Biology subjects

Erkinaro, J.

Publications and source records attributed to Erkinaro, J..

27 records · Page 2Linked to original sources

bioRxiv2019

Large single-locus effects for maturation timing are mediated via condition variation in Atlantic salmon

Maturation timing is a pivotal life-history trait balancing probabilities between mortality and reproduction. Environmental vs. genetic contributions to traits associated with maturation initiation, such as growth and body condition, remain uncertain because of difficulties in determining causality. In Atlantic salmon, maturation timing associates with a large-effect locus around vgll3, but how this locus affects maturation remains unknown. We combined controlled breeding with common-garden experimentation at two temperatures and show that vgll3 effects on maturation of males express primarily via body condition, which we demonstrate in the males non-maturing female relatives, thus avoiding reverse causality. Between homozygous vgll3 genotypes, maturation probability differed several folds and female condition differed 2% in both temperature environments. Vgll3 effects explained 25 and 16% of maturation probability heritability and 15 and 6% of female condition heritability, in the warm and cold environment, respectively. Non-significant vgll3 effects on female length were antagonistic to those on condition but of equal proportional size. When controlling for vgll3 effects, genetic correlations changed antagonistically between both maturation and condition vs. growth, suggesting vgll3 as a resource-allocation locus. The results support large vgll3 maturation effects being mediated via environmentally stable body condition effects, enabling rapid co-evolution between the life-history traits.

evolutionary biology↗

bioRxiv2019

Transcription profiles of age-at-maturity-associated genes suggest cell fate commitment regulation as a key factor in the Atlantic salmon maturation process

Despite recent taxonomic diversification in studies linking genotype with phenotype, follow-up studies aimed at understanding the molecular processes of such genotype-phenotype associations remain rare. The age at which an individual reaches sexual maturity is an important fitness trait in many wild species. However, the molecular mechanisms regulating maturation timing processes remain obscure. A recent genome-wide association study in Atlantic salmon (Salmo salar) identified large-effect age-at-maturity-associated chromosomal regions including genes vgll3, akap11 and six6, which have roles in adipogenesis, spermatogenesis and the hypothalamic-pituitary-gonadal (HPG) axis, respectively. Here, we determine expression patterns of these genes during salmon development and their potential molecular partners and pathways. Using Nanostring transcription profiling technology, we show development- and tissue-specific mRNA expression patterns for vgll3, akap11 and six6. Correlated expression levels of vgll3 and akap11, which have adjacent chromosomal location, suggests they may have shared regulation. Further, vgll3 correlating with arhgap6 and yap1, and akap11 with lats1 and yap1 suggests that Vgll3 and Akap11 take part in actin cytoskeleton regulation. Tissue-specific expression results indicate that vgll3 and akap11 paralogs have sex-dependent expression patterns in gonads. Moreover, six6 correlating with slc38a6 and rtn1, and Hippo signaling genes suggests that Six6 could have a broader role in the HPG neuroendrocrine and cell fate commitment regulation, respectively. We conclude that Vgll3, Akap11 and Six6 may influence Atlantic salmon maturation timing via affecting on adipogenesis and gametogenesis by regulating cell fate commitment and the HPG axis. These results may help to unravel general molecular mechanisms behind maturation.

genetics↗

bioRxiv2019

Regulatory divergence in vgll3 underlies variation in age at maturity in male Atlantic salmon

A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report a cis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factor vestigial-like 3 (vgll3) associate with variation in a key life history trait, age at maturity, in Atlantic salmon (Salmo salar). Using a common-garden experiment, we first show that vgll3 genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling of vgll3 expression in ten tissues across the first year of salmon development, we identify a pubertal transition in vgll3 expression where maturation coincided with a 66% reduction in testicular vgll3 expression. The late maturation allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform of vgll3 pre-puberty. By comparing absolute vgll3 mRNA copies in heterozygotes we show that the expression difference between the early and late maturity alleles is largely cis-regulatory. We propose a model whereby expression of a rare isoform from the late allele shifts the liability of its carriers towards delaying puberty. These results reveal how regulatory differences can be a central mechanism for the evolution of life history traits. Author summaryAlternative life history strategies are an important source of diversity within populations and promote the maintenance of adaptive capacity and population resilience. However, in many cases the molecular basis of different life history strategies remains elusive. Age at maturity is a key adaptive life history trait in Atlantic salmon and has a relatively simple genetic basis. Using salmon age at maturity as a model, we report a mechanism whereby different transcript isoforms of the key age at maturity gene, vestigial-like 3 (vgll3), associate with variation in the timing of male puberty. Our results show how gene regulatory differences in conjunction with variation in gene transcript structure can encode for complex alternative life histories.

evolutionary biology↗

bioRxiv2019

Time spent in distinct life-history stages has sex-specific effects on reproductive fitness in wild Atlantic salmon

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a four-year pedigree to investigate if time spent in two distinct life history stages has sex-specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW), and years spent in the marine environment prior to sexual maturation (sea age, SW) on 264 spawning adults. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5000 offspring). Sea age is positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: increase of 16.5 offspring/SW and 0.86 mates/SW; males: increase of 12.4 offspring/SW and 0.43 mates/SW). Younger freshwater age was related to older sea age and thus increased reproductive fitness, but only among females (females: -9.0 offspring/FW and -0.80 mates/FW). This implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and males returned to spawn earlier than females despite the fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex-specific consequence on female reproductive fitness, demonstrating a life-history trade-off between maturation and reproduction in wild Atlantic salmon.

evolutionary biology↗

bioRxiv2018

Genetic correlation between sea age at maturity and iteroparity in Atlantic salmon.

Genetic correlations in life history traits may result in unpredictable evolutionary trajectories if not accounted for in life-history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and among populations. In the Teno River in northern Europe, iteroparous individuals constitute an important component of many populations and have experienced a sharp increase in abundance in the last 20 years, partly overlapping with a general decrease in age structure. The physiological basis of iteroparity bears similarities to that of age at first maturity, another life history trait with substantial fitness effects in salmon. Sea age at maturity in Atlantic salmon is controlled by a major locus around the vgll3 gene, and we used this opportunity demonstrate that the two traits are genetically correlated around this genome region. The odds ratio of survival until second reproduction was up to 2.4 (1.8-3.5 90% CI) times higher for fish with the early-maturing vgll3 genotype (EE) compared to fish with the late-maturing genotype (LL). The association had a dominance architecture, although the dominant allele was reversed in the late-maturing group compared to younger groups that stayed only one year at sea before maturation. Post hoc analysis indicated that iteroparous fish with the EE genotype had accelerated growth prior to first reproduction compared to first-time spawners, across all age groups, while this effect was not detected in fish with the LL genotype. These results broaden the functional link around the vgll3 genome region and help us understand constraints in the evolution of life history variation in salmon. Our results further highlight the need to account for genetic correlations between fitness traits when predicting demographic changes in changing environments.

evolutionary biology↗

bioRxiv2018

Bayesian arrival model for Atlantic salmon smolt counts powered by environmental covariates and expert knowledge

Annual run size and timing of Atlantic salmon smolt migration was estimated using Bayesian model framework and data from six years of a video monitoring survey. The model has a modular structure. It separates sub-processes of departing, traveling and observing, of which the first two together define the arrival distribution. The sub-processes utilize biological background and expert knowledge about the migratory behavior of smolts and about the probability to observe them from the video footage under varying environmental conditions. Daily mean temperature and discharge were used as environmental covariates. The model framework does not require assuming a simple distributional shape for the arrival dynamics and thus also allows for multimodal arrival distributions. Results indicate that 25 % - 75% of smolts pass the Utsjoki monitoring site unobserved. Predictive studies were made to estimate daily run size in cases with missing counts either at the beginning or in the middle of the run, indicating good predictive performance.

ecology↗

bioRxiv2018

Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon

Understanding the mechanisms by which populations adapt to their environments is a fundamental aim in biology. However, it remains challenging to identify the genetic basis of traits, provide evidence of genetic changes and quantify phenotypic responses. Age at maturity in Atlantic salmon represents an ideal trait to study contemporary adaptive evolution as it has been associated with a single locus in the vgll3 region, and has also strongly changed in recent decades. Here, we provide an empirical example of contemporary adaptive evolution of a large effect locus driving contrasting sex-specific evolutionary responses at the phenotypic level. We identified an 18% decrease in the vgll3 allele associated with late maturity (L) in a large and diverse salmon population over 36 years, induced by sex-specific selection during the sea migration. Those genetic changes resulted in a significant evolutionary response in males only, due to sex-specific dominance patterns and vgll3 allelic effects. The vgll3 allelic and dominance effects differed greatly in a second population and were likely to generate different selection and evolutionary patterns. Our study highlights the importance of knowledge of genetic architecture to better understand fitness trait evolution and phenotypic diversity. It also emphasizes the potential role of adaptive evolution in the trend toward earlier maturation observed in numerous Atlantic salmon populations worldwide.

evolutionary biology↗

bioRxiv2018

Home ground advantage: selection against dispersers promotes cryptic local adaptation in wild salmon

A long-held, but poorly tested, assumption in natural populations is that individuals that disperse into new areas for reproduction are at a disadvantage compared to individuals that reproduce in their natal habitat, underpinning the eco-evolutionary processes of local adaptation and ecological speciation. Here, we capitalize on fine-scale population structure and natural dispersal events to compare the reproductive success of local and dispersing individuals captured on the same spawning ground in four consecutive parent-offspring cohorts of wild Atlantic salmon (Salmo salar). Parentage analysis conducted on adults and juvenile fish showed that local females and males had 9.6 and 2.9 times higher reproductive success than dispersers, respectively. Our results reveal how dispersal disadvantage in reproductive success may act in natural populations to drive population divergence and local adaptation over microgeographic spatial scales without clear morphological differences or physical barriers to gene flow.

evolutionary biology↗

bioRxiv2018

Genomic signatures of fine-scale local adaptation in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis, behaviour, and immune defence-related genes.

Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study we used a dense SNP array to identify candidate loci underlying fine-scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene-environment association, and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci be adaptively important in Atlantic salmon at sub-drainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis, behaviour, and immune defence. These included the large-effect age-at-matunty gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations, and that is also a candidate for local selection over the global range of Atlantic salmon. This region co-localized with a genomic region strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to river flow volume and co-vanes with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research.

evolutionary biology↗