Spatial covariation between genetic and epigenetic diversity in wild plant and animal populations: a meta-analysis.

Epigenetic variation may be crucial in understanding the structure of wild populations, thereby aiding in their management and conservation. However, the relationship between epigenetic and genetic variation remains poorly understood, especially in wild populations. To address this, we conducted a meta-analysis of studies that examined the genetic and epigenetic structures of wild plant and animal populations. We aimed to determine whether epigenetic variation is spatially independent of genetic variation in the wild and to highlight the conditions under which epigenetic variation might be informative. We show a significant positive correlation between genetic and epigenetic pairwise differentiation, indicating that in wild populations, epigenetic diversity is closely linked to genetic differentiation. The correlation was weaker for population pairs that were weakly differentiated genetically, suggesting that in such cases, epigenetic marks might be independent of genetic marks. Additionally, we found that global levels of genetic and epigenetic differentiation were similar across plant and animal populations, except when populations were weakly differentiated genetically. In such cases, epigenetic differentiation was either higher or lower than genetic differentiation. Our results suggest that epigenetic information is particularly relevant in populations that have recently diverged genetically or are connected by gene flow. Future studies should consider the genetic structure of populations when inferring the role of epigenetic diversity in local adaptation in wild populations. Furthermore, there is a need to identify the factors that sustain the links between genetic and epigenetic diversity to improve our understanding of the interplay between these two forms of variation in wild populations.

Optimizing detectability of the endangered fan mussel using eDNA and ddPCR.

Spatial and temporal monitoring of species threatened with extinction is of critical importance for conservation and ecosystem management. In the Mediterranean coast, the fan mussel (Pinna nobilis) is listed as critically endangered after suffering from a mass mortality event since 2016, leading to 100% mortality in most marine populations. Conventional monitoring for this macroinvertebrate is done using scuba, which is challenging in dense meadows or with low visibility. Here we developed an environmental DNA assay targeting the fan mussel and assessed the influence of several environmental parameters on the species detectability in situ. We developed and tested an eDNA molecular marker and collected 48 water samples in two sites at the Thau lagoon (France) with distinct fan mussel density, depths and during two seasons (summer and autumn). Our marker can amplify fan mussel DNA but lacks specificity since it also amplifies a conspecific species (Pinna rudis). We successfully amplified fan mussel DNA from in situ samples with 46 positive samples (out of 48) using ddPCR, although the DNA concentrations measured were low over almost all samples. Deeper sampling depth slightly increased DNA concentrations, but no seasonal effect was found. We highlight a putative spawning event on a single summer day with much higher DNA concentration compared to all other samples. We present an eDNA molecular assay able to detect the endangered fan mussel and provide guidelines to optimize the sampling protocol to maximize detectability. Effective and non-invasive monitoring tools for endangered species are promising to monitor remaining populations and have the potential of ecological restoration or habitat recolonization following a mass mortality event.

Responses of animals and plants to physiological doses of ethanol: a molecular messenger of hypoxia?

Our viewpoint is that ethanol could act as a molecular messenger in animal and plant organisms under conditions of hypoxia or other stresses and could elicit physiological responses to such conditions. There is evidence that both animal and plant organisms have endogenous levels of ethanol, but reports on the changes induced by this alcohol at physiological levels are sparse. Studies have shown that ethanol has different effects on cell metabolism at low and high concentrations, resembling a hormetic response. Further studies have addressed the potential cellular and molecular mechanisms used by organisms to sense changes in physiological concentrations of ethanol. This article summarizes the possible mechanisms by which ethanol may be sensed, particularly at the cell membrane level. Our analysis shows that current knowledge on this subject is limited. More research is required on the effects of ethanol at very low doses, in plants and animals at both molecular and physiological levels. We believe that further research on this topic could lead to new discoveries in physiology and may even help us understand metabolic adjustments related to climate change. As temperatures rise more frequently, dissolved oxygen levels drop, leading to hypoxic conditions and consequently, an increase in cellular ethanol levels.

Genetic erosion reduces biomass temporal stability in wild fish populations.

Genetic diversity sustains species adaptation. However, it may also support key ecosystems functions and services, for example biomass production, that can be altered by the worldwide loss of genetic diversity. Despite extensive experimental evidence, there have been few attempts to empirically test whether genetic diversity actually promotes biomass and biomass stability in wild populations. Here, using long-term demographic wild fish data from two large river basins in southwestern France, we demonstrate through causal modeling analyses that populations with high genetic diversity do not reach higher biomasses than populations with low genetic diversity. Nonetheless, populations with high genetic diversity have much more stable biomasses over recent decades than populations having suffered from genetic erosion, which has implications for the provision of ecosystem services and the risk of population extinction. Our results strengthen the importance of adopting prominent environmental policies to conserve this important biodiversity facet.

Phylogenetically-conserved candidate genes unify biodiversity-ecosystem function relationships and eco-evolutionary dynamics across biological scales.

The intra- and interspecific facets of biodiversity have traditionally been analysed separately, limiting our understanding of how evolution has shaped biodiversity, how biodiversity (as a whole) alters ecological dynamics and hence eco-evolutionary feedbacks at the community scale. Here, we propose using candidate genes phylogenetically-conserved across species and sustaining functional traits as an inclusive biodiversity unit transcending the intra- and interspecific boundaries. This framework merges knowledge from functional genomics and functional ecology, and we first provide guidelines and a concrete example for identifying phylogenetically-conserved candidate genes (PCCGs) within communities and for measuring biodiversity from PCCGs. We then explain how biodiversity measured at PCCGs can be linked to ecosystem functions, which unifies recent observations that both intra- and interspecific biodiversity are important for ecosystem functions. We then highlight the eco-evolutionary processes shaping PCCG diversity patterns and argue that their respective role can be inferred from concepts derived from population genetics. Finally, we explain how PCCGs may shift the field of eco-evolutionary dynamics from a focal-species approach to a more realistic focal-community approach. This framework provides a novel perspective to investigate the global ecosystem consequences of diversity loss across biological scales, and how these ecological changes further alter biodiversity evolution.

Contrasts in riverscape patterns of intraspecific genetic variation in a diverse Neotropical fish community of high conservation value.

Spatial patterns of genetic variation compared across species provide information about the predictability of genetic diversity in natural populations, and areas requiring conservation measures. Due to their remarkable fish diversity, rivers in Neotropical regions are ideal systems to confront theory with observations and would benefit greatly from such approaches given their increasing vulnerability to anthropogenic pressures. We used SNP data from 18 fish species with contrasting life-history traits, co-sampled across 12 sites in the Maroni- a major river system from the Guiana Shield -, to compare patterns of intraspecific genetic variation and identify their underlying drivers. Analyses of covariance revealed a decrease in genetic diversity as distance from the river outlet increased for 5 of the 18 species, illustrating a pattern commonly observed in riverscapes for species with low-to-medium dispersal abilities. However, the mean within-site genetic diversity was lowest in the two easternmost tributaries of the Upper Maroni and around an urbanized location downstream, indicating the need to address the potential influence of local pressures in these areas, such as gold mining or fishing. Finally, the relative influence of isolation by stream distance, isolation by discontinuous river flow, and isolation by spatial heterogeneity in effective size on pairwise genetic differentiation varied across species. Species with similar dispersal and reproductive guilds did not necessarily display shared patterns of population structure. Increasing the knowledge of specific life history traits and ecological requirements of fish species in these remote areas should help further understand factors that influence their current patterns of genetic variation.

A longitudinal survey in the wild reveals major shifts in fish host microbiota after parasite infection.

Recent studies have highlighted associations between diseases and host microbiota. It remains extremely challenging - especially under natural conditions - to clarify whether host microbiota promote future infections, or whether changes in host microbiota result from infections. Nonetheless, deciphering between these two processes is essential for highlighting the role of microbes in disease progression. We longitudinally surveyed, in the wild, the microbiota of individual fish hosts (Leuciscus burdigalensis) both before and after infection by a crustacean ectoparasite (Tracheliastes polycolpus). We found a striking association between parasite infection and the host microbiota composition restricted to the fins the parasite anchored. We clearly demonstrated that infections by the parasite induced a shift in (and did not result from) the host fin microbiota. Furthermore during infection, the microbiota of infected fins got similar to the microbiota of the adult stage, and the free-living infective stage of the parasite with a predominance of the Burkholderiaceae bacteria family. This suggests that some Burkholderiaceae bacteria are involved in a coinfection process and possibly facilitate T. polycolpus infection. In this study, we reveal novel mechanistic insights for understanding the role of the microbiota in host-parasite interactions, which has implications for predicting the progression of diseases in natural host populations.

Dispersal syndromes in challenging environments: A cross-species experiment.

Dispersal is a central biological process tightly integrated into life-histories, morphology, physiology and behaviour. Such associations, or syndromes, are anticipated to impact the eco-evolutionary dynamics of spatially structured populations, and cascade into ecosystem processes. As for dispersal on its own, these syndromes are likely neither fixed nor random, but conditional on the experienced environment. We experimentally studied how dispersal propensity varies with individuals' phenotype and local environmental harshness using 15 species ranging from protists to vertebrates. We reveal a general phenotypic dispersal syndrome across studied species, with dispersers being larger, more active and having a marked locomotion-oriented morphology and a strengthening of the link between dispersal and some phenotypic traits with environmental harshness. Our proof-of-concept metacommunity model further reveals cascading effects of context-dependent syndromes on the local and regional organisation of functional diversity. Our study opens new avenues to advance our understanding of the functioning of spatially structured populations, communities and ecosystems.

Transcriptomic Adjustments in a Freshwater Ectoparasite Reveal the Role of Molecular Plasticity for Parasite Host Shift.

A parasite's lifestyle is characterized by a critical dependency on its host for feeding, shelter and/or reproduction. The ability of parasites to exploit new host species can reduce the risk associated with host dependency. The number of host species that can be infected by parasites strongly affects their ecological and evolutionary dynamics along with their pathogenic effects on host communities. However, little is known about the processes and the pathways permitting parasites to successfully infect alternative host species, a process known as host shift. Here, we tested whether molecular plasticity changes in gene expression and in molecular pathways could favor host shift in parasites. Focusing on an invasive parasite, Tracheliastes polycolpus, infecting freshwater fish, we conducted a transcriptomic study to compare gene expression in parasites infecting their main host species and two alternative host species. We found 120 significant differentially expressed genes (DEGs) between parasites infecting the different host species. A total of 90% of the DEGs were identified between parasites using the main host species and those using the two alternative host species. Only a few significant DEGs (seven) were identified when comparing parasites from the two alternative host species. Molecular pathways enriched in DEGs and associated with the use of alternative host species were related to cellular machinery, energetic metabolism, muscle activity and oxidative stress. This study strongly suggests that molecular plasticity is an important mechanism sustaining the parasite's ability to infect alternative hosts.

Impacts of temperature on O2 consumption of the Pyrenean brook newt (Calotriton asper) from populations along an elevational gradient.

Global warming impacts biodiversity worldwide, leading to species' adaptation, migration, or extinction. The population's persistence depends on the maintenance of essential activities, which is notably driven by phenotypic adaptation to local environments. Metabolic rate - that increases with temperature in ectotherms - is a key physiological proxy for the energy available to fuel individuals' activities. Cold-adapted ectotherms can exhibit a higher resting metabolism than warm-adapted ones to maintain functionality at higher elevations or latitudes, known as the metabolic cold-adaptation hypothesis. How climate change will affect metabolism in species inhabiting contrasting climates (cold or warm) is still a debate. Therefore, it is of high interest to assess the pace of metabolic responses to global warming among populations adapted to highly different baseline climatic conditions. Here, we conducted a physiological experiment in the endemic Pyrenean brook newt (Calotriton asper). We measured a proxy of standard metabolic rate (SMR) along a temperature gradient in individuals sampled among 6 populations located from 550 to 2189 m a.s.l. We demonstrated that SMR increased with temperature, but significantly diverged depending on populations' origins. The baseline and the slope of the relationship between SMR and temperature were both higher for high-elevation populations than for low-elevation populations. We discussed the stronger metabolic response observed in high-elevation populations suggesting a drop of performance in essential life activities for these individuals under current climate change. With the increase of metabolism as the climate warms, the metabolic-cold adaptation strategy selected in the past could compromise the sustainability of cold-adapted populations if short-term evolutionary responses do not allow to offset this evolutionary legacy.

Molecular approaches reveal weak sibship aggregation and a high dispersal propensity in a non-native fish parasite.

Inferring parameters related to the aggregation pattern of parasites and to their dispersal propensity are important for predicting their ecological consequences and evolutionary potential. Nonetheless, it is notoriously difficult to infer these parameters from wildlife parasites given the difficulty in tracking these organisms. Molecular-based inferences constitute a promising approach that has yet rarely been applied in the wild. Here, we combined several population genetic analyses including sibship reconstruction to document the genetic structure, patterns of sibship aggregation, and the dispersal dynamics of a non-native parasite of fish, the freshwater copepod ectoparasite Tracheliastes polycolpus. We collected parasites according to a hierarchical sampling design, with the sampling of all parasites from all host individuals captured in eight sites spread along an upstream-downstream river gradient. Individual multilocus genotypes were obtained from 14 microsatellite markers, and used to assign parasites to full-sib families and to investigate the genetic structure of T. polycolpus among both hosts and sampling sites. The distribution of full-sibs obtained among the sampling sites was used to estimate individual dispersal distances within families. Our results showed that T. polycolpus sibs tend to be aggregated within sites but not within host individuals. We detected important upstream-to-downstream dispersal events of T. polycolpus between sites (modal distance: 25.4 km; 95% CI [22.9, 27.7]), becoming scarcer as the geographic distance from their family core location increases. Such a dispersal pattern likely contributes to the strong isolation-by-distance observed at the river scale. We also detected some downstream-to-upstream dispersal events (modal distance: 2.6 km; 95% CI [2.2-23.3]) that likely result from movements of infected hosts. Within each site, the dispersal of free-living infective larvae among hosts likely contributes to increasing genetic diversity on hosts, possibly fostering the evolutionary potential of T. polycolpus.

Evolutionary Dynamics of Wild Populations.

Wild populations are facing rapid and sometimes extreme environmental changes that are currently exacerbated by pressing human activities [...].

Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functions.

Loss in intraspecific diversity can alter ecosystem functions, but the underlying mechanisms are still elusive, and intraspecific biodiversity-ecosystem function (iBEF) relationships have been restrained to primary producers. Here, we manipulated genetic and functional richness of a fish consumer (Phoxinus phoxinus) to test whether iBEF relationships exist in consumer species and whether they are more likely sustained by genetic or functional richness. We found that both genotypic and functional richness affected ecosystem functioning, either independently or interactively. Loss in genotypic richness reduced benthic invertebrate diversity consistently across functional richness treatments, whereas it reduced zooplankton diversity only when functional richness was high. Finally, losses in genotypic and functional richness altered functions (decomposition) through trophic cascades. We concluded that iBEF relationships lead to substantial top-down effects on entire food chains. The loss of genotypic richness impacted ecological properties as much as the loss of functional richness, probably because it sustains "cryptic" functional diversity.

Patterns of Epigenetic Diversity in Two Sympatric Fish Species: Genetic vs. Environmental Determinants.

Epigenetic components are hypothesized to be sensitive to the environment, which should permit species to adapt to environmental changes. In wild populations, epigenetic variation should therefore be mainly driven by environmental variation. Here, we tested whether epigenetic variation (DNA methylation) observed in wild populations is related to their genetic background, and/or to the local environment. Focusing on two sympatric freshwater fish species (Gobio occitaniae and Phoxinus phoxinus), we tested the relationships between epigenetic differentiation, genetic differentiation (using microsatellite and single nucleotide polymorphism (SNP) markers), and environmental distances between sites. We identify positive relationships between pairwise genetic and epigenetic distances in both species. Moreover, epigenetic marks better discriminated populations than genetic markers, especially in G. occitaniae. In G. occitaniae, both pairwise epigenetic and genetic distances were significantly associated to environmental distances between sites. Nonetheless, when controlling for genetic differentiation, the link between epigenetic differentiation and environmental distances was not significant anymore, indicating a noncausal relationship. Our results suggest that fish epigenetic variation is mainly genetically determined and that the environment weakly contributed to epigenetic variation. We advocate the need to control for the genetic background of populations when inferring causal links between epigenetic variation and environmental heterogeneity in wild populations.

Quantifying the individual impact of artificial barriers in freshwaters: A standardized and absolute genetic index of fragmentation.

Fragmentation by artificial barriers is an important threat to freshwater biodiversity. Mitigating the negative aftermaths of fragmentation is of crucial importance, and it is now essential for environmental managers to benefit from a precise estimate of the individual impact of weirs and dams on river connectivity. Although the indirect monitoring of fragmentation using molecular data constitutes a promising approach, it is plagued with several constraints preventing a standardized quantification of barrier effects. Indeed, observed levels of genetic differentiation GD depend on both the age of the obstacle and the effective size of the populations it separates, making comparisons of the actual barrier effect of different obstacles difficult. Here, we developed a standardized genetic index of fragmentation (F INDEX), allowing an absolute and independent assessment of the individual effects of obstacles on connectivity. The F INDEX is the standardized ratio between the observed GD between pairs of populations located on either side of an obstacle and the GD expected if this obstacle completely prevented gene flow. The expected GD is calculated from simulations taking into account two parameters: the number of generations since barrier creation and the expected heterozygosity of the populations, a proxy for effective population size. Using both simulated and empirical datasets, we explored the validity and the limits of the F INDEX. We demonstrated that it allows quantifying effects of fragmentation only from a few generations after barrier creation and provides valid comparisons among obstacles of different ages and populations (or species) of different effective sizes. The F INDEX requires a minimum amount of fieldwork and genotypic data and solves some of the difficulties inherent to the study of artificial fragmentation in rivers and potentially in other ecosystems. This makes the F INDEX promising to support the management of freshwater species affected by barriers, notably for planning and evaluating restoration programs.

Comment on "Forest microclimate dynamics drive plant responses to warming".

Zellweger et al (Reports, 15 May 2020, p. 772) claimed that forest plant communities' response to global warming is primarily controlled by microclimate dynamics. We show that community thermophilization is poorly explained by the underlying components of microclimate, and that global warming primarily controls the climatic lag of plant communities. Deconstructing the underlying components of microclimate provides insights for managers.

Seventh BMC ecology image competition: the winning images.

The seventh BMC Ecology competition attracted entries from talented ecologists from around the world. Together, they showcase the beauty and diversity of life on our planet as well as providing an insight into the biological interactions found in nature. This editorial celebrates the winning images as selected by the Editor of BMC Ecology and senior members of the journal's editorial board. Enjoy!

A river runs through it: The causes, consequences, and management of intraspecific diversity in river networks.

Rivers are fascinating ecosystems in which the eco-evolutionary dynamics of organisms are constrained by particular features, and biologists have developed a wealth of knowledge about freshwater biodiversity patterns. Over the last 10 years, our group used a holistic approach to contribute to this knowledge by focusing on the causes and consequences of intraspecific diversity in rivers. We conducted empirical works on temperate permanent rivers from southern France, and we broadened the scope of our findings using experiments, meta-analyses, and simulations. We demonstrated that intraspecific (genetic) diversity follows a spatial pattern (downstream increase in diversity) that is repeatable across taxa (from plants to vertebrates) and river systems. This pattern can result from interactive processes that we teased apart using appropriate simulation approaches. We further experimentally showed that intraspecific diversity matters for the functioning of river ecosystems. It indeed affects not only community dynamics, but also key ecosystem functions such as litter degradation. This means that losing intraspecific diversity in rivers can yield major ecological effects. Our work on the impact of multiple human stressors on intraspecific diversity revealed that-in the studied river systems-stocking of domestic (fish) strains strongly and consistently alters natural spatial patterns of diversity. It also highlighted the need for specific analytical tools to tease apart spurious from actual relationships in the wild. Finally, we developed original conservation strategies at the basin scale based on the systematic conservation planning framework that appeared pertinent for preserving intraspecific diversity in rivers. We identified several important research avenues that should further facilitate our understanding of patterns of local adaptation in rivers, the identification of processes sustaining intraspecific biodiversity-ecosystem function relationships, and the setting of reliable conservation plans.

Assessing metacommunity processes through signatures in spatiotemporal turnover of community composition.

Although metacommunity ecology has been a major field of research in the last decades, with both conceptual and empirical outputs, the analysis of the temporal dynamics of metacommunities has only emerged recently and consists mostly of repeated static analyses. Here we propose a novel analytical framework to assess metacommunity processes using path analyses of spatial and temporal diversity turnovers. We detail the principles and practical aspects of this framework and apply it to simulated datasets to illustrate its ability to decipher the respective contributions of entangled drivers of metacommunity dynamics. We then apply it to four empirical datasets. Empirical results support the view that metacommunity dynamics may be generally shaped by multiple ecological processes acting in concert, with environmental filtering being variable across both space and time. These results reinforce our call to go beyond static analyses of metacommunities that are blind to the temporal part of environmental variability.