Sex- and age-specific mercury accumulation in a long-lived seabird.

Mercury levels in the environment are increasing, such that they are also expected to accumulate in top-predators, but individual-based longitudinal studies required to investigate this are rare. Between 2017 and 2023, we therefore collected 1314 blood samples from 588 individual common terns (Sterna hirundo) to examine how total blood mercury concentration changed with age, and whether this differed between the sexes. Blood mercury concentrations were highly variable, but all exceeded toxicity thresholds above which adverse health effects were previously observed. A global model showed blood mercury to be higher in older birds of both sexes. Subsequent models partitioning the age effect into within- and among-individual components revealed a linear within-individual accumulation with age in females, and a decelerating within-individual accumulation with age in males. Time spent at the (particularly contaminated) breeding grounds prior to sampling, as well as egg laying in females, were also found to affect mercury concentrations. As such, our study provides evidence that male and female common terns differentially accumulate mercury in their blood as they grow older and calls for further studies of the underlying mechanisms as well as its consequences for fitness components, such as reproductive performance and survival.

Partitioning variance in a signaling trade-off under sexual selection reveals among-individual covariance in trait allocation.

Understanding the evolution of traits subject to trade-offs is challenging because phenotypes can (co)vary at both the among- and within-individual levels. Among-individual covariation indicates consistent, possibly genetic, differences in how individuals resolve the trade-off, while within-individual covariation indicates trait plasticity. There is also the potential for consistent among-individual differences in behavioral plasticity, although this has rarely been investigated. We studied the sources of (co)variance in two characteristics of an acoustic advertisement signal that trade off with one another and are under sexual selection in the gray treefrog, Hyla chrysoscelis: call duration and call rate. We recorded males on multiple nights calling spontaneously and in response to playbacks simulating different competition levels. Call duration, call rate, and their product, call effort, were all repeatable both within and across social contexts. Call duration and call rate covaried negatively, and the largest covariance was at the among-individual level. There was extensive plasticity in calling with changes in social competition, and we found some evidence for among-individual variance in call rate plasticity. The significant negative among-individual covariance in trait values is perpendicular to the primary direction of sexual selection in this species, indicating potential limits on the response to selection.

When and how can we predict adaptive responses to climate change?

Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change.

Micro-evolutionary response of spring migration timing in a wild seabird.

In the context of rapid climate change, phenological advance is a key adaptation for which evidence is accumulating across taxa. Among vertebrates, phenotypic plasticity is known to underlie most of this phenological change, while evidence for micro-evolution is very limited and challenging to obtain. In this study, we quantified phenotypic and genetic trends in timing of spring migration using 8,032 dates of arrival at the breeding grounds obtained from observations on 1,715 individual common terns (Sterna hirundo) monitored across 27 years, and tested whether these trends were consistent with predictions of a micro-evolutionary response to selection. We observed a strong phenotypic advance of 9.3 days in arrival date, of which c. 5% was accounted for by an advance in breeding values. The Breeder's equation and Robertson's Secondary Theorem of Selection predicted qualitatively similar evolutionary responses to selection, and these theoretical predictions were largely consistent with our estimated genetic pattern. Overall, our study provides rare evidence for micro-evolution underlying (part of) an adaptive response to climate change in the wild, and illustrates how a combination of adaptive micro-evolution and phenotypic plasticity facilitated a shift towards earlier spring migration in this free-living population of common terns.

What is the meta-analytic evidence for life-history trade-offs at the genetic level?

Understanding the evolutionary mechanisms underlying the maintenance of individual differences in behavior and physiology is a fundamental goal in ecology and evolution. The pace-of-life syndrome hypothesis is often invoked to explain the maintenance of such within-population variation. This hypothesis predicts that behavioral traits are part of a suite of correlated traits that collectively determine an individual's propensity to prioritize reproduction or survival. A key assumption of this hypothesis is that these traits are underpinned by genetic trade-offs among life-history traits: genetic variants that increase fertility, reproduction and growth might also reduce lifespan. We performed a systematic literature review and meta-analysis to summarize the evidence for the existence of genetic trade-offs between five key life-history traits: survival, growth rate, body size, maturation rate, and fertility. Counter to our predictions, we found an overall positive genetic correlation between survival and other life-history traits and no evidence for any genetic correlations between the non-survival life-history traits. This finding was generally consistent across pairs of life-history traits, sexes, life stages, lab vs. field studies, and narrow- vs. broad-sense correlation estimates. Our study highlights that genetic trade-offs may not be as common, or at least not as easily quantifiable, in animals as often assumed.

Rapid decline of prenatal maternal effects with age is independent of postnatal environment in a precocial bird.

Maternal effects are an important source of phenotypic variation with potentially large fitness consequences, but how their importance varies with the quality of the environment across an individual's ontogeny is poorly understood. We bred Japanese quail (Coturnix japonica) of known pedigree and experimentally manipulated the quality of the offspring diet, to estimate the importance of prenatal maternal effects in shaping variation in body mass from hatching to adulthood. Maternal genetic effects on body mass at hatching were strong, and largely caused by variation in egg mass, but their importance rapidly declined with age. Whereas there was a large effect of diet on growth, this did not affect the decline of maternal effects variance. The importance of additive genetic and residual variance increased with age, with the latter being considerably larger in the poor diet treatment. Hence, we found no evidence for prenatal maternal effect by postnatal environment interactions and that prenatal maternal effects are rapidly replaced by direct additive genetic and residual effects when offspring start to develop outside the egg. Thereby these results shed new light on the dynamics of the role of maternal versus offspring genes across ontogeny and environments.

Great tits differ in glucocorticoid plasticity in response to spring temperature.

Fluctuations in environmental temperature affect energy metabolism and stimulate the expression of reversible phenotypic plasticity in vertebrate behavioural and physiological traits. Changes in circulating concentrations of glucocorticoid hormones often underpin environmentally induced phenotypic plasticity. Ongoing climate change is predicted to increase fluctuations in environmental temperature globally, making it imperative to determine the standing phenotypic variation in glucocorticoid responses of free-living populations to evaluate their potential for coping via plastic or evolutionary changes. Using a reaction norm approach, we repeatedly sampled wild great tit (Parus major) individuals for circulating glucocorticoid concentrations during reproduction across five years to quantify individual variation in glucocorticoid plasticity along an environmental temperature gradient. As expected, baseline and stress-induced glucocorticoid concentrations increased with lower environmental temperatures at the population and within-individual level. Moreover, we provide unique evidence that individuals differ significantly in their plastic responses to the temperature gradient for both glucocorticoid traits, with some displaying greater plasticity than others. Average concentrations and degree of plasticity covaried for baseline glucocorticoids, indicating that these two reaction norm components are linked. Hence, individual variation in glucocorticoid plasticity in response to a key environmental factor exists in a wild vertebrate population, representing a crucial step to assess their potential to endure temperature fluctuations.

Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

The quantitative genetics of fitness in a wild seabird.

Additive genetic variance in fitness is a prerequisite for adaptive evolution, as a trait must be genetically correlated with fitness to evolve. Despite its relevance, additive genetic variance in fitness has not often been estimated in nature. Here, we investigate additive genetic variance in lifetime and annual fitness components in common terns (Sterna hirundo). Using 28 years of data comprising approximately 6000 pedigreed individuals, we find that additive genetic variances in the zero-inflated and Poisson components of lifetime fitness were effectively zero but estimated with high uncertainty. Similarly, additive genetic variances in adult annual reproductive success and survival did not differ from zero but were again associated with high uncertainty. Simulations suggested that we would be able to detect additive genetic variances as low as 0.05 for the zero-inflated component of fitness but not for the Poisson component, for which adequate statistical power would require approximately two more decades (four tern generations) of data collection. As such, our study suggests heritable variance in common tern fitness to be rather low if not zero, shows how studying the quantitative genetics of fitness in natural populations remains challenging, and highlights the importance of maintaining long-term individual-based studies of natural populations.

Terminology use in animal personality research: a self-report questionnaire and a systematic review.

Whether animal personality studies provide insights of broader evolutionary and ecological relevance to the field of behavioural ecology is frequently questioned. One of the sources of controversy is the vast, but often vague terminology present in the field. From a statistical perspective, animal personality is defined as among-individual variance in behaviour. However, numerous conceptual definitions of animal personality are available in the literature. Here, we performed (i) a self-report questionnaire and (ii) a systematic literature review to quantify how researchers interpreted conceptual and statistical definitions commonly used in animal personality research. We also compared whether data obtained from the questionnaire matched with data from the literature review. Among the 430 self-reported researchers that participated in our questionnaire, we observed discrepancies in key questions such as the conceptual definition of animal personality or the interpretation of repeatability. Furthermore, our literature review generally confirmed the global patterns revealed by the questionnaire. Overall, we identified common disagreements within the field of animal personality and discussed potential solutions. We advocate for adopting a terminology that avoids ambiguous interpretations and helps to make more explicit the widespread connotations implicit in the label 'animal personality'.

Telomere length is heritable and genetically correlated with lifespan in a wild bird.

Telomeres are protective caps at the end of eukaryotic chromosomes that shorten with age and in response to stressful or resource-demanding conditions. Their length predicts individual health and lifespan across a wide range of animals, but whether the observed positive association between telomere length and lifespan is environmentally induced, or set at conception due to a shared genetic basis, has not been tested in wild animals. We applied quantitative genetic "animal models" to longitudinal telomere measurements collected over a 10-year period from individuals of a wild seabird (common tern; Sterna hirundo) with known pedigree. We found no variation in telomere shortening with age among individuals at the phenotypic and genetic level, and only a small permanent environmental effect on adult telomere length. Instead, we found telomere length to be highly heritable and strongly positively genetically correlated with lifespan. Such heritable differences between individuals that are set at conception may present a hitherto underappreciated component of variation in somatic state.

Immunosenescence in the wild? A longitudinal study in a long-lived seabird.

Longitudinal studies of various vertebrate populations have demonstrated senescent declines in reproductive performance and survival probability to be almost ubiquitous. Longitudinal studies of potential underlying proximate mechanisms, however, are still scarce. Due to its critical function in the maintenance of health and viability, the immune system is among the potential (mediators of) proximate mechanisms that could underlie senescence. Here, we studied three innate immune parameters-haemagglutination titre, haemolysis titre and haptoglobin concentration-in a population of common terns (Sterna hirundo) known to undergo actuarial senescence. We repeatedly sampled birds of known sex and age across 11 years and used random regression models to (a) quantify how immune parameters vary among individuals and (b) describe within-individual age-specific changes in, and potential trade-offs between, immune parameters. Our models revealed no differences between males and females in haemagglutination titre and haptoglobin concentration, and very low among-individual variation in these parameters in general. Within individuals, haemagglutination titre increased with age, while haptoglobin concentration did not change. We found no indication for selective (dis)appearance in relation to haemagglutination titre or haptoglobin concentration, nor for the existence of a trade-off between them. Haemolysis was absent in the majority (76%) of samples. Common terns do not exhibit clear senescence in haemagglutination titre and haptoglobin concentration and show very little among-individual variation in these parameters in general. This may be explained by canalisation of the immune parameters or by the colonial breeding behaviour of our study species, but more longitudinal studies are needed to facilitate investigation of links between species' characteristics and immunosenescence in wild animals.

Sexual selection moderates heat stress response in males and females.

A widespread effect of climate change is the displacement of organisms from their thermal optima. The associated thermal stress imposed by climate change has been argued to have a particularly strong impact on male reproduction but evidence for this postulated sex-specific stress response is equivocal.One important factor that may explain intra- and interspecific variation in stress responses is sexual selection, which is predicted to magnify negative effects of stress. Nevertheless, empirical studies exploring the interplay of sexual selection and heat stress are still scarce.We tested experimentally for an interaction between sexual selection and thermal stress in the red flour beetle Tribolium castaneum by contrasting heat responses in male and female reproductive success between enforced monogamy and polygamy.We found that polygamy magnifies detrimental effects of heat stress in males but relaxes the observed negative effects in females. Our results suggest that sexual selection can reverse sex differences in thermal sensitivity, and may therefore alter sex-specific selection on alleles associated with heat tolerance.Assuming that sexual selection and natural selection are aligned to favour the same genetic variants under environmental stress, our findings support the idea that sexual selection on males may promote the adaptation to current global warming. Read the free Plain Language Summary for this article on the Journal blog.

Stronger net selection on males across animals.

Sexual selection is considered the major driver for the evolution of sex differences. However, the eco-evolutionary dynamics of sexual selection and their role for a population's adaptive potential to respond to environmental change have only recently been explored. Theory predicts that sexual selection promotes adaptation at a low demographic cost only if sexual selection is aligned with natural selection and if net selection is stronger on males compared to females. We used a comparative approach to show that net selection is indeed stronger in males and provide preliminary support that this sex bias is associated with sexual selection. Given that both sexes share the vast majority of their genes, our findings corroborate the notion that the genome is often confronted with a more stressful environment when expressed in males. Collectively, our study supports one of the long-standing key assumptions required for sexual selection to bolster adaptation, and sexual selection may therefore enable some species to track environmental change more efficiently.

Integrating Behavior in Life-History Theory: Allocation versus Acquisition?

Central theories explaining the maintenance of individual differences in behavior build on the assumption that behavior mediates life-history trade-offs between current and future reproduction. However, current empirical evidence does not robustly support this assumption. This mismatch might be because current theory is not clear about the role of behavior in individual allocation versus acquisition of resources, hindering empirical testing. The relative importance of allocation compared to acquisition is a key feature of classic life-history theory, but appears to have been lost in translation in recent developments of life-history theory involving behavior. We argue that determining the relative balance between variation in resource allocation and acquisition, and the role of behavior in this process, will help to build more robust and precise predictions.

Understanding the Social Dynamics of Breeding Phenology: Indirect Genetic Effects and Assortative Mating in a Long-Distance Migrant.

AbstractPhenological traits, such as the timing of reproduction, are often influenced by social interactions between paired individuals. Such partner effects may occur when pair members affect each other's prebreeding environment. Partner effects can be environmentally and/or genetically determined, and quantifying direct and indirect genetic effects is important for understanding the evolutionary dynamics of phenological traits. Here, using 26 years of data from a pedigreed population of a migratory seabird, the common tern (Sterna hirundo), we investigate male and female effects on female laying date. We find that female laying date harbors both genetic and environmental variation and is additionally influenced by the environmental and, to a lesser extent, genetic component of its mate. We demonstrate this partner effect to be largely explained by male arrival date. Interestingly, analyses of mating patterns with respect to arrival date show mating to be strongly assortative, and using simulations we show that assortative mating leads to overestimation of partner effects. Our study provides evidence for partner effects on breeding phenology in a long-distance migrant while uncovering the potential causal pathways underlying the observed effects and raising awareness for confounding effects resulting from assortative mating or other common environmental effects.

Individual differences in behaviour explain variation in survival: a meta-analysis.

Research focusing on among-individual differences in behaviour ('animal personality') has been blooming for over a decade. Central theories explaining the maintenance of such behavioural variation posits that individuals expressing greater "risky" behaviours should suffer higher mortality. Here, for the first time, we synthesize the existing empirical evidence for this key prediction. Our results did not support this prediction as there was no directional relationship between riskier behaviour and greater mortality; however there was a significant absolute relationship between behaviour and survival. In total, behaviour explained a significant, but small, portion (5.8%) of the variance in survival. We also found that risky (vs. "shy") behavioural types live significantly longer in the wild, but not in the laboratory. This suggests that individuals expressing risky behaviours might be of overall higher quality but the lack of predation pressure and resource restrictions mask this effect in laboratory environments. Our work demonstrates that individual differences in behaviour explain important differences in survival but not in the direction predicted by theory. Importantly, this suggests that models predicting behaviour to be a mediator of reproduction-survival trade-offs may need revision and/or empiricists may need to reconsider their proxies of risky behaviours when testing such theory.

Individual variation in age-dependent reproduction: Fast explorers live fast but senesce young?

Adaptive integration of life history and behaviour is expected to result in variation in the pace-of-life. Previous work focused on whether 'risky' phenotypes live fast but die young, but reported conflicting support. We posit that individuals exhibiting risky phenotypes may alternatively invest heavily in early-life reproduction but consequently suffer greater reproductive senescence. We used a 7-year longitudinal dataset with >1,200 breeding records of >800 female great tits assayed annually for exploratory behaviour to test whether within-individual age dependency of reproduction varied with exploratory behaviour. We controlled for biasing effects of selective (dis)appearance and within-individual behavioural plasticity. Slower and faster explorers produced moderate-sized clutches when young; faster explorers subsequently showed an increase in clutch size that diminished with age (with moderate support for declines when old), whereas slower explorers produced moderate-sized clutches throughout their lives. There was some evidence that the same pattern characterized annual fledgling success, if so, unpredictable environmental effects diluted personality-related differences in this downstream reproductive trait. Support for age-related selective appearance was apparent, but only when failing to appreciate within-individual plasticity in reproduction and behaviour. Our study identifies within-individual age-dependent reproduction, and reproductive senescence, as key components of life-history strategies that vary between individuals differing in risky behaviour. Future research should thus incorporate age-dependent reproduction in pace-of-life studies.

To eat and not be eaten: diurnal mass gain and foraging strategies in wintering great tits.

Adaptive theory predicts that the fundamental trade-off between starvation and predation risk shapes diurnal patterns in foraging activity and mass gain in wintering passerine birds. Foragers mitigating both types of risk should exhibit a bimodal distribution (increased foraging and mass gain early and late in the day), whereas both foraging and mass gains early (versus late) during the day are expected when the risk of starvation (versus predation) is greatest. Finally, relatively constant rates of foraging and mass gain should occur when the starvation-predation risk trade-off is independent of body mass. Using automated feeders with integrated digital balances, we estimated diurnal patterns in foraging and body mass gain to test which ecological scenario was best supported in wintering great tits Parus major Based on data of 40 consecutive winter days recording over 12 000 body masses of 28 individuals, we concluded that birds foraged and gained mass early during the day, as predicted by theory when the starvation-predation risk trade-off is mass-dependent and starvation risk outweighs predation risk. Slower explorers visited the feeders more often, and decreased their activity along the day more strongly, compared with faster explorers, thereby explaining a major portion of the individual differences in diurnal patterning of foraging activity detected using random regression analyses. Birds did not differ in body mass gain trajectories, implying both that individuals differed in the usage of feeders, and that unbiased conclusions regarding how birds resolve starvation-predation risk trade-off require the simultaneous recording of foraging activity and body mass gain trajectories. Our study thereby provides the first unambiguous demonstration that individual birds are capable of adjusting their diurnal foraging and mass gain trajectories in response to ecological predictors of starvation risk as predicted by starvation-predation risk trade-off theory.

Effect of ursodeoxycholic acid treatment on the altered progesterone and bile acid homeostasis in the mother-placenta-foetus trio during cholestasis of pregnancy.

AIM: Intrahepatic cholestasis of pregnancy (ICP) is characterized by pruritus and elevated bile acid concentrations in maternal serum. This is accompanied by an enhanced risk of intra-uterine and perinatal complications. High concentrations of sulphated progesterone metabolites (PMS) have been suggested to be involved in the multifactorial aetiopathogenesis of ICP. The aim of this study was to investigate further the mechanism accounting for the beneficial effect of oral administration of ursodeoxycholic acid (UDCA), which is the standard treatment, regarding bile acid and PMS homeostasis in the mother-placenta-foetus trio. METHOD: Using HPLC-MS/MS bile acids and PMS were determined in maternal and foetal serum and placenta. The expression of ABC proteins in placenta was determined by real time quantitative PCR (RT-QPCR) and immunofluorescence. RESULTS: In ICP, markedly increased concentrations of bile acids (tauroconjugates > glycoconjugates >> unconjugated), progesterone and PMS in placenta and maternal serum were accompanied by enhanced concentrations in foetal serum of bile acids, but not of PMS. UDCA treatment reduced bile acid accumulation in the mother-placenta-foetus trio, but had no significant effect on progesterone and PMS concentrations. ABCG2 mRNA abundance was increased in placentas from ICP patients vs. controls and remained stable following UDCA treatment, despite an apparent further increase in ABCG2. CONCLUSION: UDCA administration partially reduces ICP-induced bile acid accumulation in mothers and foetuses despite the lack of effect on concentrations of progesterone and PMS in maternal serum. Up-regulation of placental ABCG2 may play an important role in protecting the foetus from high concentrations of bile acids and PMS during ICP.