Adaptive Maternal Effects Shape Offspring Phenotype and Survival in Natal Environments.

AbstractMaternal effects can give newborns a head start in life by adjusting natal phenotypes to natal environments, yet their strength and adaptiveness are often difficult to investigate in natural populations. Here, we studied anticipatory maternal effects and their adaptiveness in common lizards in a seminatural experimental system. Specifically, we investigated how maternal environments (i.e., vegetation cover) and maternal phenotype (i.e., activity levels and body length) can shape offspring phenotype. We further studied whether such maternal effects influenced offspring survival in natal environments varying with respect to vegetation cover, conspecific density, and, consequently, maternal fitness. More active females from dense vegetation habitats produced bigger offspring than their less active counterparts, the contrary being true for sparse vegetation habitats. Moreover, females from dense vegetation habitats produced more active offspring and more active offspring survived better in dense vegetation habitats, resulting in greater maternal fitness through maternal effects. These results suggest adaptive anticipatory maternal effects, induced by vegetation structure and mediated by activity levels that may shape early-life prospects in natal environments.

Diet contributes to urban-induced alterations in gut microbiota: experimental evidence from a wild passerine.

Urban sprawl increasingly affects the ecology of natural populations, including host-microbiota interactions, with observed differences in the gut microbiota between urban and rural hosts. While different mechanisms could explain this pattern, dietary uptake constitutes a likely candidate. To assess the contribution of diet in explaining urban-rural variation in gut microbiota, we performed an aviary experiment in which urban and rural house sparrows were fed with mimics of urban or rural diets. Before the experiment, rural sparrows hosted more diverse gut communities, with a higher relative abundance of Enterococcaceae and Staphylococcaceae and lower abundance of genes involved in xenobiotic degradation and lipid metabolism than their urban counterparts. The experimental diets significantly altered gut microbiota α- and ß-diversity and taxonomic composition, with the strongest shifts occurring in individuals exposed to contrasting diets. Overall, diet-induced shifts resembled initial differences between free-ranging urban and rural hosts. Furthermore, rural diet had a positive impact on urban host body mass but only in hosts with the highest initial gut diversity. Overall, our results indicate that diet constitutes an important factor contributing to differences in gut microbiota along the urbanization gradient and provide new insights on possible fitness consequences of a reduced gut diversity in urban settings.

Altered trophic interactions in warming climates: consequences for predator diet breadth and fitness.

Species interactions are central in predicting the impairment of biodiversity with climate change. Trophic interactions may be altered through climate-dependent changes in either predator food preferences or prey communities. Yet, climate change impacts on predator diet remain surprisingly poorly understood. We experimentally studied the consequences of 2°C warmer climatic conditions on the trophic niche of a generalist lizard predator. We used a system of semi-natural mesocosms housing a variety of invertebrate species and in which climatic conditions were manipulated. Lizards in warmer climatic conditions ate at a greater predatory to phytophagous invertebrate ratio and had smaller individual dietary breadths. These shifts mainly arose from direct impacts of climate on lizard diets rather than from changes in prey communities. Dietary changes were associated with negative changes in fitness-related traits (body condition, gut microbiota) and survival. We demonstrate that climate change alters trophic interactions through top-predator dietary shifts, which might disrupt eco-evolutionary dynamics.

Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change.

Evidence has accumulated in recent decades on the drastic impact of climate change on biodiversity. Warming temperatures have induced changes in species physiology, phenology, and have decreased body size. Such modifications can impact population dynamics and could lead to changes in life cycle and demography. More specifically, conceptual frameworks predict that global warming will severely threaten tropical ectotherms while temperate ectotherms should resist or even benefit from higher temperatures. However, experimental studies measuring the impacts of future warming trends on temperate ectotherms' life cycle and population persistence are lacking. Here we investigate the impacts of future climates on a model vertebrate ectotherm species using a large-scale warming experiment. We manipulated climatic conditions in 18 seminatural populations over two years to obtain a present climate treatment and a warm climate treatment matching IPCC predictions for future climate. Warmer temperatures caused a faster body growth, an earlier reproductive onset, and an increased voltinism, leading to a highly accelerated life cycle but also to a decrease in adult survival. A matrix population model predicts that warm climate populations in our experiment should go extinct in around 20 y. Comparing our experimental climatic conditions to conditions encountered by populations across Europe, we suggest that warming climates should threaten a significant number of populations at the southern range of the distribution. Our findings stress the importance of experimental approaches on the entire life cycle to more accurately predict population and species persistence in future climates.

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal.

Predation is a strong selective pressure generating morphological, physiological and behavioural responses in organisms. As predation risk is often higher during juvenile stages, antipredator defences expressed early in life are paramount to survival. Maternal effects are an efficient pathway to produce such defences. We investigated whether maternal exposure to predator cues during gestation affected juvenile morphology, behaviour and dispersal in common lizards (Zootoca vivipara). We exposed 21 gravid females to saurophagous snake cues for one month while 21 females remained unexposed (i.e. control). We measured body size, preferred temperature and activity level for each neonate, and released them into semi-natural enclosures connected to corridors in order to measure dispersal. Offspring from exposed mothers grew longer tails, selected lower temperatures and dispersed thrice more than offspring from unexposed mothers. Because both tail autotomy and altered thermoregulatory behaviour are common antipredator tactics in lizards, these results suggest that mothers adjusted offspring phenotype to risky natal environments (tail length) or increased risk avoidance (dispersal). Although maternal effects can be passive consequences of maternal stress, our results strongly militate for them to be an adaptive antipredator response that may increase offspring survival prospects.

Dynamics of Gut Microbiota Diversity During the Early Development of an Avian Host: Evidence From a Cross-Foster Experiment.

Despite the increasing knowledge on the processes involved in the acquisition and development of the gut microbiota in model organisms, the factors influencing early microbiota successions in natural populations remain poorly understood. In particular, little is known on the role of the rearing environment in the establishment of the gut microbiota in wild birds. Here, we examined the influence of the nesting environment on the gut microbiota of Great tits (Parus major) by performing a partial cross-fostering experiment during the intermediate stage of nestling development. We found that the cloacal microbiota of great tit nestlings underwent substantial changes between 8 and 15 days of age, with a strong decrease in diversity, an increase in the relative abundance of Firmicutes and a shift in the functional features of the community. Second, the nesting environment significantly influenced community composition, with a divergence among separated true siblings and a convergence among foster siblings. Third, larger shifts in both microbiota diversity and composition correlated with lower nestling body condition. Our results shed new light on the dynamics of microbial diversity during the ontogeny of avian hosts, indicating that the nest environment continues to shape the gut microbiota during the later stages of nestling development and that the increase in gut diversity between hatching and adulthood may not be as linear as previously suspected. Lastly, the microbiota changes incurred during this period may have implications for nestling body condition which can lead to long-term consequences for host fitness.

Do wild-caught urban house sparrows show desensitized stress responses to a novel stressor?

While urbanization exposes individuals to novel challenges, urban areas may also constitute stable environments in which seasonal fluctuations are buffered. Baseline and stress-induced plasma corticosterone (cort) levels are often found to be similar in urban and rural populations. Here we aimed to disentangle two possible mechanisms underlying such pattern: (i) urban environments are no more stressful or urban birds have a better ability to habituate to stressors; or (ii) urban birds developed desensitized stress responses. We exposed wild-caught urban and rural house sparrows (Passer domesticus) to combined captivity and diet treatments (urban versus rural diet) and measured corticosterone levels both in natural tail feathers and in regrown homologous ones (cortf). Urban and rural house sparrows showed similar cortf levels in the wild and in response to novel stressors caused by the experiment, supporting the growing notion that urban environments are no more stressful during the non-breeding season than are rural ones. Still, juveniles and males originating from urban populations showed the highest cortf levels in regrown feathers. We did not find evidence that cortf was consistent within individuals across moults. Our study stresses the need for incorporating both intrinsic and environmental factors for the interpretation of variation in cortf between populations.

Inside the guts of the city: Urban-induced alterations of the gut microbiota in a wild passerine.

Urbanisation represents one of the most radical forms of terrestrial land use change and has been shown to lead to alterations in ecosystem functioning and community dynamics and changes in individual phenotypic traits. While the recent surge in microbiome studies has brought about a paradigm shift by which individuals cannot truly be considered independently of the bacterial communities they host, the role of gut microbiota in organismal response to human-induced environmental change is still scarcely studied. Here, we applied a metabarcoding approach to examine the impact of urbanisation on the gut microbiota of Passer domesticus. We found urbanisation to be associated to lower microbiota species diversity, modifications in taxonomic composition and community structure, and changes in functional composition. The strength of these relationships, however, depended on the spatial scale and season at which they were considered. Such spatio-temporal effect suggests that urbanisation may dampen the natural seasonal variation of the gut microbiota observed in more pristine habitats, potentially influencing the fitness of urban organisms. Our results hence shed light on a hitherto little considered perspective, i.e. that the negative effects of urbanisation on city-dwelling organisms may extend to their microbiomes, causing potential dysbioses.

Effects of urbanization on host-pathogen interactions, using Yersinia in house sparrows as a model.

Urbanization strongly affects biodiversity, altering natural communities and often leading to a reduced species richness. Yet, despite its increasingly recognized importance, how urbanization impacts on the health of individual animals, wildlife populations and on disease ecology remains poorly understood. To test whether, and how, urbanization-driven ecosystem alterations influence pathogen dynamics and avian health, we use house sparrows (Passer domesticus) and Yersinia spp. (pathogenic for passerines) as a case study. Sparrows are granivorous urban exploiters, whose western European populations have declined over the past decades, especially in highly urbanized areas. We sampled 329 house sparrows originating from 36 populations along an urbanization gradient across Flanders (Belgium), and used isolation combined with 'matrix-assisted laser desorption ionization- time of flight mass spectrometry' (MALDI-TOF MS) and PCR methods for detecting the presence of different Yersinia species. Yersinia spp. were recovered from 57.43% of the sampled house sparrows, of which 4.06%, 53.30% and 69.54% were identified as Y. pseudotuberculosis, Y. enterocolitica and other Yersinia species, respectively. Presence of Yersinia was related to the degree of urbanization, average daily temperatures and the community of granivorous birds present at sparrow capture locations. Body condition of suburban house sparrows was found to be higher compared to urban and rural house sparrows, but no relationships between sparrows' body condition and presence of Yersinia spp. were found. We conclude that two determinants of pathogen infection dynamics, body condition and pathogen occurrence, vary along an urbanization gradient, potentially mediating the impact of urbanization on avian health.

House Sparrows Do Not Constitute a Significant Salmonella Typhimurium Reservoir across Urban Gradients in Flanders, Belgium.

In recent decades major declines in urban house sparrow (Passer domesticus) populations have been observed in north-western European cities, whereas suburban and rural house sparrow populations have remained relatively stable or are recovering from previous declines. Differential exposure to avian pathogens known to cause epidemics in house sparrows may in part explain this spatial pattern of declines. Here we investigate the potential effect of urbanization on the development of a bacterial pathogen reservoir in free-ranging house sparrows. This was achieved by comparing the prevalence of Salmonella enterica subspecies enterica serotype Typhimurium in 364 apparently healthy house sparrows captured in urban, suburban and rural regions across Flanders, Belgium between September 2013 and March 2014. In addition 12 dead birds, received from bird rescue centers, were necropsied. The apparent absence of Salmonella Typhimurium in fecal samples of healthy birds, and the identification of only one house sparrow seropositive for Salmonella spp., suggests that during the winter of 2013-2014 these birds did not represent any considerable Salmonella Typhimurium reservoir in Belgium and thus may be considered naïve hosts, susceptible to clinical infection. This susceptibility is demonstrated by the isolation of two different Salmonella Typhimurium strains from two of the deceased house sparrows: one DT99, typically associated with disease in pigeons, and one DT195, previously associated with a passerine decline. The apparent absence (prevalence: <1.3%) of a reservoir in healthy house sparrows and the association of infection with clinical disease suggests that the impact of Salmonella Typhimurium on house sparrows is largely driven by the risk of exogenous exposure to pathogenic Salmonella Typhimurium strains. However, no inference could be made on a causal relationship between Salmonella infection and the observed house sparrow population declines.