Periodic Reporting for period 4 - MATURATION (Age at maturity in Atlantic salmon: molecular and ecological dissection of an adaptive trait)
Reporting period: 2022-03-01 to 2022-12-31
In biology, life-history research is a field of study focused on understanding the causes and consequences of variation in reproduction and survival, i.e. fitness. As in many species, age at maturity in Atlantic salmon is tightly linked with size at maturity and thus represents a classic evolutionary trade-off: later maturing individuals spend more time at sea before returning to freshwater to spawn and have higher reproductive success due to their larger size but also have a higher risk of dying prior to first reproduction as they delay their first breeding attempt until a later age. My earlier research discovered a gene with a large effect on this key life history trait. A single gene having such a large effect on a life-history trait is unusual, and this fact, combined with the features of Atlantic salmon as a model system offer an ideal opportunity to better understand the molecular mechanisms and ecological drivers underlying a locally adapted life history trait. In MATURATION I am i) characterizing age at maturity candidate gene functions and allelic effects on phenotypes (WP1) ii) elucidating fitness effects of these phenotypes and the combined effects of genetic and environmental factors (WP3) iii) developing a mechanistic model for the sex-dependent dominance and validate intra-locus sexual conflict resolution (WP3) and assessing the evolutionary conservation of the genetic architecture (WP4). Better understanding the molecular mechanisms and ecological consequences of life-history variation also has a broad range of practical applications, from being a key tool for estimating maximum sustainable yield in commercial fisheries, to explaining why girls are reaching puberty at an increasingly early age.
Overall, we have shown that the large effect gene, vgll3, can be considered as a master regulator of life-history variation in salmon. By extensive common garden rearing of salmon with different vgll3 genotypes, we to confirmed the influence the gene has on maturation probability in both males and females. Further, we also showed that it influences a range of different features of individual salmon, including behaviour, physiology, as well as gene expression. We also showed that the effects of the gene are similar in warmer and colder conditions, and also in individuals fed feed of differing nutritional quality. We also studied population-level processes using an historical time series and showed that vgll3 allele frequency canges appear to be adaptive, and are linked to the abundance of a salmon prey species (capelin)- this abundance is driven mainly by commercial fishing of capelin. We thus identified an indirect means (capelin harvest) affecting wild Atlantic salmon life-history variation. Combined, we demonstrate how Atlantic salmon is a very useful model species for studying maturation processes.
Overall, we have shown that the large effect gene, vgll3, can be considered as a master regulator of life-history variation in salmon. By extensive common garden rearing of salmon with different vgll3 genotypes, we to confirmed the influence the gene has on maturation probability in both males and females. Further, we also showed that it influences a range of different features of individual salmon, including behaviour, physiology, as well as gene expression. We also showed that the effects of the gene are similar in warmer and colder conditions, and also in individuals fed feed of differing nutritional quality. We also studied population-level processes using an historical time series and showed that vgll3 allele frequency canges appear to be adaptive, and are linked to the abundance of a salmon prey species (capelin)- this abundance is driven mainly by commercial fishing of capelin. We thus identified an indirect means (capelin harvest) affecting wild Atlantic salmon life-history variation. Combined, we demonstrate how Atlantic salmon is a very useful model species for studying maturation processes.
WP1. Functional characterization of age at maturity candidate genes was mostly very successful. We collected a large developmental time series (samples collected routinely at different developmental time points) of tissues in fish with different vgll3 genotypes and have published a number of studies based on this material . These results show that vgll3 is a master regulator of a number of other genes in important maturation-related gene networks (Kurko et al. 2020; Verta et al. 2020, Ahi et al. 2022, 2023a,b). Further, we identified effects of vgll3 genotypes on a range of phenotypes, including behaviour (Bangura et al. 2022, Niemelä et al. 2022), metabolic rate (Prokkola et al. 2022), lipid profiles House et al. in prep) and body condition (Debes et al. 2021; House et al. 2023. We further used a traditional fine-mapping experiment for validating the roles of vgll3 in sexual maturation (Sinclair-Waters et al. 2021).
WP2. For better understanding reaction norms related to large-effect maturation genes, we conducted both temperature and food restriction treatments and found they temperature has a large effect on maturation rate, there is no interaction with the effect of vgll3 (it affects maturation in a similar manner in both temperatures tested (Åsheim et al. 2023). We have identified a strong link between the decline of the large, late maturing phenotype in a wild population, and vgll3 genotype, strongly suggesting that the population has undergone adaptive evolution for increased frequency of early maturation (Czorlich et al. 2019) and is affected by prey abundance in the Barents Sea (Czorlich et al. 2022).
WP3. Empirical studies of sexual conflict resolution in a wild population are proceeding but publication is slightly delayed due to the main post doc moving to an Associate Professor position. We have now collected over 10 cohorts of data, and have published several studies outlining the basics or reproductive fitness in the population (Mobley et al. 2019, 2020). Work Identifying interaction partners and molecular mechanisms of dominance in VGLL3 is ongoing, and on schedule with one post-doc focusing on the laboratory work currently.
WP4. Studying the evolutionary conservation of genetic architecture revealed that there is a heterogeneous genetic basis of age at maturity in salmonid fishes with a second large-effect locus (six6) but not vgll3 being linked with age at maturity is several Pacific salmon species (Waters et al. 2021)
Overall, we have shown that the large effect gene, vgll3, can be considered as a master regulator of life-history variation in salmon. By extensive common garden rearing of salmon with different vgll3 genotypes, we to confirmed the influence the gene has on maturation probability in both males and females. Further, we also showed that it influences a range of different features of individual salmon, including behaviour, physiology, as well as gene expression. We also showed that the effects of the gene are similar in warmer and colder conditions, and also in individuals fed feed of differing nutritional quality. We also studied population-level processes using an historical time series and showed that vgll3 allele frequency canges appear to be adaptive, and are linked to the abundance of a salmon prey species (capelin)- this abundance is driven mainly by commercial fishing of capelin. We thus identified an indirect means (capelin harvest) affecting wild Atlantic salmon life-history variation. Combined, we demonstrate how Atlantic salmon is a very useful model species for studying maturation processes.
WP2. For better understanding reaction norms related to large-effect maturation genes, we conducted both temperature and food restriction treatments and found they temperature has a large effect on maturation rate, there is no interaction with the effect of vgll3 (it affects maturation in a similar manner in both temperatures tested (Åsheim et al. 2023). We have identified a strong link between the decline of the large, late maturing phenotype in a wild population, and vgll3 genotype, strongly suggesting that the population has undergone adaptive evolution for increased frequency of early maturation (Czorlich et al. 2019) and is affected by prey abundance in the Barents Sea (Czorlich et al. 2022).
WP3. Empirical studies of sexual conflict resolution in a wild population are proceeding but publication is slightly delayed due to the main post doc moving to an Associate Professor position. We have now collected over 10 cohorts of data, and have published several studies outlining the basics or reproductive fitness in the population (Mobley et al. 2019, 2020). Work Identifying interaction partners and molecular mechanisms of dominance in VGLL3 is ongoing, and on schedule with one post-doc focusing on the laboratory work currently.
WP4. Studying the evolutionary conservation of genetic architecture revealed that there is a heterogeneous genetic basis of age at maturity in salmonid fishes with a second large-effect locus (six6) but not vgll3 being linked with age at maturity is several Pacific salmon species (Waters et al. 2021)
Overall, we have shown that the large effect gene, vgll3, can be considered as a master regulator of life-history variation in salmon. By extensive common garden rearing of salmon with different vgll3 genotypes, we to confirmed the influence the gene has on maturation probability in both males and females. Further, we also showed that it influences a range of different features of individual salmon, including behaviour, physiology, as well as gene expression. We also showed that the effects of the gene are similar in warmer and colder conditions, and also in individuals fed feed of differing nutritional quality. We also studied population-level processes using an historical time series and showed that vgll3 allele frequency canges appear to be adaptive, and are linked to the abundance of a salmon prey species (capelin)- this abundance is driven mainly by commercial fishing of capelin. We thus identified an indirect means (capelin harvest) affecting wild Atlantic salmon life-history variation. Combined, we demonstrate how Atlantic salmon is a very useful model species for studying maturation processes.
This research representes one of the most detailed accounts of the molecular basis of a life-history trait ever conducted in a non-model organism. By also linking this information with the ecology and evolution of the species it is of high significance in the fields of ecology and evolutionary biology. Better understanding the molecular mechanisms and ecological consequences of life-history variation also has a broad range of practical applications, from being a key tool for estimating maximum sustainable yield in commercial fisheries, to explaining why girls are reaching puberty at an increasingly early age.