Foster rather than biological parental telomere length predicts offspring survival and telomere length in king penguins

Because telomere length and dynamics relate to individual growth, reproductive investment and survival, telomeres have emerged as possible markers of individual quality. Here, we tested the hypothesis that, in species with parental care, parental telomere length can be a marker of parental quality that predicts offspring phenotype and survival. In king penguins (Aptenodytes patagonicus), we experimentally swapped the single egg of 66 breeding pairs just after egg laying to disentangle the contribution of prelaying parental quality (e.g., genetics, investment in the egg) and/or postlaying parental quality (e.g., incubation, postnatal feeding rate) on offspring growth, telomere length and survival. Parental quality was estimated through the joint effects of biological and foster parent telomere length on offspring traits, both soon after hatching (day 10) and at the end of the prewinter growth period (day 105). We expected that offspring traits would be mostly related to the telomere lengths (i.e., quality) of biological parents at day 10 and to the telomere lengths of foster parents at day 105. Results show that chick survival up to 10 days was negatively related to biological fathers’ telomere length, whereas survival up to 105 days was positively related to foster fathers’ telomere lengths. Chick growth was not related to either biological or foster parents’ telomere length. Chick telomere length was positively related to foster mothers’ telomere length at both 10 and 105 days. Overall, our study shows that, in a species with biparental care, parents’ telomere length is foremost a proxy of postlaying parental care quality, supporting the “telomere – parental quality hypothesis.”     

Telomere shortening correlates with harsh weather conditions in the bat species Myotis myotis

The relationship of telomere shortening and cellular ageing in cultured cells such as fibroblasts is straightforward: telomeres shorten with an increasing number of cell divisions until they trigger replicative senescence which prevents further mitotic cycles. But studies investigating the relationship between telomere shortening and ageing in whole organisms show contrasting results: while there is a clear decline in telomere length (TL) with chronological age in some species such as humans, no such decline is observed in others. In this issue of Molecular Ecology, Foley et al. (2020) show that experiencing harsh weather conditions correlates with longitudinal telomere shortening in the bat species Myotis myotis, whereas chronological age does not (Foley et al., 2020). Further, the authors investigated whether genetics influence TL and find a low heritability (h² = 0.01–0.06) again suggesting that environmental effects are the dominant drivers of variation in TL in this species. These are important findings as there is disagreement in the literature about the relative magnitude of genetic and environmental effects contributing to TL variation in different species. This paper investigating the impact of environmental effects makes a novel and important contribution to the literature on TL in free‐living mammals.     

Energy–water and seasonal variations in climate underlie the spatial distribution patterns of gymnosperm species richness in China

Studying the pattern of species richness is crucial in understanding the diversity and distribution of organisms in the earth. Climate and human influences are the major driving factors that directly influence the large‐scale distributions of plant species, including gymnosperms. Understanding how gymnosperms respond to climate, topography, and human‐induced changes is useful in predicting the impacts of global change. Here, we attempt to evaluate how climatic and human‐induced processes could affect the spatial richness patterns of gymnosperms in China. Initially, we divided a map of the country into grid cells of 50 × 50 km² spatial resolution and plotted the geographical coordinate distribution occurrence of 236 native gymnosperm taxa. The gymnosperm taxa were separated into three response variables: (a) all species, (b) endemic species, and (c) nonendemic species, based on their distribution. The species richness patterns of these response variables to four predictor sets were also evaluated: (a) energy–water, (b) climatic seasonality, (c) habitat heterogeneity, and (d) human influences. We performed generalized linear models (GLMs) and variation partitioning analyses to determine the effect of predictors on spatial richness patterns. The results showed that the distribution pattern of species richness was highest in the southwestern mountainous area and Taiwan in China. We found a significant relationship between the predictor variable set and species richness pattern. Further, our findings provide evidence that climatic seasonality is the most important factor in explaining distinct fractions of variations in the species richness patterns of all studied response variables. Moreover, it was found that energy–water was the best predictor set to determine the richness pattern of all species and endemic species, while habitat heterogeneity has a better influence on nonendemic species. Therefore, we conclude that with the current climate fluctuations as a result of climate change and increasing human activities, gymnosperms might face a high risk of extinction.     

Environmental influences on and antimicrobial activity of the skin microbiota of Proceratophrys boiei (Amphibia,Anura) across forest fragments

The composition of the skin microbiota of amphibians is related to the biology of host species and environmental microbial communities. In this system, the environment serves as a microbial source and can modulate the hosted community. When habitats are fragmented and the environment disturbed, changes in the structure of this microbial community are expected. One important potential consequence of fragmentation is a compromised protective function of the microbiota against pathogenic microorganisms. In this study, the skin microbiota of the amphibian Proceratophrys boiei was characterized, evaluated for relationships with environmental variables and environmental sources of microbial communities, and its diversity evaluated for frog populations from fragmented and continuous forests. In addition, the antimicrobial activity of this skin community was studied in frogs from both forest types. Culture methods and 16S rRNA high‐throughput gene sequencing were used to characterize the microbial community and demonstrated that the skin microbiota of P. boiei is more closely related to the soil microbial communities than those inhabiting water bodies or fragment matrix, the unforested area around the forested fragment. The microbial diversity and abundance of P. boiei skin microbiota are different between continuous forests and fragments. This community is correlated with environmental variables, especially with temperature of microhabitat and distance to human dwelling. All individuals of P. boiei harbored bacteria capable of inhibiting the growth of pathogenic bacteria and different strains of the pathogenic fungus Batrachochytrium dendrobatidis, and a total of 27 bacterial genera were detected. The results of this study indicate that the persistence of populations of this species will need balanced and sustained interactions among host, microorganisms, and environment.     

Occupancy versus colonization–extinction models for projecting population trends at different spatial scales

Understanding spatiotemporal population trends and their drivers is a key aim in population ecology. We further need to be able to predict how the dynamics and sizes of populations are affected in the long term by changing landscapes and climate. However, predictions of future population trends are sensitive to a range of modeling assumptions. Deadwood‐dependent fungi are an excellent system for testing the performance of different predictive models of sessile species as these species have different rarity and spatial population dynamics, the populations are structured at different spatial scales, and they utilize distinct substrates. We tested how the projected large‐scale occupancies of species with differing landscape‐scale occupancies are affected over the coming century by different modeling assumptions. We compared projections based on occupancy models against colonization–extinction models, conducting the modeling at alternative spatial scales and using fine‐ or coarse‐resolution deadwood data. We also tested effects of key explanatory variables on species occurrence and colonization–extinction dynamics. The hierarchical Bayesian models applied were fitted to an extensive repeated survey of deadwood and fungi at 174 patches. We projected higher occurrence probabilities and more positive trends using the occupancy models compared to the colonization–extinction models, with greater difference for the species with lower occupancy, colonization rate, and colonization:extinction ratio than for the species with higher estimates of these statistics. The magnitude of future increase in occupancy depended strongly on the spatial modeling scale and resource resolution. We encourage using colonization–extinction models over occupancy models, modeling the process at the finest resource‐unit resolution that is utilizable by the species, and conducting projections for the same spatial scale and resource resolution at which the model fitting is conducted. Further, the models applied should include key variables driving the metapopulation dynamics, such as the availability of suitable resource units, habitat quality, and spatial connectivity.     

Trait‐based diatom functional diversity as an appropriate tool for understanding the effects of environmental changes in soda pans

Saline lakes, among the most seriously endangered ecosystems, are threatened due to climate change and human activities. One valuable feature of these environments is that they constitute areas of high biodiversity. Ecologists are, therefore, under great pressure to improve their understanding of the effects of natural and anthropogenic disturbances on the biodiversity of saline lakes. In this study, a total of 257 samples from 32 soda pans in Central Europe between 2006 and 2015 were examined. The effects of environmental variables and of geographical and limnoecological factors on functional diversity were analyzed. Furthermore, the explanatory power of the trait‐based approach was assessed, and the applicability of the indices for biomonitoring purposes was determined. It was found that low habitat heterogeneity and harsh environments lead to the selection of a small number of suitable traits, and consequently, to a naturally low level of functional diversity. Anthropogenic activities enhance diversity at functional level due to the shift toward freshwater characteristics. On the regional scale, the effects of the region and status (natural, degraded, reconstructed) on diatom functional diversity were significant and more pronounced than that of the environmental and other limnoecological factors. The degree of variance found in functional diversity ascribed to environmental variables is five times greater in the case of the application of a trait‐based approach, than when a taxonomic one is employed in the literature. Each of the tested functional diversity indices was sensitive to the most important environmental variables. Furthermore, these were type‐specific and proved to be more complex indicators than taxonomic metrics. It is possible to suggest four functional diversity indices (FGR, FRic, FDis, and FDiv) which emphasize their independence from substrate and seasonal variations for ecological status assessment and conservation planning.     

Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish

The perception of predation risk could affect prey phenotype both within and between generations (via parental effects). The response to predation risk could involve modifications in physiology, morphology, and behavior and can ultimately affect long‐term fitness. Among the possible modifications mediated by the exposure to predation risk, telomere length could be a proxy for investigating the response to predation risk both within and between generations, as telomeres can be significantly affected by environmental stress. Maternal exposure to the perception of predation risk can affect a variety of offspring traits but the effect on offspring telomere length has never been experimentally tested. Using a live‐bearing fish, the guppy (Poecilia reticulata), we tested if the perceived risk of predation could affect the telomere length of adult females directly and that of their offspring with a balanced experimental setup that allowed us to control for both maternal and paternal contribution. We exposed female guppies to the perception of predation risk during gestation using a combination of both visual and chemical cues and we then measured female telomere length after the exposure period. Maternal effects mediated by the exposure to predation risk were measured on offspring telomere length and body size at birth. Contrary to our predictions, we did not find a significant effect of predation‐exposure neither on female nor on offspring telomere length, but females exposed to predation risk produced smaller offspring at birth. We discuss the possible explanations for our findings and advocate for further research on telomere dynamics in ectotherms.     

Disentangling the spatial and temporal causes of decline in a bird population

The difficulties in understanding the underlying reasons of a population decline lie in the typical short duration of field studies, the often too small size already reached by a declining population or the multitude of environmental factors that may influence population trend. In this difficult context, useful demographic tools such as integrated population models (IPM) may help disentangling the main reasons for a population decline. To understand why a hoopoe Upupa epops population has declined, we followed a three step model analysis. We built an IPM structured with respect to habitat quality (approximated by the expected availability of mole crickets, the main prey in our population) and estimated the contributions of habitat‐specific demographic rates to population variation and decline. We quantified how much each demographic rate has decreased and investigated whether habitat quality influenced this decline. We tested how much weather conditions and research activities contributed to the decrease in the different demographic rates. The decline of the hoopoe population was mainly explained by a decrease in first‐year apparent survival and a reduced number of fledglings produced, particularly in habitats of high quality. Since a majority of pairs bred in habitats of the highest quality, the decrease in the production of locally recruited yearlings in high‐quality habitat was the main driver of the population decline despite a homogeneous drop of recruitment across habitats. Overall, the explanatory variables we tested only accounted for 19% of the decrease in the population growth rate. Among these variables, the effects of spring temperature (49% of the explained variance) contributed more to population decline than spring precipitation (36%) and research activities (maternal capture delay, 15%). This study shows the power of IPMs for identifying the vital rates involved in population declines and thus paves the way for targeted conservation and management actions.     

Native drivers of fish life history traits are lost during the invasion process

Rapid adaptation to global change can counter vulnerability of species to population declines and extinction. Theoretically, under such circumstances both genetic variation and phenotypic plasticity can maintain population fitness, but empirical support for this is currently limited. Here, we aim to characterize the role of environmental and genetic diversity, and their prior evolutionary history (via haplogroup profiles) in shaping patterns of life history traits during biological invasion. Data were derived from both genetic and life history traits including a morphological analysis of 29 native and invasive populations of topmouth gudgeon Pseudorasbora parva coupled with climatic variables from each location. General additive models were constructed to explain distribution of somatic growth rate (SGR) data across native and invasive ranges, with model selection performed using Akaike's information criteria. Genetic and environmental drivers that structured the life history of populations in their native range were less influential in their invasive populations. For some vertebrates at least, fitness‐related trait shifts do not seem to be dependent on the level of genetic diversity or haplogroup makeup of the initial introduced propagule, nor of the availability of local environmental conditions being similar to those experienced in their native range. As long as local conditions are not beyond the species physiological threshold, its local establishment and invasive potential are likely to be determined by local drivers, such as density‐dependent effects linked to resource availability or to local biotic resistance.     

In silico and empirical evaluation of twelve metabarcoding primer sets for insectivorous diet analyses

During the most recent decade, environmental DNA metabarcoding approaches have been both developed and improved to minimize the biological and technical biases in these protocols. However, challenges remain, notably those relating to primer design. In the current study, we comprehensively assessed the performance of ten COI and two 16S primer pairs for eDNA metabarcoding, including novel and previously published primers. We used a combined approach of in silico, in vivo‐mock community (33 arthropod taxa from 16 orders), and guano‐based analyses to identify primer sets that would maximize arthropod detection and taxonomic identification, successfully identify the predator (bat) species, and minimize the time and financial costs of the experiment. We focused on two insectivorous bat species that live together in mixed colonies: the greater horseshoe bat (Rhinolophus ferrumequinum) and Geoffroy's bat (Myotis emarginatus). We found that primer degeneracy is the main factor that influences arthropod detection in silico and mock community analyses, while amplicon length is critical for the detection of arthropods from degraded DNA samples. Our guano‐based results highlight the importance of detecting and identifying both predator and prey, as guano samples can be contaminated by other insectivorous species. Moreover, we demonstrate that amplifying bat DNA does not reduce the primers' capacity to detect arthropods. We therefore recommend the simultaneous identification of predator and prey. Finally, our results suggest that up to one‐third of prey occurrences may be unreliable and are probably not of primary interest in diet studies, which may decrease the relevance of combining several primer sets instead of using a single efficient one. In conclusion, this study provides a pragmatic framework for eDNA primer selection with respect to scientific and methodological constraints.