Lizards from warm and declining populations are born with extremely short telomeres.

Aging is the price to pay for acquiring and processing energy through cellular activity and life history productivity. Climate warming can exacerbate the inherent pace of aging, as illustrated by a faster erosion of protective telomere DNA sequences. This biomarker integrates individual pace of life and parental effects through the germline, but whether intra- and intergenerational telomere dynamics underlies population trends remains an open question. Here, we investigated the covariation between life history, telomere length (TL), and extinction risk among three age classes in a cold-adapted ectotherm (Zootoca vivipara) facing warming-induced extirpations in its distribution limits. TL followed the same threshold relationships with population extinction risk at birth, maturity, and adulthood, suggesting intergenerational accumulation of accelerated aging rate in declining populations. In dwindling populations, most neonates inherited already short telomeres, suggesting they were born physiologically old and unlikely to reach recruitment. At adulthood, TL further explained females' reproductive performance, switching from an index of individual quality in stable populations to a biomarker of reproductive costs in those close to extirpation. We compiled these results to propose the aging loop hypothesis and conceptualize how climate-driven telomere shortening in ectotherms may accumulate across generations and generate tipping points before local extirpation.

Agricultural intensification alters marbled newt genetic diversity and gene flow through density and dispersal reduction.

Recent agricultural intensification threatens global biodiversity with amphibians being one of the most impacted groups. Because of their biphasic life cycle, amphibians are particularly vulnerable to habitat loss and fragmentation that often result in small, isolated populations and loss of genetic diversity. Here, we studied how landscape heterogeneity affects genetic diversity, gene flow and demographic parameters in the marbled newt, Triturus marmoratus, over a hedgerow network landscape in Western France. While the northern part of the study area consists of preserved hedged farmland, the southern part was more profoundly converted for intensive arable crops production after WWII. Based on 67 sampled ponds and 10 microsatellite loci, we characterized regional population genetic structure and evaluated the correlation between landscape variables and (i) local genetic diversity using mixed models and (ii) genetic distance using multiple regression methods and commonality analysis. We identified a single genetic population characterized by a spatially heterogeneous isolation-by-distance pattern. Pond density in the surrounding landscape positively affected local genetic diversity while arable crop land cover negatively affected gene flow and connectivity. We used demographic inferences to quantitatively assess differences in effective population density and dispersal between the contrasted landscapes characterizing the northern and southern parts of the study area. Altogether, results suggest recent land conversion affected T. marmoratus through reduction in both effective population density and dispersal due to habitat loss and reduced connectivity.

Fish from urban rivers and with high pollutant levels have shorter telomeres.

Environmental pressures, such as urbanization and exposure to pollutants may jeopardize survival of free-living animals. Yet, much remains to be known about physiological and ecological responses to currently-released pollutants, especially in wild vertebrate ectotherms. We tested the effect of urbanization and pollution (phthalates, organochlorine and pyrethroid pesticides, polychlorobiphenyls, polybromodiphenylethers, polycyclic aromatic hydrocarbons, and some of their metabolites) on telomere length, a suggested biomarker of life expectancy, in the European chub, Squalius cephalus, from urban and agricultural rivers of the Marne hydrographic network, France. We showed that telomere length was reduced in chub from urban rivers. Moreover, among the wide range of anthropogenic contaminants investigated, high levels of phthalate metabolites in liver were associated with shorter telomeres. This study suggests that urbanization and chemical pollution may compromise survival of wild fish, by accelerating telomere attrition.

Relationships between avian malaria resilience and corticosterone, testosterone and prolactin in a Hawaiian songbird.

Glucocorticoids, androgens, and prolactin regulate metabolism and reproduction, but they also play critical roles in immunomodulation. Since the introduction of avian malaria to Hawaii a century ago, low elevation populations of the Hawaii Amakihi (Chlorodrepanis virens) that have experienced strong selection by avian malaria have evolved increased resilience (the ability to recover from infection), while high elevation populations that have undergone weak selection remain less resilient. We investigated how variation in malaria selection has affected corticosterone, testosterone, and prolactin hormone levels in Amakihi during the breeding season. We predicted that baseline corticosterone and testosterone (which have immunosuppressive functions) would be reduced in low elevation and malaria-infected birds, while stress-induced corticosterone and prolactin (which have immunostimulatory functions) would be greater in low elevation and malaria-infected birds. As predicted, prolactin was significantly higher in malaria-infected than uninfected females (although more robust sample sizes would help to confirm this relationship), while testosterone trended higher in malaria-infected than uninfected males and, surprisingly, neither baseline nor stress-induced CORT varied with malaria infection. Contrary to our predictions, stress-induced corticosterone was significantly lower in low than high elevation birds while testosterone in males and prolactin in females did not vary by elevation, suggesting that Amakihi hormone modulation across elevation is determined by variables other than disease selection (e.g., timing of breeding, energetic challenges). Our results shed new light on relationships between introduced disease and hormone modulation, and they raise new questions that could be explored in experimental settings.

Parasitism reduces oxidative stress of fish host experimentally exposed to PAHs.

Some parasites are known to bioaccumulate some environmental pollutants within their host. We hypothesized that these parasites may be beneficial for their hosts in polluted environments. We experimentally increased long-term (five weeks) exposure to polycyclic aromatic hydrocarbons (PAHs, three levels: 0.1X, 1X, 10X environmental exposure) in European chubs (Squalius cephalus) that were naturally infected or uninfected with acanthocephalan parasites. We monitored PAHs levels in fish tissues, as well as oxidative stress, telomere length and condition indices. Although parasite infection did not significantly reduce the levels of PAHs and PAH metabolites in host tissues, host oxidative status was explained by parasitism and pollution levels. Oxidative damage increased with parasitism in fish exposed to low PAH levels (0.1X) but decreased in infected fish at higher PAH exposure (10X), thus corroborating our hypothesis. Meanwhile, antioxidant capacity did not differ in response to parasite infection nor PAHs exposure. Despite this imbalance in oxidative status, experimental increase in PAH levels did not compromise telomere length, body condition, or survival in infected and uninfected fish. This study provides the first experimental evidence that the outcome of host-parasite interactions can shift from negative to positive as pollutant exposure increases.

Chronic water restriction triggers sex-specific oxidative stress and telomere shortening in lizards.

Animals use a variety of strategies to avoid acute dehydration and death. Yet, how chronic exposure to sub-lethal dehydration may entail physiological and fitness costs remains elusive. In this study, we experimentally tested if water restriction causes increased oxidative stress (OS) and telomere length (TL) shortening, two well-described mediators of environment-fitness relationships. We exposed 100 yearling female and male common lizards (Zootoca vivipara) either to a 51-day period of water restriction or to water ad libitum, followed by 45 days in common garden outdoor conditions. We measured the kinetic changes in OS and TL and found that water-restricted males had enhanced antioxidant defences and decreased oxidative damage at day 36, whereas females did not immediately respond. A month and a half after water restriction, both sexes experienced a drop in antioxidant capacity but only males exhibited significant TL shortening. In the following 3 years, we found that lizards with longer initial TL and those who maintained stronger antioxidant defences experienced higher longevity, irrespective of sex and water restriction. Together, these results unravelled sex-specific responses to water restriction, with potential applications in better understanding the physiological costs of increasing summer droughts as a result of global climate change.

Exposure to PFAS is Associated with Telomere Length Dynamics and Demographic Responses of an Arctic Top Predator.

Environmental factors that can influence telomeres are diverse, but the association between telomeres and exposure to environmental contaminants is yet to be elucidated. To date, prior studies have focused on legacy persistent chlorinated pollutants (POPs), while the effects of poly- and perfluoroalkyl substances (PFAS) have been poorly documented. Here, we investigated the associations among PFAS congeners, absolute telomere length (cross-sectional approach), and telomere dynamics (rate of telomere length change over time, longitudinal approach) in one of the most contaminated arctic top predators, the glaucous gull Larus hyperboreus from Svalbard. We further estimated the effect of PFAS on apparent survival rates and re-sighting probabilities using a 10-year capture/recapture dataset (2010-2019). We found that birds exposed to higher concentrations of perfluorononadecanoate (PFNA) (median of 1565 pg/mL of ww in males and 1370 pg/mL of ww in females) and perfluorotetradecanoate (PFTeDA) (median of 370 pg/mL of ww in males and 210 pg/mL of ww in females) showed the slowest rate of telomere shortening. We also found that high blood concentrations of perfluorooctanoate (PFOA) (median of 120 pg/mL of ww in males and 150 pg/mL of ww in females) and perfluorohexanesulfonate (PFHxS) (median of 495 pg/mL of ww in males and 395 pg/mL of ww in females) were positively associated with higher re-sighting probabilities and apparent survival in males but not in females. Our work is the first to report an association between single PFAS compounds and telomeres, and the first to link PFAS exposure with survival probabilities, suggesting that the effect of PFAS exposure might be more tied to the type of compound rather than the total concentration of PFAS.

Traffic noise exposure affects telomere length in nestling house sparrows.

In a consistently urbanizing world, anthropogenic noise has become almost omnipresent, and there are increasing evidence that high noise levels can have major impacts on wildlife. While the effects of anthropogenic noise exposure on adult animals have been widely studied, surprisingly, there has been little consideration of the effects of noise pollution on developing organisms. Yet, environmental conditions experienced in early life can have dramatic lifelong consequences for fitness. Here, we experimentally manipulated the acoustic environment of free-living house sparrows (Passer domesticus) breeding in nest boxes. We focused on the impact of such disturbance on nestlings' telomere length and fledging success, as telomeres (the protective ends of chromosomes) appear to be a promising predictor of longevity. We showed that despite the absence of any obvious immediate consequences (growth and fledging success), nestlings reared under traffic noise exposure exhibited reduced telomere lengths compared with their unexposed neighbours. Although the mechanisms responsible for this effect remain to be determined, our results provide the first experimental evidence that noise alone can affect a wild vertebrate's early-life telomere length. This suggests that noise exposure may entail important costs for developing organisms.

Warmer incubation temperatures and later lay-orders lead to shorter telomere lengths in wood duck (Aix sponsa) ducklings.

The environment that animals experience during development shapes phenotypic expression. In birds, two important aspects of the early-developmental environment are lay-order sequence and incubation. Later-laid eggs tend to produce weaker offspring, sometimes with compensatory mechanisms to accelerate their growth rate to catch-up to their siblings. Further, small decreases in incubation temperature slow down embryonic growth rates and lead to wide-ranging negative effects on many posthatch traits. Recently, telomeres, noncoding DNA sequences at the end of chromosomes, have been recognized as a potential proxy for fitness because longer telomeres are positively related to lifespan and individual quality in many animals, including birds. Although telomeres appear to be mechanistically linked to growth rate, little is known about how incubation temperature and lay-order may influence telomere length. We incubated wood duck (Aix sponsa) eggs at two ecologically-relevant temperatures (34.9°C and 36.2°C) and measured telomere length at hatch and 1 week after. We found that ducklings incubated at the lower temperature had longer telomeres than those incubated at the higher temperature both at hatch and 1 week later. Further, we found that later-laid eggs produced ducklings with shorter telomeres than those laid early in the lay-sequence, although lay-order was not related to embryonic developmental rate. This study contributes to our broader understanding of how parental effects can affect telomere length early in life. More work is needed to determine if these effects on telomere length persist until adulthood, and if they are associated with effects on fitness in this precocial species.

Environmental Drivers of Growth and Oxidative Status during Early Life in a Long-Lived Antarctic Seabird, the Adélie Penguin.

AbstractIn vertebrates, developmental conditions can have long-term effects on individual performance. It is increasingly recognized that oxidative stress could be one physiological mechanism connecting early-life experience to adult phenotype. Accordingly, markers of oxidative status could be useful for assessing the developmental constraints encountered by offspring. Although some studies have demonstrated that developmental constraints are associated with high levels of oxidative stress in offspring, it remains unclear how growth, parental behavior, and brood competition may altogether affect oxidative stress in long-lived species in the wild. Here, we investigated this question in a long-lived Antarctic bird species by testing the impact of brood competition (e.g., brood size and hatching order) on body mass and on two markers of oxidative damage in Adélie penguin chicks. We also examined the influence of parental effort (i.e., foraging trip duration) and parental body condition on chick body mass and oxidative damage. First, we found that brood competition and parental traits had significant impacts on chick body mass. Second, we found that chick age and, to a lesser extent, chick body mass were two strong determinants of the levels of oxidative damage in Adélie penguin chicks. Finally, and importantly, we also found that brood competition significantly increased the levels of one marker of oxidative damage and was associated with a lower survival probability. However, parental effort and parental condition were not significantly linked to chick levels of oxidative damage. Overall, our study demonstrates that sibling competition can generate an oxidative cost even for this long-lived Antarctic species with a limited brood size (maximum of two chicks).

Carryover effects of winter mercury contamination on summer concentrations and reproductive performance in little auks.

Many animals migrate after reproduction to respond to seasonal environmental changes. Environmental conditions experienced on non-breeding sites can have carryover effects on fitness. Exposure to harmful chemicals can vary widely between breeding and non-breeding grounds, but its carryover effects are poorly studied. Mercury (Hg) contamination is a major concern in the Arctic. Here, we quantified winter Hg contamination and its carryover effects in the most abundant Arctic seabird, the little auk Alle alle. Winter Hg contamination of birds from an East Greenland population was inferred from head feather concentrations. Birds tracked with Global Location Sensors (GLS, N = 28 of the total 92) spent the winter in western and central North Atlantic waters and had increasing head feather Hg concentrations with increasing longitude (i.e., eastward). This spatial pattern was not predicted by environmental variables such as bathymetry, sea-surface temperature or productivity, and needs further investigation. Hg concentrations in head feathers and blood were strongly correlated, suggesting a carryover effect of adult winter contamination on the consequent summer concentrations. Head feather Hg concentrations had no clear association with telomere length, a robust fitness indicator. In contrast, carryover negative effects were detected on chick health, as parental Hg contamination in winter was associated with decreasing growth rate of chicks in summer. Head feather Hg concentrations of females were not associated with egg membrane Hg concentrations, or with egg volume. In addition, parental winter Hg contamination was not related to Hg burdens in chicks' body feathers. Therefore, we hypothesise that the association between parental winter Hg exposure and the growth of their chick results from an Hg-related decrease in parental care, and needs further empirical evidence. Our results stress the need of considering parental contamination on non-breeding sites to understand Hg trans-generational effects in migrating seabirds, even at low concentrations.

Aminomethylphosphonic acid (AMPA) alters oxidative status during embryonic development in an amphibian species.

Glyphosate's primary metabolite (aminomethylphosphonic acid, AMPA) is known to alter embryonic development at environmentally relevant concentrations in amphibians. However, we have limited understanding of the physiological mechanisms through which AMPA affects organisms. In this study, we tested whether alteration of the oxidative status is one mechanism through which AMPA affects organism performance. To this end, we analysed several oxidative status markers in hatchling tadpoles that were exposed to sublethal concentrations of AMPA during embryonic development (~16 days). We compared the influence of environmentally relevant concentrations of AMPA (from 0.07 to 3.57 µg l-1) on the relation between developmental traits (i.e, embryonic development duration, embryonic mortality and hatchling size) and oxidative status markers known to alter homeostasis when unbalanced (superoxide dismutase (SOD), glutathione peroxidase (GPx), catalase (CAT), thiols and ratios thereof). We included measures of telomere length as an indicator of physiological state. We found that AMPA concentrations induce non-monotonic effects on some oxidative status markers with hatchlings displaying elevated antioxidant responses (elevated thiols and unbalanced SOD/(GPx + CAT) ratio). The lack of effect of AMPA on the relation between developmental traits, oxidative status and telomere length suggests that selective mortality of embryos susceptible to oxidative stress may have occurred prior to hatching in individuals less resistant to AMPA which display lower hatching success. Future studies are required to disentangle whether oxidative unbalance is a cause or a consequence of AMPA exposition. This study highlights the need to investigate effects of the metabolites of contaminants at environmental concentrations to comprehensively assess impacts of anthropogenic contamination on wildlife.

Sea surface temperature, rather than land mass or geographic distance, may drive genetic differentiation in a species complex of highly dispersive seabirds.

Seabirds, particularly Procellariiformes, are highly mobile organisms with a great capacity for long dispersal, though simultaneously showing high philopatry, two conflicting life-history traits that may lead to contrasted patterns of genetic population structure. Landmasses were suggested to explain differentiation patterns observed in seabirds, but philopatry, isolation by distance, segregation between breeding and nonbreeding zones, and oceanographic conditions (sea surface temperatures) may also contribute to differentiation patterns. To our knowledge, no study has simultaneously contrasted the multiple factors contributing to the diversification of seabird species, especially in the gray zone of speciation. We conducted a multilocus phylogeographic study on a widespread seabird species complex, the little shearwater complex, showing highly homogeneous morphology, which led to considerable taxonomic debate. We sequenced three mitochondrial and six nuclear markers on all extant populations from the Atlantic (lherminieri) and Indian Oceans (bailloni), that is, five nominal lineages from 13 populations, along with one population from the eastern Pacific Ocean (representing the dichrous lineage). We found sharp differentiation among populations separated by the African continent with both mitochondrial and nuclear markers, while only mitochondrial markers allowed characterizing the five nominal lineages. No differentiation could be detected within these five lineages, questioning the strong level of philopatry showed by these shearwaters. Finally, we propose that Atlantic populations likely originated from the Indian Ocean. Within the Atlantic, a stepping-stone process accounts for the current distribution. Based on our divergence time estimates, we suggest that the observed pattern of differentiation mostly resulted from historical and current variation in sea surface temperatures.

Physiological and morphological correlates of blood parasite infection in urban and non-urban house sparrow populations.

In the last decade, house sparrow populations have shown a general decline, especially in cities. Avian malaria has been recently suggested as one of the potential causes of this decline, and its detrimental effects could be exacerbated in urban habitats. It was initially thought that avian malaria parasites would not have large negative effects on wild birds because of their long co-evolution with their hosts. However, it is now well-documented that they can have detrimental effects at both the primo- and chronical infection stages. In this study, we examined avian malaria infection and its physiological and morphological consequences in four populations of wild house sparrows (2 urban and 2 rural). We did not find any relationship between the proportions of infected individuals and the urbanisation score calculated for our populations. However, we observed that the proportion of infected individuals increased during the course of the season, and that juveniles were less infected than adults. We did not detect a strong effect of malaria infection on physiological, morphological and condition indexes. Complex parasite dynamics and the presence of confounding factors could have masked the potential effects of infection. Thus, longitudinal and experimental studies are needed to understand the evolutionary ecology of this very common, but still poorly understood, wild bird parasite.

Direct and indirect effects of multiple environmental stressors on fish health in human-altered rivers.

Freshwater fish face multiple challenges in human-altered rivers such as trace metal contamination, temperature increase and parasitism. These multiple stressors could have unexpected interactive effects on fish health due to shared physiological pathways, but few studies investigated this question in wild fish populations. In this study, we compared 16 populations of gudgeon (Gobio occitaniae) distributed along perturbation gradients in human-altered rivers in the South of France. We tested the effects of single and combined stressors (i.e., metal contamination, temperature, parasitism) on key traits linked to fish health across different biological levels using a Structural Equation Modelling approach. Parasitism and temperature alone had limited deleterious effects on fish health. In contrast, fish living in metal-contaminated sites had higher metal bioaccumulation and higher levels of cellular damage in the liver through the induction of an inflammatory response. In addition, temperature and contamination had interactive negative effects on growth. These results suggest that trace metal contamination has deleterious effects on fish health at environmentally realistic concentrations and that temperature can modulate the effects of trace metals on fish growth. With this study, we hope to encourage integrative approaches in realistic field conditions to better predict the effects of natural and anthropogenic stressors on aquatic organisms.