The short-term and long-term effects of parental age in the bean weevil (Acanthoscelides obtectus)

We examined the influence of parental age on life history traits of their offspring in the lines of bean weevil that have evolved different rates of senescence. Measurements included preadult traits (egg size, embryonic developmental time, total preadult developmental time, preadult viability) and adult traits (body weight, total realized fecundity of females, first day of egg laying, early fecundity, late fecundity and longevity). The negative parental age effects were observed for all traits except for the early and total realized fecundity. We did not detect statistically significant line×parental age interactions for either preadult- or adult-survival, so offspring survival did not change with parental age after selection for early vs. late reproduction. It seems that selection acting on the quality of offspring produced by parents of different ages has not been responsible for the evolution of senescence in bean weevil. This revised version was published online in August 2006 with corrections to the Cover Date.     

Phenotypic selection and regulation of reproduction in different environments in wild barley

Plasticity of the phenotypic architecture of wild barley, Hordeum spontaneum, was studied in response to water and nutrient stress. Direct and indirect selection on several vegetative and reproductive traits was estimated and path analysis used to reveal how regulating pathways via maternal investment differed between environments. Vegetative traits displayed differential regulating effect on fitness across experimental environments: (1) increase in size was selected for under optimal conditions and under water stress, but not under nutrient stress; (2) allocation to root biomass was selected for under optimal conditions, but it had no effect under nutrient stress and was strongly selected against when water was limiting; (3) delayed onset of reproduction was selected under nutrient limitation whereas earlier onset was selected under water stress. The regulating effect of reproductive traits on final reproductive output also differed across treatments, operating either at the 'early' stage of plant development through varying the number of initiated spikelets per spike (no stress and water stress treatment) or at the 'late' developmental stage adjusting the fertile spikelet weight (no stress and nutrient stress treatment). Reproductive output was regulated via seed abortion under no stress and water stress treatments. Although the underlying mechanism of the regulation through abortion has yet to be discovered, the specific mechanism of abortion under water stress appears to be different from that under optimal conditions. Our results demonstrate that not only is the character architecture in wild barley plastic and sensitive to changing availability of water and nutrients, but the regulating mechanism of maternal investment is also environmentally sensitive.     

Adaptation to developmental diet influences the response to selection on age at reproduction in the fruit fly

Experimental evolution (EE) is a powerful tool for addressing how environmental factors influence life‐history evolution. While in nature different selection pressures experienced across the lifespan shape life histories, EE studies typically apply selection pressures one at a time. Here, we assess the consequences of adaptation to three different developmental diets in combination with classical selection for early or late reproduction in the fruit fly Drosophila melanogaster. We find that the response to each selection pressure is similar to that observed when they are applied independently, but the overall magnitude of the response depends on the selection regime experienced in the other life stage. For example, adaptation to increased age at reproduction increased lifespan across all diets; however, the extent of the increase was dependent on the dietary selection regime. Similarly, adaptation to a lower calorie developmental diet led to faster development and decreased adult weight, but the magnitude of the response was dependent on the age‐at‐reproduction selection regime. Given that multiple selection pressures are prevalent in nature, our findings suggest that trade‐offs should be considered not only among traits within an organism, but also among adaptive responses to different—sometimes conflicting—selection pressures, including across life stages.     

Oxidative shielding and the cost of reproduction

Life‐history theory assumes that reproduction and lifespan are constrained by trade‐offs which prevent their simultaneous increase. Recently, there has been considerable interest in the possibility that this cost of reproduction is mediated by oxidative stress. However, empirical tests of this theory have yielded equivocal support. We carried out a meta‐analysis to examine associations between reproduction and oxidative damage across markers and tissues. We show that oxidative damage is positively associated with reproductive effort across females of various species. Yet paradoxically, categorical comparisons of breeders versus non‐breeders reveal that transition to the reproductive state is associated with a step‐change reduction in oxidative damage in certain tissues and markers. Developing offspring may be particularly sensitive to harm caused by oxidative damage in mothers. Therefore, such reductions could potentially function to shield reproducing mothers, gametes and developing offspring from oxidative insults that inevitably increase as a consequence of reproductive effort. According to this perspective, we hypothesise that the cost of reproduction is mediated by dual impacts of maternally‐derived oxidative damage on mothers and offspring, and that mothers may be selected to diminish such damage. Such oxidative shielding may explain why many existing studies have concluded that reproduction has little or no oxidative cost. Future advance in life‐history theory therefore needs to take account of potential transgenerational impacts of the mechanisms underlying life‐history trade‐offs.     

Among‐year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana

Incomplete information regarding both selection regimes and the genetic basis of fitness limits our understanding of adaptive evolution. Among‐year variation in the genetic basis of fitness is rarely quantified, and estimates of selection are typically based on single components of fitness, thus potentially missing conflicting selection acting during other life‐history stages. Here, we examined among‐year variation in selection on a key life‐history trait and the genetic basis of fitness covering the whole life cycle in the annual plant Arabidopsis thaliana. We planted freshly matured seeds of >200 recombinant inbred lines (RILs) derived from a cross between two locally adapted populations (Italy and Sweden), and both parental genotypes at the native site of the Swedish population in three consecutive years. We quantified selection against the nonlocal Italian genotype, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on timing of germination during different life stages. In all 3 years, the local Swedish genotype outperformed the nonlocal Italian genotype. However, both the contribution of early life stages to relative fitness, and the effects of fitness QTL varied among years. Timing of germination was under conflicting selection through seedling establishment vs. adult survival and fecundity, and both the direction and magnitude of net selection varied among years. Our results demonstrate that selection during early life stages and the genetic basis of fitness can vary markedly among years, emphasizing the need for multiyear studies considering the whole life cycle for a full understanding of natural selection and mechanisms maintaining local adaptation.     

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.     

Heat knockdown resistance and chill‐coma recovery as correlated responses to selection on mating success at high temperature in Drosophila buzzatii

Reproduction and related traits such as mating success are strongly affected by thermal stress. We tested direct and correlated responses to artificial selection in replicated lines of Drosophila buzzatii that were selected for mating success at high temperature. Knockdown resistance at high temperature (KRHT) and chill‐coma recovery (CCR) were tested as correlated selection responses. Virgin flies were allowed to mate for four hours at 33°C in three replicated lines (S lines) to obtain the selected flies and then returned at 25°C to lay eggs. Other three replicated lines were maintained at 25°C without any selection as control (C lines). After 15 selection generations, KRHT and CCR were measured. Both traits were assessed in flies that did not receive any hardening pretreatments as well as in flies that were either heat or cold hardened. Thermotolerance traits showed significant correlated responses with higher KRHT in S than in C lines, both with a heat‐hardening pretreatment and without a heat‐hardening pretreatment. CCR time was longer in S than in C lines both with a cold‐hardening pretreatment and without a cold‐hardening pretreatment. Hardening treatments improved both KRHT and CCR in all cases excepting KRHT in C lines. Overall, KRHT and CCR showed an antagonistic pattern of correlated responses to our selection regime, suggesting either pleiotropy or tightly linked trait‐specific genes partially affecting KRHT and CCR.     

Heat shock proteins mediate trade‐offs between early‐life reproduction and late survival in Drosophila melanogaster

Ageing and the resulting increased likelihood mortality are the inescapable fate of organisms because selection pressures on genes that exert their function late in life is weak, promoting the evolution of genes that enhance early‐life reproductive performance at the same time as sacrificing late survival. Heat shock proteins (HSP) are known to buffer various environmental stresses and are also involved in protein homeostasis and longevity. The characteristics of genes for HSPs (hsp) imply that they affect various life‐history traits, which in turn affect longevity; however, little is known about the effects of hsp genes on life‐history traits and their interaction with longevity. In the present study, the effects of hsp genes on multiple fitness traits, such as locomotor activity, total fecundity, early fecundity and survival time, are investigated in Drosophila melanogaster Meigen using RNA interference (RNAi). In egg‐laying females, RNAi knockdown of six hsp genes (hsp22, hsp23, hsp67Ba, hsp67Bb, hsp67Bc and hsp27‐like) does not shorten survival but rather increases it. Knockdown of five of those genes on an individual basis reduces early‐life reproduction, suggesting that several hsp genes mediate the trade‐off between early reproduction and late survival. The data indicate a positive effect of hsp genes on early reproduction and also negative effects on survival time, supporting the antagonistic pleiotropic effects predicted by the optimality theory of ageing.     

Experimental evidence of early costs of reproduction in conspecific viviparous and oviparous lizards

Reproduction entails costs, and disentangling the relative importance of each stage of the reproductive cycle may be important to assess the costs and benefits of different reproductive strategies. We studied the early costs of reproduction in oviparous and viviparous lizard females of the bimodal reproductive species Zootoca vivipara. Egg retention time in oviparous females is approximately one-third of the time in viviparous females. We compared the vitellogenesis and egg retention stages that are common to both reproductive modes. Precisely, we monitored the thermoregulatory behaviour, the weight gain and the immunocompetence of the females. Moreover, we injected an antigen in half of the females (immune challenge) to study the trade-offs between reproductive mode and immune performance and between different components of the immune system. Finally, we experimentally induced parturition in viviparous females at the time of egg laying in oviparous females. Oviparous and viviparous females did not show strong differences in response to the immune challenge. However, viviparous females spent more time thermoregulating while partially hidden and gained more weight than oviparous females. The greater weight gain indicates that the initial period of egg retention is less costly for viviparous than for oviparous females or that viviparous females are able to save and accumulate energy at this period. This energy may be used by viviparous females to cope with the subsequent costs of the last two-third of the gestation. Such an ability to compensate the higher costs of a longer egg retention period may account for the frequent evolution of viviparity in squamate reptiles.     

Sexual selection on brain size in shorebirds (Charadriiformes)

Natural selection is considered a major force shaping brain size evolution in vertebrates, whereas the influence of sexual selection remains controversial. On one hand, sexual selection could promote brain enlargement by enhancing cognitive skills needed to compete for mates. On the other hand, sexual selection could favour brain size reduction due to trade‐offs between investing in brain tissue and in sexually selected traits. These opposed predictions are mirrored in contradictory relationships between sexual selection proxies and brain size relative to body size. Here, we report a phylogenetic comparative analysis that highlights potential flaws in interpreting relative brain size‐mating system associations as effects of sexual selection on brain size in shorebirds (Charadriiformes), a taxonomic group with an outstanding diversity in breeding systems. Considering many ecological effects, relative brain size was not significantly correlated with testis size. In polyandrous species, however, relative brain sizes of males and females were smaller than in monogamous species, and females had smaller brain size than males. Although these findings are consistent with sexual selection reducing brain size, they could also be due to females deserting parental care, which is a common feature of polyandrous species. Furthermore, our analyses suggested that body size evolved faster than brain size, and thus the evolution of body size may be confounding the effect of the mating system on relative brain size. The brain size‐mating system association in shorebirds is thus not only due to sexual selection on brain size but rather, to body size evolution and other multiple simultaneous effects.     

Species with greater seed mass are more tolerant of conspecific neighbours: a key driver of early survival and future abundances in a tropical forest

Multiple niche‐based processes including conspecific negative density dependence (CNDD) determine plant regeneration and community structure. We ask how interspecific and intraspecific density‐dependent interactions relate to plant life histories and associated functional traits. Using hierarchical models, we analysed how such interactions affected first‐year survival of seedling recruits of 175 species in a tropical forest, and how species abundances and functional traits are related to interspecific variation in density‐dependent effects. Conspecific seedling neighbour effects prevailed over the effects of larger conspecific and all heterospecific neighbours. Tolerance of seedling CNDD enhanced recruit survival and subsequent abundance, all of which were greater among larger seeded, slow‐growing and well‐defended species. Niche differentiation along the growth–survival trade‐off and tolerance of seedling CNDD strongly correlated with regeneration success, with manifest consequences for community structure. The ability of larger seeded species to better tolerate CNDD suggests a novel mechanism for CNDD to contribute to seed‐size variation and promote species coexistence through a tolerance–fecundity trade‐off.     

The effects of reproduction on courtship, fertility and longevity within and between alternative male mating tactics of the horned beetle, Onthophagus binodis

Life history theory provides a powerful tool to study an organism's biology within an evolutionary framework. The notion that males face a longevity cost of competing for and displaying to females lies at the core of sexual selection theory. Likewise, recent game theory models of the evolution of ejaculation strategies assume that males face a trade-off between expenditure on the ejaculate and expenditure on gaining additional matings. Males of the dung beetle Onthophagus binodis adopt alternative reproductive tactics in which major males fight for and help provision females, and minor males sneak copulations with females that are guarded by major males. Minor males are always subject to sperm competition, and consistent with theoretical expectation, minor males have a greater expenditure on their ejaculate than major males. We used this model system to seek evidence that mating comes at a cost for future fertility and/or male expenditure on courtship and attractiveness, and to establish whether these traits vary between alternative mating tactics. We monitored the lifespan of males exposed to females and nonmating populations, and sampled males throughout their lives to assess their fertility and courtship behaviour. We found a significant longevity cost of reproduction, but no fertility cost. On average, males from mating populations had a lower courtship rate than those from nonmating populations. This small effect, although statistically nonsignificant, was associated with significant increases in the time males required to achieve mating. Minor males had lower courtship rates than major males, and took longer to achieve mating. Although we did not measure ejaculate expenditure in this study, the correlation between lower courtship rate and longer mating speed of minor males documented here with their greater expenditure on the ejaculate found in previous studies, is consistent with game theory models of ejaculate expenditure which assume that males trade expenditure on gaining matings for expenditure on gaining fertilizations.     

Cognitive costs of reproduction: life‐history trade‐offs explain cognitive decline during pregnancy in women

Life‐history theory predicts that access to limited resources leads to trade‐offs between competing body functions. Women, who face higher costs of reproduction when compared to men, should be especially vulnerable to these trade‐offs. We propose the ‘cognitive costs of reproduction hypothesis’, which states that energy trade‐offs imposed by reproduction may lead to a decline in maternal cognitive function during gestation. In particular, we hypothesize that the decline in cognitive function frequently observed during pregnancy is associated with the allocation of resources between the competing energetic requirements of the mother's brain and the developing foetus. Several distinctive anatomical and physiological features including a high metabolic rate of the brain, large infant size, specific anatomical features of the placenta and trophoblast, and the lack of maternal control over glucose flow through the placenta make the occurrence of these trade‐offs likely. Herein, we review several lines of evidence for trade‐offs between gestation and cognition that are related to: (i) energy metabolism during reproduction; (ii) energy metabolism of the human brain; (iii) links between energy metabolism and cognitive function; and (iv) links between gestation and cognitive function. We also review evidence for the important roles of cortisol, corticotropin‐releasing hormone and sex hormones in mediating the effects of gestation on cognition, and we discuss possible neurophysiological mechanisms underlying the observed effects. The evidence supports the view that energy trade‐offs between foetal growth and maternal endocrine and brain function lead to changes in maternal cognition, and that this phenomenon is mediated by neuroendocrine mechanisms involving the hypothalamic–pituitary–adrenal axis, brainstem nucleus locus coeruleus and hippocampus.     

One big, and many small reasons that direct selection on offspring number is still open for discussion

In a recent paper, I proposed that natural selection should act to increase offspring number when diversification bet hedging is favoured. The simple underlying reasoning is that a target diversification strategy is more reliably generated with increasing sample size. The intention of opening a discussion has been realized; recent criticisms of the idea argue that selection does not act to increase offspring number when population size is large or infinite. Here I agree that criticisms have merit; indeed they are largely confined to the caveats discussed in my original paper. The critique, however, implies a verdict of outright rejection of the idea of selection on offspring number, which would be erroneous. Contrary to the assertions of the criticism, then, the importance of selection acting directly on offspring number remains an open question.     

The influence of nuptial feeding and sperm transfer on the immunological cost of reproduction in the ground cricket Allonemobius socius

Mating is often accompanied by decreased female immune function across numerous animals systems, suggesting that immune suppression is a widespread reproductive cost. However, the trade‐off between immunity and reproduction can be minimized when females have access to abundant nutrient resources. This observation suggests that the nuptial gifts provided by males in many insect systems may help to offset the common immunological cost to reproduction. In the present study, this hypothesis is tested in the ground cricket Allonemobius socius (Scudder), whose females receive a sizeable haemolymph‐based gift. Accordingly, male gift donation is controlled by covering the tibial spur (the source of the gift) of randomly chosen males with clear nail polish. The influence of sperm transfer on female immunity is disentangled from that of the nuptial gift by also examining females who fail to receive sperm during mating (spermatophore transfer has a 40% failure rate in virgin males). It is predicted that females who receive a nuptial gift will exhibit superior immune function compared with those who receive no gift. The results show that sperm transfer reduces female immune function, which is an expected immunological cost of reproduction. By contrast to the prediction, nuptial gifts do not minimize the immunological cost of reproduction in this system. Unexpectedly, the receipt of a gift appears to decrease female immune function independent of sperm transfer. The findings suggest that the nuptial gift, similar to sperm, signals the female to begin her reproductive investment, causing limited resources to be reallocated from immune function.     

Parent–offspring conflict and selection on egg size in turtles

The trade‐off between offspring size and number can present a conflict between parents and their offspring. Because egg size is constrained by clutch size, the optimal egg size for offspring fitness may not always be equivalent to that which maximizes parental fitness. We evaluated selection on egg size in three turtle species (Apalone mutica, Chelydra serpentina and Chrysemys picta) to determine if optimal egg sizes differ between offspring and their mothers. Although hatching success was generally greater for larger eggs, the strength and form of selection varied. In most cases, the egg size that maximized offspring fitness was greater than that which maximized maternal fitness. Consistent with optimality theory, mean egg sizes in the populations were more similar to the egg sizes that maximized maternal fitness, rather than offspring fitness. These results provide evidence that selection has maximized maternal fitness to achieve an optimal balance between egg size and number.     

Horn growth rate and longevity: implications for natural and artificial selection in thinhorn sheep (Ovis dalli)

We used horn measurements from natural and hunted mortalities of male thinhorn sheep Ovis dalli from Yukon Territory, Canada, to examine the relationship between rapid growth early in life and longevity. We found that rapid growth was associated with reduced longevity for sheep aged 5 years and older for both the hunted and natural mortality data sets. The negative relationship between growth rate and longevity in hunted sheep can at least partially be explained by morphologically biased hunting regulations. The same trend was evident from natural mortalities from populations that were not hunted or underwent very limited hunting, suggesting a naturally imposed mortality cost directly or indirectly associated with rapid growth. Age and growth rate were both positively associated with horn size at death for both data sets, however of the two growth rate appeared to be a better predictor. Large horn size can be achieved both by individuals that grow horns rapidly and by those that have greater longevity, and the trade-off between growth rate and longevity could limit horn size evolution in this species. The similarity in the relationship between growth rate and longevity for hunted and natural mortalities suggests that horn growth rate should not respond to artificial selection. Our study highlights the need for the existence and study of protected populations to properly assess the impacts of selective harvesting.     

Climate‐dependent costs of reproduction: Survival and fecundity costs decline with length of the growing season and summer temperature

Costs of reproduction are expected to vary with environmental conditions thus influencing selection on life‐history traits. Yet, the effects of habitat conditions and climate on trade‐offs among fitness components remain poorly understood. For 2–5 years, we quantified costs of experimentally increased reproduction in two populations (coastal long‐season vs. inland short‐season) of two long‐lived orchids that differ in natural reproductive effort (RE; 30 vs. 75% fruit set). In both species, survival costs were found only at the short‐season site, whereas growth and fecundity costs were evident at both sites, and both survival and fecundity costs declined with increasing growing season length and/or summer temperature. The results suggest that the expression of costs of reproduction depend on the local climate, and that climate warming could result in selection favouring increased RE in both study species.