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

2021 ◽  
Author(s):  
Jenni M. Prokkola ◽  
Eirik R Åsheim ◽  
Sergey Morozov ◽  
Paul Bangura ◽  
Jaakko Erkinaro ◽  
...  
Keyword(s):  
Life History ◽  
Atlantic Salmon ◽  
Metabolic Rate ◽  
Aerobic Performance ◽  
Age At Maturity ◽  
Life History Variation ◽  
Early Maturation ◽  
Genomic Regions ◽  
Late Maturation

1. The physiological underpinnings of life history adaptations in ectotherms are not well understood. Theories suggest energy metabolism influences life history variation via modulation of resource acquisition. However, the genetic basis of this relation and its dependence on ecological conditions, such as food availability, have rarely been characterized, despite being critical to predicting the responses of populations to environmental changes. 2. The Atlantic salmon (Salmo salar) is an emerging wild model species for addressing these questions; strong genetic determination of age-at-maturity at two unlinked genomic regions (vgll3 and six6) enables the use of complex experimental designs and tests of hypotheses on the physiological and genetic basis of life-history trait variation. 3. In this study, we crossed salmon to obtain individuals with all combinations of late and early maturation genotypes for vgll3 and six6 within full-sib families. Using more than 250 juveniles in common garden conditions, we tested (i) whether metabolic phenotypes (i.e., standard and maximum metabolic rates, and absolute aerobic scope) were correlated with the age-at-maturity genotypes and (ii) if high vs. low food availability modulated the relationship. 4. We found that salmon with vgll3 early maturation genotype had a higher aerobic scope and maximum metabolic rate, but not standard metabolic rate, compared to salmon with vgll3 late maturation genotype. This suggests that physiological or structural pathways regulating maximum oxygen supply or demand are potentially important for the determination of age-at-maturity in Atlantic salmon. 5. Vgll3 and six6 exhibited physiological epistasis, whereby maximum metabolic rate significantly decreased when late maturation genotypes were present concurrently in both loci compared to other genotype combinations. 6. The growth of the feed restricted group decreased substantially compared to the high food group. However, the effects of life-history genomic regions were similar in both feeding regimes, indicating a lack of genotype-by-environment interactions. 7. Our results indicate that aerobic performance of juvenile salmon may affect their age-at-maturity. The results may help to better understand the mechanistic basis of life-history variation, and the metabolic constrains on life-history evolution.

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

2018 ◽  
Author(s):  
Tutku Aykanat ◽  
Mikhail Ozerov ◽  
Juha-Pekka Vähä ◽  
Panu Orell ◽  
Eero Niemelä ◽  
...  
Keyword(s):  
Life History ◽  
Atlantic Salmon ◽  
Genetic Correlations ◽  
Age Groups ◽  
Life History Trait ◽  
Age At Maturity ◽  
Life History Variation ◽  
Functional Link ◽  
Physiological Basis ◽  
Genome Region

AbstractGenetic 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.

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

2021 ◽  
Author(s):  
Petri T Niemela ◽  
Ines Klemme ◽  
Anssi Karvonen ◽  
Pekka Hyvarinen ◽  
Paul V Debes ◽  
...  
Keyword(s):  
Life History ◽  
Atlantic Salmon ◽  
Salmo Salar ◽  
Life History Strategy ◽  
Dependent Manner ◽  
Life History Variation ◽  
Migration Activity ◽  
Early Maturation ◽  
Atlantic Salmon Salmo Salar ◽  
Activity Measurements

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.

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

2021 ◽  
Author(s):  
Yann Czorlich ◽  
Tutku Aykanat ◽  
Jaakko Erkinaro ◽  
Panu Orell ◽  
Craig R Primmer
Keyword(s):  
Atlantic Salmon ◽  
Prey Species ◽  
Barents Sea ◽  
Fishing Effort ◽  
Age At Maturity ◽  
Anthropogenic Pressures ◽  
Sea Temperature ◽  
Early Maturation ◽  
Commercial Harvest ◽  
Late Maturation

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 cycle. Previous research has shown that salmon age at maturity has evolved towards earlier maturation over the last 40 years, with an 18% decrease in the allele associated with late maturation at the large-effect vgll3 locus; 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 lacking. As capelin are primarily harvested to produce fish meal and oil for aquaculture, we hereby identify an indirect path by which Atlantic salmon aquaculture may negatively affect wild populations.

scholarly journals Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon

2019 ◽  
Author(s):  
Jukka-Pekka Verta ◽  
Paul Vincent Debes ◽  
Nikolai Piavchenko ◽  
Annukka Ruokolainen ◽  
Outi Ovaskainen ◽  
...  
Keyword(s):  
Life History ◽  
Atlantic Salmon ◽  
Life Histories ◽  
Life History Traits ◽  
Life History Strategies ◽  
Life History Trait ◽  
Gene Transcript ◽  
Genome Wide Association Studies ◽  
Age At Maturity ◽  
Life History Variation

AbstractA 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.

scholarly journals Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout

2014 ◽  
Vol 281 (1783) ◽  
pp. 20140012 ◽  
Author(s):  
Devon E. Pearse ◽  
Michael R. Miller ◽  
Alicia Abadía-Cardoso ◽  
John Carlos Garza
Keyword(s):  
Life History ◽  
Rainbow Trout ◽  
Parallel Evolution ◽  
Genomic Region ◽  
Life History Strategies ◽  
Strong Linkage Disequilibrium ◽  
Rapid Adaptation ◽  
Life History Variation ◽  
Standing Variation ◽  
Genomic Regions

Rapid adaptation to novel environments may drive changes in genomic regions through natural selection. Such changes may be population-specific or, alternatively, may involve parallel evolution of the same genomic region in multiple populations, if that region contains genes or co-adapted gene complexes affecting the selected trait(s). Both quantitative and population genetic approaches have identified associations between specific genomic regions and the anadromous (steelhead) and resident (rainbow trout) life-history strategies of Oncorhynchus mykiss . Here, we use genotype data from 95 single nucleotide polymorphisms and show that the distribution of variation in a large region of one chromosome, Omy5, is strongly associated with life-history differentiation in multiple above-barrier populations of rainbow trout and their anadromous steelhead ancestors. The associated loci are in strong linkage disequilibrium, suggesting the presence of a chromosomal inversion or other rearrangement limiting recombination. These results provide the first evidence of a common genomic basis for life-history variation in O. mykiss in a geographically diverse set of populations and extend our knowledge of the heritable basis of rapid adaptation of complex traits in novel habitats.

scholarly journals Genetic architecture of age at maturity can generate divergent and disruptive harvest-induced evolution

2017 ◽  
Vol 372 (1712) ◽  
pp. 20160035 ◽  
Author(s):  
Anna Kuparinen ◽  
Jeffrey A. Hutchings
Keyword(s):  
Life History ◽  
Atlantic Salmon ◽  
Genetic Architecture ◽  
Life History Traits ◽  
Single Locus ◽  
Sexually Dimorphic ◽  
Age At Maturity ◽  
Sexually Dimorphic Expression ◽  
Strong Control ◽  
Dimorphic Expression

Life-history traits are generally assumed to be inherited quantitatively. Fishing that targets large, old individuals is expected to decrease age at maturity. In Atlantic salmon ( Salmo salar ), it has recently been discovered that sea age at maturity is under strong control by a single locus with sexually dimorphic expression of heterozygotes, which makes it less intuitive to predict how life histories respond to selective fishing. We explore evolutionary responses to fishing in Atlantic salmon, using eco-evolutionary simulations with two alternative scenarios for the genetic architecture of age at maturity: (i) control by multiple loci with additive effects and (ii) control by one locus with sexually dimorphic expression. We show that multi-locus control leads to unidirectional evolution towards earlier maturation, whereas single-locus control causes largely divergent and disruptive evolution of age at maturity without a clear phenotypic trend but a wide range of alternative evolutionary trajectories and greater trait variability within trajectories. Our results indicate that the range of evolutionary responses to selective fishing can be wider than previously thought and that a lack of phenotypic trend need not imply that evolution has not occurred. These findings underscore the role of genetic architecture of life-history traits in understanding how human-induced selection can shape target populations. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

scholarly journals Hypoxia during incubation does not affect aerobic performance or haematology of Atlantic salmon (Salmo salar) when re-exposed in later life

2019 ◽  
Vol 7 (1) ◽  
Author(s):  
Andrew T Wood ◽  
Sarah J Andrewartha ◽  
Nicholas G Elliott ◽  
Peter B Frappell ◽  
Timothy D Clark
Keyword(s):  
Atlantic Salmon ◽  
Metabolic Rate ◽  
Salmo Salar ◽  
Later Life ◽  
Hypoxia Tolerance ◽  
Aerobic Performance ◽  
Hypoxia Exposure ◽  
Short And Long Term ◽  
Fish Performance

Abstract Hypoxia in aquatic ecosystems is becoming increasingly prevalent, potentially reducing fish performance and survival by limiting the oxygen available for aerobic activities. Hypoxia is a challenge for conserving and managing fish populations and demands a better understanding of the short- and long-term impacts of hypoxic environments on fish performance. Fish acclimate to hypoxia via a variety of short- and long-term physiological modifications in an attempt to maintain aerobic performance. In particular, hypoxia exposure during early development may result in enduring cardio-respiratory modifications that affect future hypoxia acclimation capacity, yet this possibility remains poorly investigated. We incubated Atlantic salmon (Salmo salar) in normoxia (~100% dissolved oxygen [DO, as percent air saturation]), moderate hypoxia (~63% DO) or cyclical hypoxia (100–25% DO daily) from fertilization until 113 days post-fertilization prior to rearing all groups in normoxia for a further 8 months. At ~11 months of age, subsets of each group were acclimated to hypoxia (50% DO) for up to 44 days prior to haematology, aerobic metabolic rate and hypoxia tolerance measurements. Hypoxia exposure during incubation (fertilization to 113 days post-fertilization) did not affect the haematology, aerobic performance or hypoxia tolerance of juvenile salmon in later life. Juveniles acclimated to hypoxia increased maximum aerobic metabolic rate and aerobic scope by ~23 and ~52%, respectively, when measured at 50% DO but not at 100% DO. Hypoxia-incubated juveniles also increased haematocrit and haemoglobin concentration but did not affect acute hypoxia tolerance (critical oxygen level and DO at LOE). Thus, while Atlantic salmon possess a considerable capacity to physiologically acclimate to hypoxia by improving aerobic performance in low oxygen conditions, we found no evidence that this capacity is influenced by early-life hypoxia exposure.

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