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Erkinaro, J.

Publications and source records attributed to Erkinaro, J..

At least 19 recordsLinked to original sources

Interaction of two tightly linked loci in an adaptive genomic hotspot explains exploration behavior in juvenile Atlantic salmon in freshwater.

O_LIThe traits that are important for adaptation may exhibit genetic correlation due to pleiotropy or as a result of linkage. Understanding the genetic architecture of such correlations is important for predicting the selection response of populations. Exploration in fishes is a behavioral trait by which individuals may find habitats with better foraging and growth opportunities that subsequently improve their fitness. For example, in Atlantic salmon (Salmo salar), all individuals originate in spawning rivers where females lay eggs, but some juveniles migrate to small tributaries which are not spawning areas but provide favorable habitat patches for young salmon. The increased growth in these nursery streams may facilitate earlier sexual maturation, implying a potential correlation between exploration and maturation traits. C_LIO_LIIn this study, by sampling juveniles from two wild populations in the large Teno River catchment in northernmost Fennoscandia, we tested the genetic association between exploration behavior with nursery streams across four SNPs that span a 70-kb long genomic region with a major effect on age at maturity variation. Three of these SNPs are missense mutations in the vgll3 and akap11 genes, and one SNP tags a putative regulatory region with the strongest association with the age-at-maturity trait. C_LIO_LIWe show that the exploration behavior was linked to the genomic region in one of the two studied populations. However, the genetic association was substantial in the missense SNP located in the akap11 gene, which is farthest away from the vgll3 SNPs and previously ruled out as being linked to the age at maturity. We also detected a marginal interaction effect between SNPs in the vgll3 gene and akap11, indicating a potentially complex genetic architecture underlying the trait variation. C_LIO_LIOur results suggest that exploration and age at maturity are co-inherited within the same haplotype block, but we find no evidence for direct causality. These two traits may form a co-adapted trait complex that may be instrumental in local adaptation processes. C_LI

ecology↗

Food quality and vgll3 genotype influence reproductive traits in female Atlantic salmon

Age at maturity is an important factor contributing to life-history diversity. In Atlantic salmon, this trait often shows sex-specific variation, but female salmon are seldom included in experimental studies of maturation. As a result, there is a gap in our knowledge of how different genetic and environmental factors affect female maturation. Using a 4-year common-garden experiment, we assessed the influence of diet (low-fat vs. control) and vgll3 (a candidate gene in a genomic region known to influence age at maturity in Atlantic salmon) on maturation and related phenotypic traits of female Atlantic salmon from two 2nd-generation hatchery populations. We found the early-maturation-associated vgll3*E allele to be associated with higher probability of maturation. Heritability of maturation was estimated to be 0.295 with vgll3s contribution to phenotypic variance being [~]2%. In addition, both body size and body condition measured in the spring prior to spawning influenced maturation. Body condition, in turn, was influenced by population and diet. The northern Oulu population and the low-fat diet were associated with lower body condition compared to the southern Neva population and the control diet. Moreover, there was an interaction between population and diet on body condition, suggesting that populations may respond differently to nutrient availability. These results broaden our understanding of the processes underlying maturation and demonstrate that genes and environment interact to shape age at maturity in female Atlantic salmon.

evolutionary biology↗

Large effect life-history genomic regions are associated with functional morphological traits in Atlantic salmon

Understanding pleiotropic architectures of phenotypes is instrumental for identifying the functional basis of adaptive genetic variation in the wild. Life-history variation may have a morphological basis that mediates resource acquisition allocation pathways, but identifying the underlying genetic basis of such traits is challenging. Using Atlantic salmon juveniles reared in common garden conditions, we test if two life-history associated loci in Atlantic salmon, six6 and vgll3, are also associated with functional morphological traits. These loci had previously shown to exhibit strong signals of adaptation and are highly correlated with sea age at maturity. We show that genetic variation at the vgll3 locus is linked to variation in morphological traits that underlie swimming performance, along a trade-off axis between efficient cruising and maneuvering, while the genetic variation at the six6 locus was linked to variation in body-head proportions suggesting the potential functional importance of these traits for resource acquisition efficiency. However, the direction of changes in morphological traits associated with late-vs. early-maturing alleles was not always consistent with the expected direction of an effect to maturation timing. Our results reveal a complex morphological landscape associated with the genetic variation in these loci, possibly as a result of pleiotropy or linkage across these genomic regions.

ecology↗

A single nucleotide polymorphism genotyping panel for efficient genetic stock identification of the Teno river Atlantic salmon (Salmo salar) population complex

A new single nucleotide polymorphism (SNP) panel for genetic stock identification in the Teno River Atlantic salmon fishery was developed, with a view to improving on an existing microsatellite panel. Twenty-two genetically differentiated reporting units were proposed based on population genetic analyses of 1212 individuals collected at 37 locations in the river and genotyped for > 33,000 genome-wide SNPs. A small subset of these SNPs was selected for GSI using an iterative process that considered their diversity and differentiation across reporting units. A genotyping-by-sequencing assay was developed to simultaneously genotype 180 of these GSI SNPs plus a sexing marker. This new SNP panel showed comparative GSI power to the microsatellite panel, with anticipated improvements in terms of cost, speed, and robustness and transferability across laboratories and genotyping platforms. Mixed stock analysis of the 2018 Teno River salmon catch using the new panel inferred all 22 reporting units to contribute to the fishery. Estimated catch proportions positively scaled with an independent estimate of reporting unit productivity: target spawning female biomass. This demonstrates the usefulness and efficiency of the 180 SNP panel for Atlantic salmon GSI in the Teno River system. If conducted on a regular basis, GSI can enable fine-tuning of management strategies to promote sustainable fishing.

evolutionary biology↗

Sex-, development-, and nutrition-dependent expression of a major age-at-maturity gene in Atlantic salmon

Sexual maturation is a key process in the life history of an organism and is influenced by both genetic and environmental factors. In Atlantic salmon (Salmo salar), alternative alleles at the gene vgll3 have been found to associate with a large proportion of the variation in maturation age, yet the molecular and physiological mechanisms of this association are still largely unknown. Here, we investigated the mechanisms by which genetic variation in this major age-at-maturity gene translated into phenotypic variation. We established a time series of gonadal vgll3 mRNA expression in male and female Atlantic salmon in a common garden setting, starting at the prepubertal stage and spanning multiple spawning seasons. We found that vgll3 mRNA expression is reduced in early-maturing males and females. However, for the second spawning season, vgll3 expression increased with gonadal development in males, but eventually decreased in females. Expression of vgll3 had context-dependent correlations with expression of amh and lhr. We also found signs of reduced testicular vgll3 expression in a low-fat feed treatment. By significantly widening the scope of our knowledge on temporal vgll3 expression dynamics, our results exemplify that major-effect genes may use different pathways in sexes but achieve similar outcomes.

genetics↗

A salmon fish model reveals genetic signals in brain associated with early maturation

Emerging evidence suggests a link between adiposity and early maturation, potentially impacting hormonal signaling pathways governing puberty timing. Fish models have proven invaluable in studying these processes, given their genetic and physiological similarities to humans. In Atlantic salmon, in addition to being linked with environmental shifts and lipid reserves, the timing of sexual maturation also has a strong genetic basis. A gene encoding a co-factor of Hippo pathway, vgll3, is a major determinant of maturation timing in salmon, and the same gene was found to be associated with maturation timing in humans. Intriguingly, vgll3 also inhibits adipogenesis in mice. Recent studies in salmon revealed correlations between vgll3 genotypes and reproductive axis gene expression, possibly modulated through the Hippo signaling pathway. The Hippo pathway is known for its role in sexual maturation and adipogenesis and responds to environmental cues such as dietary fat and temperature. In this study, we employed a custom gene expression panel in male Atlantic salmon with different vgll3 early (E) and late (L) maturation genotypes testing components of this pathway in brain at immature and mature stages. We found increased brain expression of a major Hippo pathway kinase (lats1b) and melanocortin receptor encoding genes (mc4ra and mc4rc) in individuals with early (E) maturation genotypes of vgll3 before maturation development of testes. Moreover, we found components and interacting partners of Hippo pathway showing differential expression in brain of individuals with early (E) and late (L) vgll3 genotypes prior to maturation. This could indicate extensive and complex roles of Hippo pathway in brain processes required for preparing for [the onset of] maturation at upstream of reproductive axis. This study elucidates molecular mechanisms underpinning early maturation, and for the first time in fish, offering insights into detecting it at molecular level in brain before visible gonadal changes occur.

genetics↗

A complex mechanism translating variation of a simple genetic architecture into alternative life-histories

Linking genes to traits is a central goal in biology. Despite progress in discovering genes associated with trait differences, a poor understanding of the functional mechanisms underlying genetic associations leaves us critically far from connecting genetic and phenotypic variation. This knowledge-gap is particularly large in multifaceted phenotypes of ecological relevance such as life-history traits. Using a multiomic dissection of the genotype-phenotype association in a large-effect maturation age gene - the transcription cofactor vestigial-like 3 (vgll3) - in Atlantic salmon (Salmo salar), we show that vgll3 mediates concerted changes of distinct molecular phenotypes associated with puberty in male gonads. Vgll3 genotype conferring early maturity upregulates key genes controlling androgen production, cellular energy and adiposity, and TGF-{beta} signaling, among others, thereby increasing the likelihood of earlier pubertal initiation. Genotype-dependent developmental trajectories are produced through VGLL3 interaction with distinct transcription factors, thus coordinating differential activation of regulatory pathways. These results reveal a genetically simple, yet functionally complex, architecture underlying alternative life-histories where variation in a single major effect gene produces pleiotropic variation in a spectrum of cellular traits. Our results further suggest that evolution in correlated phenotypes such as exemplified by alternative life history strategies may be mediated by a surprisingly simple genetic architecture.

evolutionary biology↗

Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link between seasonal changes, energy balance and age at maturity

Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status. Lipid metabolism is at the heart of this transition since lipids are the main energy storing molecules. The balance between lipogenesis (lipid accumulation) and lipolysis (lipid use) determines energy status transitions. A genomic region containing a transcription co-factor of the Hippo pathway, vgll3, is the main determinant of maturation timing in Atlantic salmon. Interestingly, vgll3 acts as an inhibitor of adipogenesis in mice and its genotypes are potentially associated with seasonal heterochrony in lipid storage and usage in juvenile Atlantic salmon. Here, we explored changes in expression of more than 300 genes directly involved in the processes of adipogenesis, lipogenesis and lipolysis, as well as the Hippo pathway in the adipose tissue of immature and mature Atlantic salmon with distinct vgll3 genotypes. We found molecular evidence consistent with a scenario in which immature males exhibiting vgll3 genotype specific seasonal direction of change in their lipid profiles. We also identified components of the Hippo signaling pathway as potential major drivers of vgll3 genotype specific differences in adipose tissue gene expression. This study demonstrates the importance of adipose gene expression patterns for directly linking environmental changes with energy balance and age at maturity through genetic factors bridging lipid metabolism, seasonality and sexual maturation.

physiology↗

Genotype-specific variation in seasonal body condition at a large-effect maturation locus

O_LIOrganisms utilize varying lipid resource allocation strategies as a means to survive seasonal environmental changes and life-history stage transitions. In Atlantic salmon, a certain lipid threshold is needed to initiate sexual maturation. Because of this, an individuals maturation schedule may be affected by changes in temperature and food availability across the seasons that create natural fluctuations of lipid reserves. C_LIO_LIRecent studies have found a genome region, including the gene vgll3, that explains a large proportion of variation for size and age at maturity. Vgll3 encodes a transcription co-factor that acts as an inhibitor of adipogenesis in mice and also affects condition factor and other phenotypes in juvenile salmon. However, even with many studies investigating varying temperature effects, there is a lack of temporal studies examining the effects of seasonality on such phenotypes, nor have the effects of vgll3 genotype on condition factor and maturation in different temperatures at different life stages. C_LIO_LIHere, we investigate the influence of different larval and juvenile incubation temperatures, vgll3 genotype and their interactions on juvenile salmon phenotypes including body condition, and sexual maturation rate. We reared Atlantic salmon for 2 years in varying temperatures with an average 1.76 {degrees}C difference between warm and cold treatments in four different larval-juvenile phase treatment groups (Warm-Warm, Warm-Cold, Cold-Warm, and Cold-Cold) until the first occurrence of maturation in males. C_LIO_LIWe found no effect of larval temperature on the measured phenotypes or maturation rate, suggesting the occurrence of growth compensation over the course of the experiment. Agreeing with previous studies, an increased maturation rate was observed in individuals of the warm juvenile temperature treatment. C_LIO_LIIn addition, we observed differences in condition factor associated with vgll3 genotype, whereby vgll3*EE individuals (the genotype associated with early maturation) had a less variable condition factor across the seasons compared to the vgll3*LL (associated with late maturation) individuals. C_LIO_LIThis result suggests a vgll3 influence on resource acquisition and allocation strategies, possibly linked with the early maturation process, with individuals carrying the early maturation vgll3 genotype having a higher early maturation rate and a higher condition factor in the spring. C_LI

evolutionary biology↗

Temperature and dietary energy content influence female maturation age and egg nutritional content in Atlantic salmon

The environment experienced by a female influences reproductive traits in many species of fish. Environmental factors such as temperature and diet are not only important mediators of female maturation and reproduction but also of egg traits and offspring fitness through maternal provisioning. In this study, we use three-year-old, tank-reared, Atlantic salmon from two Finnish populations to investigate the effect of temperature and diet on maturation and egg traits. We show that a temperature difference of 2{degrees}C is sufficient to delay maturation in female Atlantic salmon whereas a 22% reduction in dietary energy content had no effect on maturation. Diet did not influence the body size, condition, or fecundity of the mature females or the size or protein content of the eggs. However, a higher energy diet increased egg lipid content. Neither female body size nor condition were associated with egg size or fat/protein composition. Our results indicate that female salmon that have a poorer diet in terms of energy content may have a reproductive disadvantage due to lower energy provisioning of eggs. This disadvantage has the potential to translate into fitness consequences for their offspring.

ecology↗

Strong effects of temperature, population and age-at-maturity genotype on maturation probability for Atlantic salmon in a common garden setting

O_LIAge at maturity is a key life history trait and involves a trade-off between survival risk and reproductive investment, has close connections to fitness, and is an important factor for population structures. Temperature can have a dramatic influence on life history in ectotherms, but this influence may differ between populations. While an increasing number of studies have examined population-dependent reactions with temperature, few have investigated this in the context of maturation timing. C_LIO_LIAtlantic salmon is a highly relevant study species for improving understanding of this topic as it displays considerable variation in life-history strategies, including maturation timing. Additionally, a large amount of this variation in maturation timing has been associated with a genomic region including the strong candidate gene vgll3, but the effect of this gene in the context of different environments and populations has not been studied. C_LIO_LIUsing a large-scale common-garden experiment, we find strong effects of temperature, population, and vgll3 genotype on maturation in 2-year-old male Atlantic salmon. Observed maturation probability was 4.8 times higher in individuals reared at a mean temperature of 8.6{degrees}C compared to 6.9{degrees}C. This temperature effect was population-specific and was higher in the southern population compared to the northern population, potentially due to a higher intrinsic growth in the southern population as well as growth-temperature interaction. C_LIO_LIThe early-maturation vgll3*E associated with a significantly higher maturation probability, but there was no vgll3-interaction with temperature or population. C_LIO_LIBoth body condition and body mass associated strongly with maturation; the body-condition association was stronger in fish carrying the vgll3*E allele, and the body mass association was only present in the warm treatment. C_LIO_LIOur findings demonstrate that the relative effect of vgll3 on maturation timing is similar for two populations and two thermal environments and gives new perspectives on the relative effect of vgll3 compared to such influences. Additionally, we show that populations can vary in their response to temperature change in terms of maturation timing, and that high intrinsic growth could potentially be associated with higher thermal sensitivity for life history variation. C_LI

evolutionary biology↗

Genetic stock identification reveals greater use of an oceanic feeding ground around the Faroe Islands by multi-sea winter Atlantic salmon.

There is a general paucity of knowledge regards spatial variation in marine resource use for many taxa, even those of high socio-economic importance such as Atlantic salmon. While it is known that the oceans around the Faroe Islands support a salmon feeding ground, the relative use of this feeding ground by different age classes across different stocks remains largely unexplored. Using a combination of genetic stock assignment and run-reconstruction models, we observed a consistent pattern whereby the proportion of multi-sea winter (MSW) salmon for a given reporting group was substantially greater around the Faroes than the MSW proportion for that reporting groups among the prefisheries abundance. Surprisingly, MSW fish from Ireland and UK were as likely to occur around the Faroes as were MSW fish from more north-eastern regions such as the Teno river and the Barents and White Seas. MSW fish from Southern Norway were the most likely to be caught at the Faroes. While 1SW salmon from Ireland and UK as well as from Southern Norway occurred at similar rates around the Faroes, 1SW fish from more north-eastern reporting groups were nearly entirely absent from the same feeding ground. In combination with previous studies that examine the marine distribution of Atlantic salmon, our results strongly indicate that the oceans around the Faroes play host to a predominantly MSW salmon feeding ground and that use of this resource varies both within the age classes of a given stock as well as between different stocks. Furthermore, these results suggest that MSW fish from certain stocks might preferentially undertake migrations to the Faroes. Variation in spatial resource use may help to buffer salmon stocks against localised negative changes in marine conditions.

ecology↗

Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar).

One of the most important life-history continuums is the fast-slow axis, where "fast" individuals mature earlier than "slow" individuals. "Fast" individuals are predicted to be more active than "slow" individuals; high activity is required to maintain a fast life-history strategy. Recent meta-analyses revealed mixed evidence for such integration. Here, we test whether known life-history genotypes differ in activity expression by using Atlantic salmon (Salmo salar) as a model. In salmon, variation in Vgll3, a transcription co-factor, explains [~]40% of variation in maturation timing. We predicted that the allele related to early maturation (vgll3*E) would be associated with increased activity. We used an automated surveillance system to follow [~]1900 juveniles including both migrants and non-migrants (i.e. smolt and parr fish, respectively) in semi-natural conditions over 31 days ([~]580 000 activity measurements). Against our prediction, vgll3 did not explain variation in activity in pooled migrant and non-migrant data. However, in migrants, vgll3 explained variation in activity according to our prediction in a sex-dependent manner. Specifically, in females the vgll3*E allele was related to increasing activity, whereas in males the vgll3*L allele (later maturation allele) was related to increasing activity. These sex-dependent effects might be a mechanism maintaining within-population genetic life-history variation.

evolutionary biology↗

Genetic coupling of life-history and aerobic performance in juvenile Atlantic salmon

A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions (vgll3 and six6) makes Atlantic salmon (Salmo salar) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes -standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS) - and the life-history genomic regions and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Further, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile-stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve.

evolutionary biology↗

Refining the genomic location of SNP variation affecting Atlantic salmon maturation timing at a key large-effect locus

Efforts to understand the genetic underpinnings of phenotypic variation are becoming more and more frequent in molecular ecology. Such efforts often lead to the identification of candidate regions showing signals of association and/or selection. These regions may contain multiple genes and therefore validation of which genes are actually responsible for the signal is required. In Atlantic salmon (Salmo salar), a large-effect locus for maturation timing, an ecologically important trait, occurs in a genomic region including two genes, vgll3 and akap11, but data for clearly determining which of the genes (or both) contribute to the association have been lacking. Here, we take advantage of natural recombination events detected between the two candidate genes in a salmon broodstock to reduce linkage disequilibrium at the locus, and thus enabling delineation of the influence of variation at these two genes on maturation timing. By rearing 5895 males to maturation age, of which 81% had recombinant vgll3/akap11 allelic combinations, we found that vgll3 SNP variation was strongly associated with maturation timing, whereas there was little or no association between akap11 SNP variation and maturation timing. These findings provide strong evidence supporting vgll3 as the primary candidate gene in the chromosome 25 locus for influencing maturation timing. This will help guide future research for understanding the genetic processes controlling maturation timing. This also exemplifies the utility of natural recombinants to more precisely map causal variation underlying ecologically important phenotypic diversity.

genetics↗

Evolution in salmon life-history induced by direct and indirect effects of fishing

Understanding the drivers of evolution is a fundamental aim in biology. However, identifying the evolutionary impacts of human activities, both direct and indirect, is challenging because of lack of temporal data and limited knowledge of the genetic basis of most traits1. Atlantic salmon is a species exposed to intense anthropogenic pressures during its anadromous life cycle2. Previous research has shown that salmon age at maturity has evolved towards earlier maturation over the last 40 years, with an 18% decrease3 in the allele associated with late maturation at the large-effect vgll3 locus4; but the drivers of this change remain unknown. Here, we link genetic and phenotypic changes in a large Atlantic salmon population with salmon prey species biomass in the Barents Sea, temperature, and fishing effort in order to identify drivers of age at maturity evolution. We show that age at maturity evolution is associated with two different types of fisheries induced evolution acting in opposing directions: an indirect effect linked with commercial harvest of a salmon prey species (capelin) at sea (selection against late maturation), and a direct effect due to temporal changes in net fishing pressure in the river (surprisingly, selection against early maturation). Although the potential for direct and indirect evolutionary effects of fishing have been acknowledged, empirical evidence for induced changes at the genetic level has been lacking5. As capelin are primarily harvested to produce fish meal and oil for aquaculture6, we hereby identify an indirect path by which Atlantic salmon aquaculture may negatively affect wild populations.

evolutionary biology↗

Sex-specific lipid profiles in muscle of Atlantic salmon juveniles

Energy allocation in juvenile fish can have important implications for future life-history progression. Inherited and environmental factors determine when and where individuals allocate energy, and timely and sufficient energy reserves are crucial for reaching key life stages involved in the timing of maturation and sea migration. In Atlantic salmon, lipid reserves are predominantly found in the viscera and myosepta in the muscle and have been shown to play a key role in determining the timing of maturity. This life-history trait is tightly linked to fitness in many species and can be different between males and females, however, the details of relative energy allocation in juveniles of different sexes is not well understood. Therefore, the aim of this study was to investigate the effects of sex, genetics and environment during juvenile development of salmon on the amount and composition of their lipid reserves. To do so, juvenile salmon were fed one of two different lipid food contents during their first summer and autumn under common-garden conditions. Muscle lipid composition and concentrations were determined by thin layer chromatography. The muscle lipid class concentrations covaried negatively with body length and males showed higher concentrations than females for phosphatidylcholine, cholesterol, sphingomyelin, and triacylglycerol. This sex-specific difference in major lipid classes presents a new scope for understanding the regulation of lipids during juvenile development and gives direction for understanding how lipids may interact and influence major life-history traits in Atlantic salmon.

molecular biology↗

The structural variation landscape in 492 Atlantic salmon genomes

Structural variants (SVs) are a major source of genetic and phenotypic variation, but remain challenging to accurately type and are hence poorly characterized in most species. We present an approach for reliable SV discovery in non-model species using whole genome sequencing and report 15,483 high-confidence SVs in 492 Atlantic salmon (Salmo salar L.) sampled from a broad phylogeographic distribution. These SVs recover population genetic structure with high resolution, include an active DNA transposon, widely affect functional features, and overlap more duplicated genes retained from an ancestral salmonid autotetraploidization event than expected. Changes in SV allele frequency between wild and farmed fish indicate polygenic selection on behavioural traits during domestication, targeting brain-expressed synaptic networks linked to neurological disorders in humans. This study offers novel insights into the role of SVs in genome evolution and the genetic architecture of domestication traits, along with resources supporting reliable SV discovery in non-model species.

genomics↗