Environment-driven reprogramming of gamete DNA methylation occurs during maturation and is transmitted intergenerationally in salmon

Wellband, Kyle; Roth, David; Linnansaari, Tommi; Curry, R. Allen; Bernatchez, Louis

doi:10.1101/2020.11.25.396069

Cited by 7 publications

(8 citation statements)

References 96 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Among the most important applications of RNA-Seq currently used is testing for rapid adaptation to environmental change (e.g., to captivity or climate warming), and to determine if environmentally-induced gene expression shifts are transgenerationally transmitted (e.g., Christie et al 2016, Charlesworth et al 2017, Skvortsova et al 2018, Navarro-Martin et al 2020, Savilammi et al 2020. Our results will facilitate future research testing for transgenerational transmission of potentially epigenetic hatchery-adaptive traits in wild fish populations (e.g., Christie et al 2016, Le Luyer et al 2017, Wellband et al 2020.…”

Section: Discussionmentioning

confidence: 85%

Gene expression estimates: Influence of sequencing library construction, fish sampling methods, and tissue harvesting time

Moreno¹,

Howard²,

Relyea³

et al. 2021

Preprint

View full text Add to dashboard Cite

RNA sequencing (RNA-Seq) is becoming a popular method for measuring gene expression in non-model organisms, including wild populations sampled in the field. While RNA-Seq can be used to measure gene expression variation among wild-caught individuals and can yield important biological insights into organismal function, technical variables may also influence gene expression estimates. We examined the influence of multiple technical variables on estimated gene expression in a non-model fish species, the westslope cutthroat trout (Oncorhynchus clarkii lewisi), using two RNA-Seq methods: 3’ RNA-Seq and whole mRNA-Seq. We evaluated the effects of dip netting versus electrofishing, and of harvesting tissue immediately versus 5 minutes after euthanasia on estimated gene expression in blood, gill, muscle, and liver. We found higher RNA degradation in the liver compared to the other tissues. There were fewer expressed genes in blood compared to gill and muscle. We found no difference in gene expression among sampling methods or due to a delay in tissue collection. However, we detected fewer genes with 3’ RNA-Seq than with whole mRNA-Seq and found statistically significant differences in gene expression between 3’ RNA-Seq and whole mRNA-Seq. The magnitude and direction of these differences does not appear to be dependent on gene type or length. Our findings indicate that RNA-Seq is robust to the technical variables related to the field sampling techniques tested here but varies based on the tissue sampled and the RNA-Seq library used. This study advances understanding of usefulness of RNA-Seq to study gene expression variation in evolution, ecology, and conservation.

show abstract

Section: Discussionmentioning

confidence: 85%

Gene expression estimates: Influence of sequencing library construction, fish sampling methods, and tissue harvesting time

Moreno¹,

Howard²,

Relyea³

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…Early environment is a deterministic factor that acts on later performance in fish (Jonsson, & Jonsson, 2009). Accordingly, mounting evidence points toward an epigenetic basis associated with the effect of hatchery environment on epigenetic reprogramming of the progeny produced in captivity (Christie et al, 2016; Gavery et al, 2018; Le Luyer et al, 2017; Leitwein et al, 2021; Wellband et al, 2021). Of particular interest is the study of Rodriguez‐Barreto et al (2019), which showed that early‐life hatchery exposure changed the pattern of methylation of Atlantic salmon males and that corticotropin‐releasing factor receptor 1‐like was one of the differentially methylated regions in hatchery fish.…”

Section: Discussionmentioning

confidence: 99%

Section: Reduced Fitness Of Captive-bred Atlantic Salmon Stocked At T...mentioning

confidence: 99%

Effects of stocking at the parr stage on the reproductive fitness and genetic diversity of a wild population of Atlantic salmon (Salmo salar L.)

Bouchard

Wellband

Lecomte

et al. 2022

Evolutionary Applications

Self Cite

View full text Add to dashboard Cite

Captive‐breeding programs are among the most adopted conservation practices to mitigate the loss of biodiversity, including genetic diversity. However, both genetic and nongenetic changes occurring in captivity can reduce the fitness of supplemented individuals, which complicate rehabilitation efforts. In the case of Atlantic salmon, the intensity of changes that occur in captivity and their impact on fitness will vary with the stocking practice adopted. In this study, we test whether salmon stocked at the parr stage have reduced reproductive success compared with their wild conspecifics and whether they contribute to increase genetic diversity in the targeted population. To do so, we use high‐throughput microsatellite sequencing of 38 loci to accurately assign 2381 offspring to a comprehensive set of possible parents from a supplemented Atlantic salmon population in Québec, Canada. Captive‐bred salmon stocked at the parr stage had fewer mates than their wild conspecifics, as well as a reduced relative reproductive success (RSS) compared with their wild counterparts. Nonetheless, in comparison with previous studies, stocking at the parr stage significantly improved RSS compared with salmon stocked as smolts and they displayed a reduction in reproductive success similar to salmon stocked as fry, which spend less time in captivity than parr. Moreover, supplementation of captive‐bred salmon significantly contributed to increasing genetic diversity. These results should contribute to informing resource managers in determining the best stocking practice to enhance Atlantic salmon populations.

show abstract

“…Early environment is a deterministic factor that acts on later performance in fish (Jonsson & Jonsson, 2014). Although differences in fitness between hatchery-reared and wild salmon were previously thought to be genetically based only, mounting evidence also points toward an epigenetic basis associated with the effect of hatchery environment on epigenetic reprogramming of the progeny produced in captivity (Christie et al 2016; Le Luyer et al 2017; Gavery et al 2018; Wellband et al 2021; Leitwein et al 2021). Of particular interest is the study of Rodriguez Barreto et al (2019) which showed that early-life hatchery exposure changed the pattern of methylation of Atlantic salmon males and that corticotropin-releasing factor receptor 1-like was one of the differentially methylated regions in hatchery fish.…”

Section: Discussionmentioning

confidence: 99%

Captive-breeding and catch-and-release’s effects on the reproductive success of Atlantic salmon (Salmo salarL.)

Bouchard¹,

Wellband²,

Lecomte³

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Captive-breeding programs as well as and catch-and-release are among the most commonly adopted conservation practices in recreational fisheries. However, risks and benefits associated with their implementation are rarely evaluated. In the case of Atlantic Salmon, while previous studies revealed that captive-bred fish show reduced fitness compared to their wild counterparts in nature. Yet, few examined the extent and causes of their reduced reproductive success or directly compared their contribution to enhance genetic diversity to that of wild fish, including mature male parr. Furthermore, only one study specifically measured the reproductive success of caught and released Atlantic salmon in natural settings, and no study to date evaluated if released salmon are able to reproduce when released at temperature above 20°C which is known to increase post-release mortality. Here, we use high-throughput microsatellite sequencing of 38 loci to accurately assign 2500 offspring to a comprehensive set of possible parents from a supplemented Atlantic salmon population in Quebec, Canada. The resolved molecular pedigree provided informative insight on the reproductive pattern of both captive-bred salmon and caught-and-released salmon. Captive-bred salmon had fewer partners than their wild conspecifics which lead to a significant reduction of reproductive success relative to that of their wild counterparts. Supplementation of captive-bred salmon significantly contributed to increase genetic diversity but mature male parr did so to an even greater extent and significantly inflated the number of alleles found among offspring. Moreover, our results showed that that at least 83% of caught-and-released salmon did successfully reproduced although caught-and-released female salmon have a significantly reduced reproductive success, averaging 73% of the reproductive output of non-caught salmon. Reproductive success of released salmon was not influenced by water temperature over 20°C which suggests either that the studied population is locally adapted to warm waters or that they behaviorally regulated body temperature by accessing nearby thermal refugia. Our results should help refining managers' ability to analyze the risks and benefits associated with captive-breeding and catch-and-release, and thus, optimize conservation practices used for the preservation of Atlantic salmon populations.

show abstract

Environment-driven reprogramming of gamete DNA methylation occurs during maturation and is transmitted intergenerationally in salmon

Cited by 7 publications

References 96 publications

Gene expression estimates: Influence of sequencing library construction, fish sampling methods, and tissue harvesting time

Gene expression estimates: Influence of sequencing library construction, fish sampling methods, and tissue harvesting time

Effects of stocking at the parr stage on the reproductive fitness and genetic diversity of a wild population of Atlantic salmon (Salmo salar L.)

Captive-breeding and catch-and-release’s effects on the reproductive success of Atlantic salmon (Salmo salarL.)

Contact Info

Product

Resources

About