation.

Experimentally reduced insulin/IGF-1 signaling in adulthood extends lifespan of parents and improves Darwinian fitness of their offspring.

Classical theory maintains that ageing evolves via energy trade-offs between reproduction and survival leading to accumulation of unrepaired cellular damage with age. In contrast, the emerging new theory postulates that ageing evolves because of deleterious late-life hyper-function of reproduction-promoting genes leading to excessive biosynthesis in late-life. The hyper-function theory uniquely predicts that optimizing nutrient-sensing molecular signaling in adulthood can simultaneously postpone ageing and increase Darwinian fitness. Here, we show that reducing evolutionarily conserved insulin/IGF-1 nutrient-sensing signaling via daf-2 RNA interference (RNAi) fulfils this prediction in Caenorhabditis elegans nematodes. Long-lived daf-2 RNAi parents showed normal fecundity as self-fertilizing hermaphrodites and improved late-life reproduction when mated to males. Remarkably, the offspring of daf-2 RNAi parents had higher Darwinian fitness across three different genotypes. Thus, reduced nutrient-sensing signaling in adulthood improves both parental longevity and offspring fitness supporting the emerging view that suboptimal gene expression in late-life lies at the heart of ageing.

Predation drives local adaptation of phenotypic plasticity.

Phenotypic plasticity is the ability of an individual genotype to alter aspects of its phenotype depending on the current environment. It is central to the persistence, resistance and resilience of populations facing variation in physical or biological factors. Genetic variation in plasticity is pervasive, which suggests its local adaptation is plausible. Existing studies on the adaptation of plasticity typically focus on single traits and a few populations, while theory about interactions among genes (for example, pleiotropy) suggests that a multi-trait, landscape scale (for example, multiple populations) perspective is required. We present data from a landscape scale, replicated, multi-trait experiment using a classic predator-prey system centred on the water flea Daphnia pulex. We find predator regime-driven differences in genetic variation of multivariate plasticity. These differences are associated with strong divergent selection linked to a predation regime. Our findings are evidence for local adaptation of plasticity, suggesting that responses of populations to environmental variation depend on the conditions in which they evolved in the past.

Evolution of a predator-induced, nonlinear reaction norm.

Inducible, anti-predator traits are a classic example of phenotypic plasticity. Their evolutionary dynamics depend on their genetic basis, the historical pattern of predation risk that populations have experienced and current selection gradients. When populations experience predators with contrasting hunting strategies and size preferences, theory suggests contrasting micro-evolutionary responses to selection. Daphnia pulex is an ideal species to explore the micro-evolutionary response of anti-predator traits because they face heterogeneous predation regimes, sometimes experiencing only invertebrate midge predators and other times experiencing vertebrate fish and invertebrate midge predators. We explored plausible patterns of adaptive evolution of a predator-induced morphological reaction norm. We combined estimates of selection gradients that characterize the various habitats that D. pulex experiences with detail on the quantitative genetic architecture of inducible morphological defences. Our data reveal a fine scale description of daphnid defensive reaction norms, and a strong covariance between the sensitivity to cues and the maximum response to cues. By analysing the response of the reaction norm to plausible, predator-specific selection gradients, we show how in the context of this covariance, micro-evolution may be more uniform than predicted from size-selective predation theory. Our results show how covariance between the sensitivity to cues and the maximum response to cues for morphological defence can shape the evolutionary trajectory of predator-induced defences in D. pulex.

Antagonistically pleiotropic allele increases lifespan and late-life reproduction at the cost of early-life reproduction and individual fitness.

Evolutionary theory of ageing maintains that increased allocation to early-life reproduction results in reduced somatic maintenance, which is predicted to compromise longevity and late-life reproduction. This prediction has been challenged by the discovery of long-lived mutants with no loss of fecundity. The first such long-lived mutant was found in the nematode worm Caenorhabditis elegans Specifically, partial loss-of-function mutation in the age-1 gene, involved in the nutrient-sensing insulin/insulin-like growth factor signalling pathway, confers longevity, as well as increased resistance to pathogens and to temperature stress without appreciable fitness detriment. Here, we show that the long-lived age-1(hx546) mutant has reduced fecundity and offspring production in early-life, but increased fecundity, hatching success, and offspring production in late-life compared with wild-type worms under standard conditions. However, reduced early-life performance of long-lived mutant animals was not fully compensated by improved performance in late-life and resulted in reduced individual fitness. These results suggest that the age-1(hx546) allele has opposing effects on early-life versus late-life fitness in accordance with antagonistic pleiotropy (AP) and disposable soma theories of ageing. These findings support the theoretical conjecture that experimental studies based on standing genetic variation underestimate the importance of AP in the evolution of ageing.

Rapamycin additively extends lifespan in short- and long-lived lines of the nematode Caenorhabditis remanei.

Despite tremendous progress in finding genes that, when manipulated, affects lifespan, little is known about the genetics underlying natural variation in lifespan. While segregating genetic variants for lifespan has been notoriously difficult to find in genome-wide association studies (GWAS), a complementary approach is to manipulate key genetic pathways in lines that differ in lifespan. If these candidate pathways are down regulated in long-lived lines, these lines can be predicted to respond less to pharmaceutical down-regulation of these pathways than short-lived lines. Experimental studies have identified the nutrient-sensing pathway TOR as a key regulator of lifespan in model organisms, and this pathway can effectively be down regulated using the drug rapamycin, which extends lifespan in all tested species. We expose short- and long-lived lines of the nematode Caenorhabditis remanei to rapamycin, and investigate if long-lived lines, which are hypothesized to already have down-regulated TOR signaling, respond less to rapamycin. We found no interaction between line and rapamycin treatment, since rapamycin extended lifespan independent of the intrinsic lifespan of the lines. This shows that rapamycin is equally effective on long and short-lived lines, and suggests that the evolution of long life may involve more factors that down-regulation of TOR.

Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles.

The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history and morphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individual-level sex-specific selection and population demography and places life-history traits at the epicenter of these dynamics.

Sexually antagonistic selection on genetic variation underlying both male and female same-sex sexual behavior.

BACKGROUND: Intralocus sexual conflict, arising from selection for different alleles at the same locus in males and females, imposes a constraint on sex-specific adaptation. Intralocus sexual conflict can be alleviated by the evolution of sex-limited genetic architectures and phenotypic expression, but pleiotropic constraints may hinder this process. Here, we explored putative intralocus sexual conflict and genetic (co)variance in a poorly understood behavior with near male-limited expression. Same-sex sexual behaviors (SSBs) generally do not conform to classic evolutionary models of adaptation but are common in male animals and have been hypothesized to result from perception errors and selection for high male mating rates. However, perspectives incorporating sex-specific selection on genes shared by males and females to explain the expression and evolution of SSBs have largely been neglected. RESULTS: We performed two parallel sex-limited artificial selection experiments on SSB in male and female seed beetles, followed by sex-specific assays of locomotor activity and male sex recognition (two traits hypothesized to be functionally related to SSB) and adult reproductive success (allowing us to assess fitness consequences of genetic variance in SSB and its correlated components). Our experiments reveal both shared and sex-limited genetic variance for SSB. Strikingly, genetically correlated responses in locomotor activity and male sex-recognition were associated with sexually antagonistic fitness effects, but these effects differed qualitatively between male and female selection lines, implicating intralocus sexual conflict at both male- and female-specific genetic components underlying SSB. CONCLUSIONS: Our study provides experimental support for the hypothesis that widespread pleiotropy generates pervasive intralocus sexual conflict governing the expression of SSBs, suggesting that SSB in one sex can occur due to the expression of genes that carry benefits in the other sex.

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.

Sex-specific Tradeoffs With Growth and Fitness Following Life-span Extension by Rapamycin in an Outcrossing Nematode, Caenorhabditis remanei.

Rapamycin inhibits the nutrient-sensing TOR pathway and extends life span in a wide range of organisms. Although life-span extension usually differs between the sexes, the reason for this is poorly understood. Because TOR influences growth, rapamycin likely affects life-history traits such as growth and reproduction. Sexes have different life-history strategies, and theory predicts that they will resolve the tradeoffs between growth, reproduction, and life span differently. Specifically, in taxa with female-biased sexual size dimorphism, reduced growth may have smaller effects on male fitness. We investigated the effects of juvenile, adult, or life-long rapamycin treatment on growth, reproduction, life span, and individual fitness in the outcrossing nematode Caenorhabditis remanei Life-long exposure to rapamycin always resulted in the strongest response, whereas postreproductive exposure did not affect life span. Although rapamycin resulted in longer life span and smaller size in males, male individual fitness was not affected. In contrast, size and fitness were negatively affected in females, whereas life span was only extended under high rapamycin concentrations. Our results support the hypothesis that rapamycin affects key life-history traits in a sex-specific manner. We argue that the fitness cost of life-span extension will be sex specific and propose that the smaller sex generally pay less while enjoying stronger life-span increase.

The alignment between phenotypic plasticity, the major axis of genetic variation and the response to selection.

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.