Recent improvements in the speed, cost and accuracy of next generation sequencing are revolutionizing the discovery of single nucleotide polymorphisms (SNPs). SNPs are increasingly being used as an ...addition to the molecular ecology toolkit in nonmodel organisms, but their efficient use remains challenging. Here, we discuss common issues when employing SNP markers, including the high numbers of markers typically employed, the effects of ascertainment bias and the inclusion of nonneutral loci in a marker panel. We provide a critique of considerations specifically associated with the application and population genetic analysis of SNPs in nonmodel taxa, focusing specifically on some of the most commonly applied methods.
A whole genome duplication occurred in the ancestor of all salmonid fishes some 50-100 million years ago. Early inheritance studies with allozymes indicated that loci in the salmonid genome are ...inherited disomically in females. However, some pairs of duplicated loci showed patterns of inheritance in males indicating pairing and recombination between homeologous chromosomes. Nearly 20% of loci in the salmonid genome are duplicated and share the same alleles (isoloci), apparently due to homeologous recombination. Half-tetrad analysis revealed that isoloci tend to be telomeric. These results suggested that residual tetrasomic inheritance of isoloci results from homeologous recombination near chromosome ends and that continued disomic inheritance resulted from homologous pairing of centromeric regions. Many current genetic maps of salmonids are based on single nucleotide polymorphisms and microsatellites that are no longer duplicated. Therefore, long sections of chromosomes on these maps are poorly represented, especially telomeric regions. In addition, preferential multivalent pairing of homeologs from the same species in F1 hybrids results in an excess of nonparental gametes (so-called pseudolinkage). We consider how not including duplicated loci has affected our understanding of population and evolutionary genetics of salmonids, and we discuss how incorporating these loci will benefit our understanding of population genomics.
Studying the effect of similar environments on diverse genetic backgrounds has long been a goal of evolutionary biologists with studies typically relying on experimental approaches. Pink salmon, a ...highly abundant and widely ranging salmonid, provide a naturally occurring opportunity to study the effects of similar environments on divergent genetic backgrounds due to a strict two‐year semelparous life history. The species is composed of two reproductively isolated lineages with overlapping ranges that share the same spawning and rearing environments in alternate years. We used restriction‐site‐associated DNA (RAD) sequencing to discover and genotype approximately 8000 SNP loci in three population pairs of even‐ and odd‐year pink salmon along a latitudinal gradient in North America. We found greater differentiation within the odd‐year than within the even‐year lineage and greater differentiation in the southern pair from Puget Sound than in the northern Alaskan population pairs. We identified 15 SNPs reflecting signatures of parallel selection using both a differentiation‐based method (BAYESCAN) and an environmental correlation method (BAYENV). These SNPs represent genomic regions that may be particularly informative in understanding adaptive evolution in pink salmon and exploring how differing genetic backgrounds within a species respond to selection from the same natural environment.
Salmonids are an important cultural and ecological resource exhibiting near worldwide distribution between their native and introduced range. Previous research has generated linkage maps and genomic ...resources for several species as well as genome assemblies for two species. We first leveraged improvements in mapping and genotyping methods to create a dense linkage map for Chinook salmon Oncorhynchus tshawytscha by assembling family data from different sources. We successfully mapped 14 620 SNP loci including 2336 paralogs in subtelomeric regions. This improved map was then used as a foundation to integrate genomic resources for gene annotation and population genomic analyses. We anchored a total of 286 scaffolds from the Atlantic salmon genome to the linkage map to provide a framework for the placement 11 728 Chinook salmon ESTs. Previously identified thermotolerance QTL were found to colocalize with several candidate genes including HSP70, a gene known to be involved in thermal response, as well as its inhibitor. Multiple regions of the genome with elevated divergence between populations were also identified, and annotation of ESTs in these regions identified candidate genes for fitness related traits such as stress response, growth and behaviour. Collectively, these results demonstrate the utility of combining genomic resources with linkage maps to enhance evolutionary inferences.
Geographic distributions of most temperate marine fishes are affected by postglacial recolonisation events, which have left complex genetic imprints on populations of marine species. This study ...investigated population structure and demographic history of European sprat (Sprattus sprattus L.) by combining inference from both mtDNA and microsatellite genetic markers throughout the species' distribution. We compared effects from genetic drift and mutation for both genetic markers in shaping genetic differentiation across four transition zones. Microsatellite markers revealed significant isolation by distance and a complex population structure across the species' distribution (overall θ(ST)=0.038, P<0.01). Across transition zones markers indicated larger effects of genetic drift over mutations in the northern distribution of sprat contrasting a stronger relative impact of mutation in the species' southern distribution in the Mediterranean region. These results were interpreted to reflect more recent divergence times between northern populations in accordance with previous findings. This study demonstrates the usefulness of comparing inference from different markers and estimators of divergence for phylogeographic and population genetic studies in species with weak genetic structure, as is the case in many marine species.
Factors such as oceanographic retention, isolation by distance and secondary contact zones have, among others, been suggested to explain the low, but statistically significant, neutral population ...structure observed in many marine fishes. European sprat Sprattus sprattus L. is not known to display philopatric spawning behaviour or to exhibit local retention of eggs and larvae. It thus constitutes a good model for studying population structure in a characteristic small pelagic fish with high dispersal potential and an opportunistic life history. We analysed 931 specimens of sprat from 9 spawning locations in and around the North Sea and Baltic Sea area and from a geographically distant population from the Adriatic Sea. Analyses of 9 microsatellite loci revealed a sharp genetic division separating samples from the northeastern Atlantic Ocean and the Baltic Sea (pairwise f = 0.019 to 0.035), concurring with a steep salinity gradient. We found, at most, weak structure among samples within the northeastern Atlantic region and within the Baltic Sea (pairwise f = 0.001 to 0.009). The Adriatic Sea population was highly differentiated from all northern samples (pairwise f = 0.071 to 0.092). Overall, the observed population structure resembles that of most other marine fishes studied in the North and Baltic Sea areas. Nevertheless, spatially explicit differences are observed among species, probably reflecting specific life histories. Such fine-scale population structures should be taken into account when considering complex ecosystem functions, e.g. in multispecies stock management.
The concept of a holobiont, a host organism and its associated microbial communities, encapsulates the vital role the microbiome plays in the normal functioning of its host. Parasitic infections can ...disrupt this relationship, leading to dysbiosis. However, it is increasingly recognized that multicellular parasites are themselves holobionts. Intestinal parasites share space with the host gut microbiome, creating a system of nested microbiomes within the primary host. However, how the parasite, as a holobiont, interacts with the host holobiont remains unclear, as do the consequences of these interactions for host health. Here, we used 16S amplicon and shotgun metagenomics sequencing to characterize the microbiome of the intestinal cestode
and its effect on the gut microbiome of its primary host, Atlantic salmon. Our results indicate that cestode infection is associated with salmon gut dysbiosis by acting as a selective force benefiting putative pathogens and potentially introducing novel bacterial species to the host. Our results suggest that parasitic cestodes may themselves be holobionts nested within the microbial community of their holobiont host, emphasizing the importance of also considering microbes associated with parasites when studying intestinal parasitic infections.
The importance of the parasite microbiome is gaining recognition. Of particular concern is understanding how these parasite microbiomes influence host-parasite interactions and parasite interactions with the vertebrate host microbiome as part of a system of nested holobionts. However, there are still relatively few studies focusing on the microbiome of parasitic helminths in general and almost none on cestodes in particular, despite the significant burden of disease caused by these parasites globally. Our study provides insights into a system of significance to the aquaculture industry, cestode infections of Atlantic salmon and, more broadly, expands our general understanding of parasite-microbiome-host interactions and introduces a new element, the microbiome of the parasite itself, which may play a critical role in modulating the host microbiome, and, therefore, the host response, to parasite infection.
Animal protein production is increasingly looking towards microbiome-associated services such as the design of new and better probiotic solutions to further improve gut health and production ...sustainability. Here, we investigate the functional effects of bacteria-based pro- and synbiotic feed additives on microbiome-associated functions in relation to growth performance in the commercially important rainbow trout (Oncorhynchus mykiss). We combine complementary insights from multiple omics datasets from gut content samples, including 16S bacterial profiling, whole metagenomes, and untargeted metabolomics, to investigate bacterial metagenome-assembled genomes (MAGs) and their molecular interactions with host metabolism.
Our findings reveal that (I) feed additives changed the microbiome and that rainbow trout reared with feed additives had a significantly reduced relative abundance of the salmonid related Candidatus Mycoplasma salmoninae in both the mid and distal gut content, (II) genome resolved metagenomics revealed that alterations of microbial arginine biosynthesis and terpenoid backbone synthesis pathways were directly associated with the presence of Candidatus Mycoplasma salmoninae, and (III) differences in the composition of intestinal microbiota among feed types were directly associated with significant changes of the metabolomic landscape, including lipids and lipid-like metabolites, amino acids, bile acids, and steroid-related metabolites.
Our results demonstrate how the use of multi-omics to investigate complex host-microbiome interactions enable us to better evaluate the functional potential of probiotics compared to studies that only measure overall growth performance or that only characterise the microbial composition in intestinal environments. Video Abstract.
Aquaculture will play an essential role in feeding a growing human population, but several biological challenges impede sustainable growth of production. Emerging evidence across all areas of life ...has revealed the importance of the intimate biological interactions between animals and their associated gut microbiota. Based on challenges in aquaculture, we leverage current knowledge in molecular biology and host microbiota interactions to propose an applied holo-omic framework that integrates molecular data including genomes, transcriptomes, epigenomes, proteomes, and metabolomes for analyzing fish and their gut microbiota as interconnected and coregulated systems. With an eye towards aquaculture, we discuss the feasibility and potential of our holo-omic framework to improve growth, health, and sustainability in any area of food production, including livestock and agriculture.
Both the host genotype and gut microbiota of an animal play significant roles in shaping key phenotypes of aquacultural relevance, including growth metabolism and immune functions.
Traditional approaches to improve production have relied on selecting for direct genotype–phenotype correlations or on directly modulating gut microbiome communities.
The hologenome theory argues that the genomes of host organisms and their associated microbial communities are subject to biological interactions and cannot be viewed independently.
The gut microbiota can be viewed as a collection of genotypes contributing to holobiont phenotypes linked to the host genotype, and any attempts to modify the gut microbiota can only be successful in the context of the host genotype ‘environment’.
A hologenomic approach to aquaculture has potential to improve growth, health, and sustainable production.
From ontogenesis to homeostasis, the phenotypes of complex organisms are shaped by the bidirectional interactions between the host organisms and their associated microbiota. Current technology can ...reveal many such interactions by combining multi-omic data from both hosts and microbes. However, exploring the full extent of these interactions requires careful consideration of study design for the efficient generation and optimal integration of data derived from (meta)genomics, (meta)transcriptomics, (meta)proteomics, and (meta)metabolomics. In this perspective, we introduce the holo-omic approach that incorporates multi-omic data from both host and microbiota domains to untangle the interplay between the two. We revisit the recent literature on biomolecular host-microbe interactions and discuss the implementation and current limitations of the holo-omic approach. We anticipate that the application of this approach can contribute to opening new research avenues and discoveries in biomedicine, biotechnology, agricultural and aquacultural sciences, nature conservation, as well as basic ecological and evolutionary research.
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Microbiome; Evolutionary Biology
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