Disentangling the effects of different human disturbances on multifaceted biodiversity indices in freshwater fish.

Evaluating the effects of anthropogenic pressures on several biodiversity metrics can inform the management and monitoring of biodiversity loss. However, the type of disturbances can lead to different responses in different metrics. In this study, we aimed at disentangling the effects of different types of anthropogenic disturbances on freshwater fish communities. We calculated diversity indices for 1109 stream fish communities across France by computing richness and evenness components for ecological, morphological, and phylogenetic diversity, and used null models to estimate standardized effect sizes. We used generalized linear mixed models to assess the relative effects of environmental and anthropogenic drivers in driving those diversity indices. Our results demonstrated that all diversity indices exhibited significant responses to both climatic conditions and anthropogenic disturbances. While we observed a decrease of ecological and phylogenetic richness with the intensity of disturbance, a weak increase in morphological richness and evenness was apparent. Overall, our results demonstrated the importance of disentangling various types of disturbances when assessing human-induced ecological impacts and highlighted that different facets of diversity are not impacted identically by anthropogenic disturbances in stream fish communities. This calls for further work seeking to integrate biodiversity responses to human disturbances into a multifaceted framework, and could have beneficial implications when planning conservation action in freshwater ecosystems.

Spatially structured freshwater fish population dynamics at the River Basin District scale: Implication for environmental management and fish conservation.

European Union environmental policy has created a unique regulatory framework to favour aquatic ecosystem management and biodiversity conservation across European countries. Identifying the spatial structure of freshwater fish population dynamics is crucial to define region-specific management and conservation planning. To implement evidence-driven management and conservation decisions at a regional scale we assessed spatial heterogeneity in common freshwater fish population dynamics in France with a focus on trends in River Basin Districts (RBDs). The abundance and biomass growth rates of 18 common European freshwater fish species were estimated with state-space models on 546 sites distributed across the 5 main RBDs sampled in France between 1990 and 2011. Anguilla anguilla, Rutilus rutilus, Salmo trutta fario and Esox spp. exhibited large scale decline in abundance and/or biomass in several RBDs. The other species showed spatial heterogeneity in population growth rates. The main declines were observed in the Adour-Garonne and Loire-Bretagne RBDs, where management and conservation measures are urgently needed to halt the erosion of freshwater fish populations. In each of the 5 investigated RBDs, our results highlight areas where most of the common species we studied exhibited negative population growth rates. Freshwater fish surveys provide the fundamental information necessary to inform the European environmental policies and local environmental management needed to restore freshwater biodiversity. The next steps are to identify the main drivers of freshwater biodiversity erosion in the areas where we demonstrated major declines and to define the most cost-effective restoration measures.

Seasonal dynamics of riverine fish communities using eDNA.

As fish communities are a major concern in rivers ecosystems, we investigated if their environmental (e)DNA signals vary according to the sampling period or hydromorphological conditions. Three rivers were studied over a year using eDNA metabarcoding approach. The majority of the species (c. 80%) were detected all year round in two rivers having similar hydromorphological conditions, whereas in the river affected by an upstream lake waterflow, more species were detected sporadically (42%). For all the rivers, in more than 98% of the occasional detections, the reads abundance represented <0.4% of the total reads per site and per sampling session. Even if the majority of the fish communities remained similar over the year for each of the three rivers, specific seasonal patterns were observed. We studied if the waterflow or the reproduction period had an effect on the observed dynamics. Waterflow, which influences eDNA downstream transportation, had a global influence in taxonomic richness, while the fishes' reproductive period had only an influence on certain species. Our results may help selecting the best sampling strategy according to research objectives. To study fish communities at local scale, seasons of low waterflow periods are recommended. This particularly helps to restraint effects of external eDNA coming from connections with other aquatic environment (tributaries, lakes, wetlands, sewage effluents, etc.). To obtain a more integrative overview of the fish community living in a river basin, high waterflow or breeding seasons are preferable for enhancing species detection probability, especially for rare species.

Development of a large SNPs resource and a low-density SNP array for brown trout (Salmo trutta) population genetics.

BACKGROUND: The brown trout (Salmo trutta) is an economically and ecologically important species for which population genetic monitoring is frequently performed. The most commonly used genetic markers for this species are microsatellites and mitochondrial markers that lack replicability among laboratories, and a large genome coverage. An alternative that may be particularly efficient and universal is the development of small to large panels of Single Nucleotide Polymorphism markers (SNPs). Here, we used Restriction site Associated DNA sequences (RADs) markers to identify a set of 12,204 informative SNPs positioned on the brown trout linkage map and suitable for population genetics studies. Then, we used this novel resource to develop a cost-effective array of 192 SNPs (96 × 2) evenly spread on this map. This array was tested for genotyping success in five independent rivers occupied by two main brown trout evolutionary lineages (Atlantic -AT- and Mediterranean -ME-) on a total of 1862 individuals. Moreover, inference of admixture rate with domestic strains and population differentiation were assessed for a small river system (the Taurion River, 190 individuals) and results were compared to a panel of 13 microsatellites. RESULTS: A high genotyping success was observed for all rivers (< 1% of non-genotyped loci per individual), although some initially used SNP failed to be amplified, probably because of mutations in primers, and were replaced. These SNPs permitted to identify patterns of isolation-by-distance for some rivers. Finally, we found that microsatellite and SNP markers yielded very similar patterns for population differentiation and admixture assessments, with SNPs having better ability to detect introgression and differentiation. CONCLUSIONS: The novel resources provided here opens new perspectives for universality and genome-wide studies in brown trout populations.

Systematic conservation planning for intraspecific genetic diversity.

Intraspecific diversity informs the demographic and evolutionary histories of populations, and should be a main conservation target. Although approaches exist for identifying relevant biological conservation units, attempts to identify priority conservation areas for intraspecific diversity are scarce, especially within a multi-specific framework. We used neutral molecular data on six European freshwater fish species (Squalius cephalus, Phoxinus phoxinus, Barbatula barbatula, Gobio occitaniae, Leuciscus burdigalensis and Parachondrostoma toxostoma) sampled at the riverscape scale (i.e. the Garonne-Dordogne river basin, France) to determine hot- and coldspots of genetic diversity, and to identify priority conservation areas using a systematic conservation planning approach. We demonstrate that systematic conservation planning is efficient for identifying priority areas representing a predefined part of the total genetic diversity of a whole landscape. With the exception of private allelic richness (PA), classical genetic diversity indices (allelic richness, genetic uniqueness) were poor predictors for identifying priority areas. Moreover, we identified weak surrogacies among conservation solutions found for each species, implying that conservation solutions are highly species-specific. Nonetheless, we showed that priority areas identified using intraspecific genetic data from multiple species provide more effective conservation solutions than areas identified for single species or on the basis of traditional taxonomic criteria.

Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding.

Global biodiversity in freshwater and the oceans is declining at high rates. Reliable tools for assessing and monitoring aquatic biodiversity, especially for rare and secretive species, are important for efficient and timely management. Recent advances in DNA sequencing have provided a new tool for species detection from DNA present in the environment. In this study, we tested whether an environmental DNA (eDNA) metabarcoding approach, using water samples, can be used for addressing significant questions in ecology and conservation. Two key aquatic vertebrate groups were targeted: amphibians and bony fish. The reliability of this method was cautiously validated in silico, in vitro and in situ. When compared with traditional surveys or historical data, eDNA metabarcoding showed a much better detection probability overall. For amphibians, the detection probability with eDNA metabarcoding was 0.97 (CI = 0.90-0.99) vs. 0.58 (CI = 0.50-0.63) for traditional surveys. For fish, in 89% of the studied sites, the number of taxa detected using the eDNA metabarcoding approach was higher or identical to the number detected using traditional methods. We argue that the proposed DNA-based approach has the potential to become the next-generation tool for ecological studies and standardized biodiversity monitoring in a wide range of aquatic ecosystems.

Ecological emergence of thermal clines in body size.

The unprecedented rate of global warming requires a better understanding of how ecosystems will respond. Organisms often have smaller body sizes under warmer climates (Bergmann's rule and the temperature-size rule), and body size is a major determinant of life histories, demography, population size, nutrient turnover rate, and food-web structure. Therefore, by altering body sizes in whole communities, current warming can potentially disrupt ecosystem function and services. However, the underlying drivers of warming-induced body downsizing remain far from clear. Here, we show that thermal clines in body size are predicted from universal laws of ecology and metabolism, so that size-dependent selection from competition (both intra and interspecific) and predation favors smaller individuals under warmer conditions. We validate this prediction using 4.1 × 10(6) individual body size measurements from French river fish spanning 29 years and 52 species. Our results suggest that warming-induced body downsizing is an emergent property of size-structured food webs, and highlight the need to consider trophic interactions when predicting biosphere reorganizations under global warming.

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.

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.

Predicting haplogroups using a versatile machine learning program (PredYMaLe) on a new mutationally balanced 32 Y-STR multiplex (CombYplex): Unlocking the full potential of the human STR mutation rate spectrum to estimate forensic parameters.

We developed a new mutationally well-balanced 32 Y-STR multiplex (CombYplex) together with a machine learning (ML) program PredYMaLe to assess the impact of STR mutability on haplogourp prediction, while respecting forensic community criteria (high DC/HD). We designed CombYplex around two sub-panels M1 and M2 characterized by average and high-mutation STR panels. Using these two sub-panels, we tested how our program PredYmale reacts to mutability when considering basal branches and, moving down, terminal branches. We tested first the discrimination capacity of CombYplex on 996 human samples using various forensic and statistical parameters and showed that its resolution is sufficient to separate haplogroup classes. In parallel, PredYMaLe was designed and used to test whether a ML approach can predict haplogroup classes from Y-STR profiles. Applied to our kit, SVM and Random Forest classifiers perform very well (average 97 %), better than Neural Network (average 91 %) and Bayesian methods (< 90 %). We observe heterogeneity in haplogroup assignation accuracy among classes, with most haplogroups having high prediction scores (99-100 %) and two (E1b1b and G) having lower scores (67 %). The small sample sizes of these classes explain the high tendency to misclassify the Y-profiles of these haplogroups; results were measurably improved as soon as more training data were added. We provide evidence that our ML approach is a robust method to accurately predict haplogroups when it is combined with a sufficient number of markers, well-balanced mutation rate Y-STR panels, and large ML training sets. Further research on confounding factors (such as CNV-STR or gene conversion) and ideal STR panels in regard to the branches analysed can be developed to help classifiers further optimize prediction scores.

Genetic structure and dynamics of a small introduced population: the pikeperch, Sander lucioperca, in the Rhône delta.

Genetic data on introduced populations may help us to understand how these species succeed in colonising new territories. The pikeperch is a predatory fish widely introduced in Europe and has at times been considered as an invasive species. However, little is known about the genetics of both native and introduced populations. In the present study, we surveyed an introduced pikeperch population from the Rhône River delta, a habitat that has been highly modified for agricultural purposes. Using six microsatellites, we genotyped 93 individuals distributed among four hydraulically connected water bodies: the Rhône River, an irrigation canal, a drainage canal and a brackish lagoon. Population isolation were revealed by significant genetic distances and bottleneck highlighted by population monitoring. However, values of allelic richness and unbiased expected heterozygosity observed in these populations were similar, or even higher, compare to 18 native populations from the Baltic Sea drainage. It may be explained by multiple introductions in the Rhône drainage but also by demographic strategy that would have facilitated population persistence in this fragmented habitat. Similarly, heterozygote deficits (revealed by F(IS) values) have been detected, but were also found in native populations suggesting that mating among relatives could also result from a mating behavior of the species, maybe reinforce here by the reduced carrying capacity of the artificial canals and their respective isolation. Despite harsh environmental conditions and suspected inbreeding, the pikeperch has successfully maintained viable populations in the Rhône delta. Our study suggests that one of the factors in this invasive success, apart from its ecology, could be the maintenance of a good level of genetic diversity in introduced pikeperch populations. This genetic diversity probably stem from both its popularity as game fish and food resource which led to numerous stocking and an increasing propagule pressure and the reproductive strategy of the species.

Y-chromosome descent clusters and male differential reproductive success: young lineage expansions dominate Asian pastoral nomadic populations.

High-frequency microsatellite haplotypes of the male-specific Y-chromosome can signal past episodes of high reproductive success of particular men and their patrilineal descendants. Previously, two examples of such successful Y-lineages have been described in Asia, both associated with Altaic-speaking pastoral nomadic societies, and putatively linked to dynasties descending, respectively, from Genghis Khan and Giocangga. Here we surveyed a total of 5321 Y-chromosomes from 127 Asian populations, including novel Y-SNP and microsatellite data on 461 Central Asian males, to ask whether additional lineage expansions could be identified. Based on the most frequent eight-microsatellite haplotypes, we objectively defined 11 descent clusters (DCs), each within a specific haplogroup, that represent likely past instances of high male reproductive success, including the two previously identified cases. Analysis of the geographical patterns and ages of these DCs and their associated cultural characteristics showed that the most successful lineages are found both among sedentary agriculturalists and pastoral nomads, and expanded between 2100 BCE and 1100 CE. However, those with recent origins in the historical period are almost exclusively found in Altaic-speaking pastoral nomadic populations, which may reflect a shift in political organisation in pastoralist economies and a greater ease of transmission of Y-chromosomes through time and space facilitated by the use of horses.

A new freshwater biodiversity indicator based on fish community assemblages.

Biodiversity has reached a critical state. In this context, stakeholders need indicators that both provide a synthetic view of the state of biodiversity and can be used as communication tools. Using river fishes as model, we developed community indicators that aim at integrating various components of biodiversity including interactions between species and ultimately the processes influencing ecosystem functions. We developed indices at the species level based on (i) the concept of specialization directly linked to the niche theory and (ii) the concept of originality measuring the overall degree of differences between a species and all other species in the same clade. Five major types of originality indices, based on phylogeny, habitat-linked and diet-linked morphology, life history traits, and ecological niche were analyzed. In a second step, we tested the relationship between all biodiversity indices and land use as a proxy of human pressures. Fish communities showed no significant temporal trend for most of these indices, but both originality indices based on diet- and habitat- linked morphology showed a significant increase through time. From a spatial point of view, all indices clearly singled out Corsica Island as having higher average originality and specialization. Finally, we observed that the originality index based on niche traits might be used as an informative biodiversity indicator because we showed it is sensitive to different land use classes along a landscape artificialization gradient. Moreover, its response remained unchanged over two other land use classifications at the global scale and also at the regional scale.

Effects of small weirs on fish parasite communities.

In this study, we examined the impacts of small weirs on the parasite community of gudgeon and toxostome in a medium-sized river. We tested changes on parasite species diversity using indices that capture both richness and abundance characteristics, and we examined parasite community structure with null models (co-occurrence index C score) and a multiple discriminant function analysis (MDFA). Our results showed that parasite community diversity of gudgeon is strongly influenced by weirs with a maximum diversity upstream of the weirs. Weirs also induce change in abundance of gudgeon parasite species particularly during summer. Nevertheless, we obtained that weirs had no effect on the parasite co-occurrence patterns. In addition, similarity indices indicate that the parasite faunas of newly established limnophilic species (roach and bleak) are host-specific and are rarely transmitted to other fish species. We conclude that fish parasite communities responded in different ways to the presence of impassable weirs, but, in a general tendency, changing environmental conditions induced by weirs may represent an ecological risk.

The effects of the ectoparasite Tracheliastes polycolpus (Copepoda: Lernaeopodidae) on the fins of rostrum dace (Leuciscus leuciscus burdigalensis).

Rostrum dace (Leuciscus leuciscus burdigalensis) from the River Viaur were found to be infested with the ectoparasite Tracheliastes polycolpus (Copepoda: Lernaeopodidae). Samples from five study sites along the river revealed different patterns of parasite infestation. Heavily infested fish were found at the upper study sites whereas much lower infestation levels were observed at the lower study sites. The copepods showed an aggregated dispersion pattern on host fins. The results showed significantly preferred microhabitats, with adult females being more abundant on the anal, pelvic and along the external part of the pectoral fins. The anal and pelvic fins were damaged by the parasite with a loss of their surface area. These fin alterations may reduce the fish's swimming ability and therefore affect the rostrum dace population. Our findings highlight the need to study the effects of parasites on stream fish populations.