Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar)

Abstract Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult. Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying inter-population differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factors.Peer reviewe

Footprints of directional selection in wild atlantic salmon populations: Evidence for parasite-driven evolution?

Mechanisms of host-parasite co-adaptation have long been of interest in evolutionary biology; however, determining the genetic basis of parasite resistance has been challenging. Current advances in genome technologies provide new opportunities for obtaining a genome-scale view of the action of parasite-driven natural selection in wild populations and thus facilitate the search for specific genomic regions underlying inter-population differences in pathogen response. European populations of Atlantic salmon (Salmo salar L.) exhibit natural variance in susceptibility levels to the ectoparasite Gyrodactylus salaris Malmberg 1957, ranging from resistance to extreme susceptibility, and are therefore a good model for studying the evolution of virulence and resistance. However, distinguishing the molecular signatures of genetic drift and environment-associated selection in small populations such as land-locked Atlantic salmon populations presents a challenge, specifically in the search for pathogen-driven selection. We used a novel genome-scan analysis approach that enabled us to i) identify signals of selection in salmon populations affected by varying levels of genetic drift and ii) separate potentially selected loci into the categories of pathogen (G. salaris)-driven selection and selection acting upon other environmental characteristics. A total of 4631 single nucleotide polymorphisms (SNPs) were screened in Atlantic salmon from 12 different northern European populations. We identified three genomic regions potentially affected by parasite-driven selection, as well as three regions presumably affected by salinity-driven directional selection. Functional annotation of candidate SNPs is consistent with the role of the detected genomic regions in immune defence and, implicitly, in osmoregulation. These results provide new insights into the genetic basis of pathogen susceptibility in Atlantic salmon and will enable future searches for the specific genes involved

Heritability estimation via molecular pedigree reconstruction in a wild fish population reveals substantial evolutionary potential for sea age at maturity, but not size within age classes

While evolutionary responses require heritable variation, estimates of heritability (h(2)) from wild fish populations remain rare. A 20-year molecular pedigree for a wild Scottish population of Atlantic salmon (Salmo salar) was used to investigate genetic contributions to (co) variation in two important, correlated, phenotypic traits: "sea age" (number of winters spent at sea prior to spawning) and size-at-maturity (body length just prior to spawning). Sea age was strongly heritable (h(2) = 0.51) and size exhibited moderate heritability (h(2) = 0.27). A very strong genetic correlation (r(G) = 0.96) between these traits implied the same functional loci must underpin variation in each. Indeed, body size within sea ages had much lower heritability that did not differ significantly from zero. Thus, within wild S. salar populations, temporal changes in sea age composition could reflect evolutionary responses, whereas rapid changes of body size within sea ages are more likely due to phenotypic plasticity. These inheritance patterns will influence the scope of evolutionary responses to factors such as harvest or climate change and, hence, have management implications for salmonid populations comprising a mix of sea ages.Peer reviewe

Commencement Program, August (1966)

https://red.mnstate.edu/commencement/1105/thumbnail.jp

Polygenic and major-locus contributions to sexual maturation timing in Atlantic salmon

Sexual maturation timing is a life-history trait central to the balance between mortality and reproduction. Maturation may be triggered when an underlying compound trait, called liability, exceeds a threshold. In many different species and especially fishes, this liability is approximated by growth and body condition. However, environmental vs. genetic contributions either directly or via growth and body condition to maturation timing remain unclear. Uncertainty exists also because the maturation process can reverse this causality and itself affect growth and body condition. In addition, disentangling the contributions of polygenic and major loci can be important. In many fishes, males mature before females, enabling the study of associations between male maturation and maturation-unbiased female liability traits. Using 40 Atlantic salmon families, longitudinal common-garden experimentation, and quantitative genetic analyses, we disentangled environmental from polygenic and major locus (vgll3) effects on male maturation, and sex-specific growth and condition. We detected polygenic heritabilities for maturation, growth, and body condition, and vgll3 effects on maturation and body condition but not on growth. Longitudinal patterns for sex-specific phenotypic liability, and for genetic variances and correlations between sexes suggested that early growth and condition indeed positively affected maturation initiation. However, towards spawning time, causality appeared reversed for males whereby maturation affected growth negatively and condition positively via both the environmental and genetic effects. Altogether, the results indicate that growth and condition are useful traits to study liability for maturation initiation, but only until maturation alters their expression, and that vgll3 contributes to maturation initiation via condition.Peer reviewe

Modularity Facilitates Flexible Tuning of Plastic and Evolutionary Gene Expression Responses during Early Divergence

Gene expression changes have been recognized as important drivers of adaptation to changing environmental conditions. Little is known about the relative roles of plastic and evolutionary responses in complex gene expression networks during the early stages of divergence. Large gene expression data sets coupled with in silico methods for identifying coexpressed modules now enable systems genetics approaches also in nonmodel species for better understanding of gene expression responses during early divergence. Here, we combined gene coexpression analyses with population genetics to separate plastic and population (evolutionary) effects in expression networks using small salmonid populations as a model system. We show that plastic and population effects were highly variable among the six identified modules and that the plastic effects explained larger proportion of the total eigengene expression than population effects. A more detailed analysis of the population effects using a Q(ST)-F-ST comparison across 16,622 annotated transcripts revealed that gene expression followed neutral expectations within modules and at the global level. Furthermore, two modules showed enrichment for genes coding for early developmental traits that have been previously identified as important phenotypic traits in thermal responses in the same model system indicating that coexpression analysis can capture expression patterns underlying ecologically important traits. We suggest that module-specific responses may facilitate the flexible tuning of expression levels to local thermal conditions. Overall, our study indicates that plasticity and neutral evolution are the main drivers of gene expression variance in the early stages of thermal adaptation in this system

Biodiversity conservation across scales: lessons from a science–policy dialogue

One of the core challenges of biodiversity conservation is to better understand the interconnectedness and interactions of scales in ecological and governance processes. These interrelationships constitute not only a complex analytical challenge but they also open up a channel for deliberative discussions and knowledge exchange between and among various societal actors which may themselves be operating at various scales, such as policy makers, land use planners, members of NGOs, and researchers. In this paper, we discuss and integrate the perspectives of various disciplines academics and stakeholders who participated in a workshop on scales of European biodiversity governance organised in Brussels in the autumn of 2010. The 23 participants represented various governmental agencies and NGOs from the European, national, and sub-national levels. The data from the focus group discussions of the workshop were analysed using qualitative content analysis. The core scale-related challenges of biodiversity policy identified by the participants were cross-level and cross-sector limitations as well as ecological, social and social-ecological complexities that potentially lead to a variety of scale-related mismatches. As ways to address these cha- llenges the participants highlighted innovations, and an aim to develop new interdisciplinary approaches to support the processes aiming to solve current scale challenges

Response of a low elevation carbonate lake in the Yucatan Peninsula (Mexico) to climatic and human forcings

The importance of climate change, specifically drought, across the Maya region in the northern Neotropics, remains a topic of lively debate. Part of this discussion hinges on the coherency of response to climatic variability across different archives and proxies. In this paper we present a 6600-year palaeolimnological record from Yaal Chac, a carbonate lake (known locally as a cenote) in the northern lowlands of the Yucatan Peninsula, 2‰), but show no covariation with δ13C. A major transition occurs at ca. 4360 cal yr BP, with a change to generally more organic sediments and increased variability in all proxies. Although direct evidence for anthropogenic activity in the Yaal Chac catchment is limited, it seems feasible that human impact was affecting the system. Comparison with other records from the Northern Maya lowlands and the wider region shows little coherence in the mid Holocene, when Yaal Chac seems to have been quite stable, but possibly responsive to increased climatic seasonality, driving the production of seasonal laminae. In the late Holocene, when the climate was generally more variable, there is more coherence between Yaal Chac and other regional records, including the so called Pan Caribbean Dry Period (3500–2500 cal yr BP) and the droughts of the late Pre-Classic period (1800–1600 cal yr BP). The Yaal Chac record shows no evidence of drought at the time of either the Maya ‘hiatus’ or the Maya ‘collapse’ of the Terminal Classic, but does record drying from the 14th to 19th centuries CE, in keeping with other proxy and historical records. This new record from Yaal Chac highlights the spatial variability of responses to climate forcings and the importance of recognising individual system sensitivity

Single nucleotide polymorphisms to discriminate different classes of hybrid between wild Atlantic salmon and aquaculture escapees

Many wild Atlantic salmon (Salmo salar) populations are threatened by introgressive hybridization from domesticated fish that have escaped from aquaculture facilities. A detailed understanding of the hybridization dynamics between wild salmon and aquaculture escapees requires discrimination of different hybrid classes; however, markers currently available to discriminate the two types of parental genome have limited power to do this. Using a high-density Atlantic salmon single nucleotide polymorphism (SNP) array, in combination with pooled-sample allelotyping and an F-st outlier approach, we identified 200 SNPs that differentiated an important Atlantic salmon stock from the escapees potentially hybridizing with it. By simulating multiple generations of wild-escapee hybridization, involving wild populations in two major phylogeographic lineages and a genetically diverse set of escapees, we showed that both the complete set of SNPs and smaller subsets could reliably assign individuals to different hybrid classes up to the third hybrid (F3) generation. This set of markers will be a useful tool for investigating the genetic interactions between native wild fish and aquaculture escapees in many Atlantic salmon populations