scholarly journals Heterogeneous genetic basis of age at maturity in salmonid fishes

Author(s):  
Charles D. Waters ◽  
Anthony Clemento ◽  
Tutku Aykanat ◽  
John Carlos Garza ◽  
Kerry A. Naish ◽  
...  

AbstractUnderstanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications to conservation and management. However, the extent to which interspecific life-history trait polymorphisms share evolutionary pathways remains under-explored. We address this gap by studying the genetic basis of a key life-history trait, age at maturity, in four species of Pacific salmon (genus Oncorhynchus) that exhibit intra- and interspecific variation in this trait – Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome-wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46×10−9 after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life-history trait, as well as the implications of our findings for conservation and management.

2018 ◽  
Author(s):  
Tutku Aykanat ◽  
Mikhail Ozerov ◽  
Juha-Pekka Vähä ◽  
Panu Orell ◽  
Eero Niemelä ◽  
...  

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.


2019 ◽  
Author(s):  
Jukka-Pekka Verta ◽  
Paul Vincent Debes ◽  
Nikolai Piavchenko ◽  
Annukka Ruokolainen ◽  
Outi Ovaskainen ◽  
...  

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.


2021 ◽  
Author(s):  
Jenni M. Prokkola ◽  
Eirik R Åsheim ◽  
Sergey Morozov ◽  
Paul Bangura ◽  
Jaakko Erkinaro ◽  
...  

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.


2017 ◽  
Vol 372 (1712) ◽  
pp. 20160035 ◽  
Author(s):  
Anna Kuparinen ◽  
Jeffrey A. Hutchings

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’.


2015 ◽  
Vol 282 (1806) ◽  
pp. 20150156 ◽  
Author(s):  
Arild Husby ◽  
Takeshi Kawakami ◽  
Lars Rönnegård ◽  
Linnéa Smeds ◽  
Hans Ellegren ◽  
...  

Understanding the genetic basis of traits involved in adaptation is a major challenge in evolutionary biology but remains poorly understood. Here, we use genome-wide association mapping using a custom 50 k single nucleotide polymorphism (SNP) array in a natural population of collared flycatchers to examine the genetic basis of clutch size, an important life-history trait in many animal species. We found evidence for an association on chromosome 18 where one SNP significant at the genome-wide level explained 3.9% of the phenotypic variance. We also detected two suggestive quantitative trait loci (QTLs) on chromosomes 9 and 26. Fitness differences among genotypes were generally weak and not significant, although there was some indication of a sex-by-genotype interaction for lifetime reproductive success at the suggestive QTL on chromosome 26. This implies that sexual antagonism may play a role in maintaining genetic variation at this QTL. Our findings provide candidate regions for a classic avian life-history trait that will be useful for future studies examining the molecular and cellular function of, as well as evolutionary mechanisms operating at, these loci.


2021 ◽  
Author(s):  
Ana Villaplana Velasco ◽  
Justin Engelmann ◽  
Konrad Rawlik ◽  
Oriol Canela-Xandri ◽  
Claire Tochel ◽  
...  

There is increasing evidence that the complexity of the retinal vasculature (measured as fractal dimension, Df) might offer earlier insights into the progression of coronary artery disease (CAD) before traditional biomarkers can be detected. This association could be partly explained by a common genetic basis; however, the genetic component of Df is poorly understood. We present here a genome-wide association study (GWAS) aimed to elucidate the genetic component of Df and to analyse its relationship with CAD. To this end, we obtained Df from retinal fundus images and genotyping information from ~38,000 white-British participants in the UK Biobank. We discovered 9 loci associated with Df, previously reported in pigmentation, retinal width and tortuosity, hypertension, and CAD studies. Significant negative genetic correlation estimates endorse the inverse relationship between Df and CAD, and between Df and myocardial infarction (MI), one of CAD fatal outcomes. This strong association motivated us to developing a MI predictive model combining clinical information, Df, a CAD polygenic risk score and using a random forest algorithm. Internal cross validation evidenced a considerable improvement in the area under the curve (AUC) of our predictive model (AUC=0.770) when comparing with an established risk model, SCORE, (AUC=0.719). Our findings shed new light on the genetic basis of Df, unveiling a common control with CAD, and highlights the benefits of its application in individualised MI risk prediction.


2020 ◽  
Author(s):  
Jamilla Akhund-Zade ◽  
Shraddha Lall ◽  
Erika Gajda ◽  
Denise Yoon ◽  
Benjamin de Bivort

AbstractDrosophila melanogaster egg production, a proxy for fecundity, is an extensively studied life-history trait with a strong genetic basis. As eggs develop into larvae and adults, space and resource constraints can put pressure on the developing offspring, leading to a decrease in viability, body size, and lifespan. Our goal was to map the genetic basis of offspring number and weight under the restriction of a standard laboratory vial. We screened 143 lines from the Drosophila Genetic Reference Panel for offspring numbers and weights to create an ‘offspring index’ that captured the number vs. weight trade-off. We found 30 associated variants in 18 genes. Validation of hid, Sox21b, CG8312, and mub candidate genes using gene disruption mutants demonstrated a role in adult stage viability, while mutations in Ih and Rbp increased offspring number and increased weight, respectively. The polygenic basis of offspring number and weight, with many variants of small effect, as well as the involvement of genes with varied functional roles, support the notion of Fisher’s “infinitesimal model” for this life-history trait.


Author(s):  
Jamilla Akhund-Zade ◽  
Shraddha Lall ◽  
Erika Gajda ◽  
Denise Yoon ◽  
Julien F Ayroles ◽  
...  

Abstract Drosophila melanogaster egg production, a proxy for fecundity, is an extensively studied life-history trait with a strong genetic basis. As eggs develop into larvae and adults, space and resource constraints can put pressure on the developing offspring, leading to a decrease in viability, body size, and lifespan. Our goal was to map the genetic basis of offspring number and weight under the restriction of a standard laboratory vial. We screened 143 lines from the Drosophila Genetic Reference Panel for offspring numbers and weights to create an ‘offspring index’ that captured the number vs. weight trade-off. We found 18 genes containing 30 variants associated with variation in the offspring index. Validation of hid, Sox21b, CG8312, and mub candidate genes using gene disruption mutants demonstrated a role in adult stage viability, while mutations in Ih and Rbp increased offspring number and increased weight, respectively. The polygenic basis of offspring number and weight, with many variants of small effect, as well as the involvement of genes with varied functional roles, support the notion of Fisher’s “infinitesimal model” for this life-history trait.


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