Demographic and genetic collapses in spatially structured populations: insights from a long-term survey in wild fish metapopulations

International audienceUnraveling the relationship between demographic declines and genetic changes over time is of critical importance to predict the persistence of at-risk populations and to propose efficient conservation plans. This is particularly relevant in spatially struc- tured populations (i.e. metapopulations) in which the spatial arrangement of local populations can modulate both demographic and genetic changes. We used ten-year demo-genetic monitoring to test 1) whether demographic declines were associated with genetic diversity declines and 2) whether the spatial structure of a metapopula- tion can weaken or reinforce these demographic and genetic temporal trends. We continuously surveyed, over time and across their entire range, two metapopulations of an endemic freshwater fish species Leuciscus burdigalensis: one metapopulation that had experienced a recent demographic decline and a second metapopulation that was stable over time. In the declining metapopulation, the number of alleles rapidly decreased, the inbreeding coefficient increased, and a genetic bottleneck emerged over time. In contrast, genetic indices were constant over time in the stable metapopulation. We further show that, in the declining metapopulation, demographic and genetic declines were not homogeneously distributed across the metapopula- tion. We notably identify one local population situated downstream as a ‘reservoir’ of individuals and genetic variability that dampens both the demographic and genetic declines measured at the metapopulation level. We demonstrate the usefulness of long-term monitoring that combines both genetic and demographic parameters to understand and predict temporal population fluctuations of at-risk species living in a metapopulation context

De novo transcriptome assembly for Tracheliastes polycolpus, an invasive ectoparasite of freshwater fish in western Europe

International audienceTracheliastes polycolpus is an ectoparasitic copepod that recently emerged in western Europe and that infects several freshwater fish species. Its recent successful spread might be due to its fascinating ability to shift to new host populations and/or species. Here, we present the first non-redundant and protein-coding de novo transcriptome assembly for T. polycolpus along with a quality assessment and reliable transcript annotations. This assembly was built from fifteen adult female parasites sampled from three different host species from a single river in southwestern France. Overall, 17,157 non-redundant contigs likely corresponding to protein-coding transcripts were identified, of which 13,093 (i.e., 76%) were successfully annotated. This assembly displayed good representativeness since 65.8% of the raw reads properly aligned back to the assembly. Similarly, 90.5% of the single copies of orthologues conserved across arthropods were retrieved in this assembly, which reflects a very good completeness. Finally, this transcriptome assembly gathered 7979 T. polycolpus specific transcripts when compared with the two closest referenced species (Lepeophtheirus salmonis and Caligus rogercresseyi), thus constituting an original genomic resource. This high-quality transcriptome is an important genomic resource for deciphering the molecular bases underlying host shifts in generalist parasites, and for studying the evolutionary biology of copepods that are major biological components of both freshwater and marine ecosystems

Resources for "Demographic and genetic collapses in spatially-structured populations: Insights from a long-term survey in wild fish metapopulations"

<p>Here are made available the datasets and R scripts required to perform the different analyses presented in the study entitled "Demographic and genetic collapses in spatially-structured populations: Insights from a long-term survey in wild fish meta-populations"</p> <p> </p> <p>More details are given in the file entitled read_me.txt</p><br

Combining species distribution models and population genomics underlines the determinants of range limitation in an emerging parasite

International audienceUnderstanding the drivers of species distribution is necessary in order to properly predict the future geographical ranges of colonizing species. Yet this task is challenging for species involved in intimate interactions, such as parasites, since their distribution is likely shaped by a complex interplay between environmental-related and host-related factors. Here we developed an original approach combining species distribution models (SDMs) and population genomics to test whether the local environmental conditions or the host genomic background most likely limits the colonization of an emerging freshwater fish ectoparasite, Tracheliastes polycolpus. We hypothesized that the absence of T. polycolpus in some areas may be due to an unsuitable environment in these areas (the 'environmental suitability hypothesis') and/or to the presence of resistant hosts in these areas (the 'genomic background hypothesis'). Using a SDM set at the French spatial extent, we first found that the environmental conditions of an uninfected area were as suitable for the parasite as those of infected areas. Then, using single nucleotide polymorphisms (SNPs) data at the host genome scale, we demonstrated that there was a strong association between the spatial occurrence of parasites and the host genomic background. In particular, the area in which the parasite was absent sustained a unique host population from a genomic standpoint, and ninety SNPs were significantly associated to the infection status (parasitized versus unparasitized) of individual hosts. We concluded that the spatial distribution of T. polycolpus (and its colonization potential) was more likely limited by intrinsic host characteristics associated to parasite resistance, rather than to the local environmental conditions. This study illustrates the usefulness of combining modeling and genomic approaches to reveal the determinants of species distribution and to improve predictions about their future ranges

A fine‐scale analysis reveals microgeographic hotspots maximizing infection rate between a parasite and its fish host

International audienceFor parasites, finding their hosts in vast and heterogeneous environments is a task that can be complex. Some parasite species rely on elaborate strategies to increase encounter rate with their hosts (e.g. behavioural modification of host), but others do not. For these parasites, a key issue is to reveal the processes that enable them to successfully find their hosts and complete their life cycles. Here, we tested the hypothesis that infective larvae of the freshwater ectoparasite Tracheliastes polycolpus are not homogeneously distributed along the river and preferentially occur in very specific microhabitats that maximize encounter rate, and hence infection rate, with their host fish. To do this, we combined an in situ experiment (caging) with an empirical survey carried out on the same sites to identify potential 'hotspots' of infection at the microgeographic scale and their environmental characteristics. Experimental and empirical results demonstrated that infections were not evenly distributed among microhabitats, and that infections were spatially aggregated in hotspots at a very fine spatial grain. We further found that certain combinations of environmental variables were consistently and nonlinearly associated with higher infection rate for both caged and wild-caught fish. Microhabitats characterized by very low or high stream velocities, associated with medium or very small substrate, respectively, and a deep water column were strongly and repeatedly associated with higher infection rates. These microhabitats could concentrate parasites and/or promote physical contact with the hosts. We conclude that the characteristics of some microhabitats could facilitate contact between hosts and parasites and explain how some parasites manage to find their hosts in complex environments

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

Schistosoma haematobium and Schistosoma bovisfirst generation hybrids undergo large gene expressions remodeling consistent with species compatibility

When two species hybridize, the two parental genomes are brought together and some alleles might interact for the first time. To the date, the extent of the transcriptomic changes in first hybrid generations, along with their functional outcome constitute an important knowledge gap especially in non-model organisms. Here we explored the molecular and functional outcomes of hybridization in first-generation hybrid between the blood fluke parasitesS. haematobiumandS. bovis. To this aim we fist assembled a hybrid reference transcriptome allowing us to measure gene expression in both parental species and hybrids to further described and quantified the profiles of gene expression encountered in hybrids. We identified large-scale gene expression remodeling since up to 55% of genes were differentially expressed in hybrids compared to at least one of the parental species. We further showed that intermediate level of expression in hybrids compared to parental species was the most prevalent expression profile (38% of genes) in agreement withS. haematobium x S. bovishigh genomic compatibility and limited divergence. Also, among the differentially expressed genes of each of the identified profiles (intermediate, under-, over-expressed, or matching the expression of one of the parental species), only a few biological processes were found enriched without patterns being consistent through crosses and sexes. Our findings suggest that hybrid heterosis could be due to change in expression of a large portion of random genes which affect various biological processes. Author SummaryWhen two species manage to produce a viable offspring, due to different parental genetic material, new allelic interactions might arise. We do not know much about how genes are expressed in such hybrids compared to their parental species and especially for non-model species. Here we gene expressions in first generation hybrids of two blood flukes’ parasitesSchistosoma haematobiumandS. bovis.We quantified and categorized gene differentially expressed in first generation hybrids. We showed that more than half the genes of the hybrids were differentially expressed compared to at least one of their parental species, hence showing major gene expression remodeling occurring during hybridization. However, the most common hybrid expression pattern was intermediate level of expression compared to parental species and various but no specific biological processes were associated with hybrids differentially expressed genes. We hypothesized that becauseS. haematobiumandS. bovisremain very compatible, when hybridizing many non-specific genes can have their expression level remodeled hence impacting the overall molecular machinery of the offspring while still sustaining highly operational hybrids

Experimental Infections Reveal Acquired Zoonotic Capacity of Human Schistosomiasis Trough Hybridization

International audienceWe are currently witnessing the endemization of urogenital schistosomiasis in southern Europe. The incriminated parasite is a hybrid between a human parasite and a livestock parasite. Using an experimental evolutionary protocol, we created hybrid lines from pure strains of both parasite species. We showed that the host spectrum of the human parasite is enlarged to the livestock parasite after genomic introgression. We also evidenced that the tropism of the parasites within the host changes and that some hybrid lines are more virulent than the parental strains. These results engage a paradigm shift from human to zoonotic transmission of urogenital schistosomiasis

Urogenital schistosomiasis in three different water access in the Senegal river basin: prevalence and monitoring praziquantel efficacy and re-infection levels

International audienceBackground: Urogenital schistosomiasis is a neglected tropical disease most prevalent in sub-Saharan Africa. In the Senegal river basin, the construction of the Diama dam led to an increase and endemicity of schistosomiasis. Since 2009, praziquantel has frequently been used as preventive chemotherapy in the form of mass administration to Senegalese school-aged children without monitoring of the treatment efficacy and the prevalence after re-infection. This study aims to determine the current prevalence of urogenital schistosomiasis (caused by Schistosoma haematobium), the efficacy of praziquantel, and the re-infection rates in children from five villages with different water access. Methods: The baseline prevalence of S. haematobium was determined in August 2020 in 777 children between 5 and 11 years old and a single dose of praziquantel (40 mg/kg) was administered to those positive. The efficacy of praziquantel and the re-infection rates were monitored 4 weeks and 7 months after treatment, respectively, in 226 children with a high intensity of infection at baseline. Results: At the baseline, prevalence was low among children from the village of Mbane who live close to the Lac de Guiers (38%), moderate among those from the villages of Dioundou and Khodit, which neighbor the Doue river (46%), and very high at Khodit (90.6%) and Guia (91.2%) which mainly use an irrigation canal. After treatment, the observed cure rates confirmed the efficacy of praziquantel. The lowest cure rate (88.5%) was obtained in the village using the irrigation canal, while high cure rates were obtained in those using the lake (96.5%) and the river (98%). However, high egg reduction rates (between 96.7 and 99.7%) were obtained in all the villages. The re-infection was significantly higher in the village using the canal (42.5%) than in the villages accessing the Lac de Guiers (18.3%) and the Doue river (14.8%). Conclusion: Praziquantel has an impact on reducing the prevalence and intensity of urogenital schistosomiasis. However, in the Senegal river basin, S. haematobium remains a real health problem for children living in the villages near the irrigation canals, despite regular treatment, while prevalence is declining from those frequenting the river and the Lac de Guiers

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

International audienceRecent studies have highlighted associations between diseases and host microbiota. It is yet extremely challenging-especially under natural conditions-to clarify whether the host microbiota promotes 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. Fin microbiota further got similar to that of the adult stage, and the free-living infective stage of the parasite during infection with a predominance of the Burkholderiaceae bacteria family. This suggests that Burkholderiaceae bacteria is involved in a co-infection process and possibly facilitate T. polycolpus infection. 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