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Biology

Pet trout: domestication rapidly alters gene expression

Christie, M.R., Marine, M.L., Fox, S.E., French, R.A., and Blouin, M.S. (2016). A single generation of domestication heritably alters the expression of hundreds of genes. Nature Communications. 7:10676. DOI: 10.1038/ncomms10676. Free open access article available here.

Domestication

As early as the Upper Paleolithic era (10,000 to 50,000 years ago), the dog emerged as the first domesticated animal, the product of generations of careful breeding and animal husbandry. Domesticated animals often bear little resemblance to their wild cousins, with extensive changes in behaviour, morphology, and physiology, to make them more suitable for life among humans. While typically seen as a long process, growing evidence suggests that genetic adaptation to captivity can occur rapidly, shedding new light on a very old process.

This study used steelhead trout, a marine population of rainbow trout, as the model organism. Rainbow trout (Oncorhynchus mykiss) are one of the few fish species considered to be fully domesticated (Teletchea & Fontaine, 2012), and have been introduced to every continent except Antarctica. Considered a “lab rat” of the fish research world, we know a lot about their genetics, physiology, life history, and ecology. Christie and colleagues exploited this knowledge to test whether the earliest stages of domestication could be detected in the offspring of first-generation hatchery-reared fish – animals spawned from wild stock, but raised in captivity for a year before release into the wild.

First-generation hatchery-reared fish have been released since 1992 to boost the threatened Hood River, OR steelhead population. Photo modified from Oregon State University @ Flickr.

First-generation hatchery-reared fish have been released since 1992 to boost the threatened Hood River, OR steelhead population. Photo modified from Oregon State University @ Flickr.

Wild and hatchery-reared crosses

Wild (W) and first-generation hatchery (H) fish were crossed to produce purebred (WxW or HxH) and hybrid (WxH or HxW) offspring. Numbers represent the total number of individuals, and families (in brackets) used in the study. Adapted from Christie et al., 2016.

Wild (W) and first-generation hatchery (H) fish were crossed to produce purebred (WxW or HxH) and hybrid (WxH or HxW) offspring. Numbers represent the total number of individuals, and families (in brackets) used in the study. Adapted from Christie et al., 2016.

The authors bred wild stock and first-generation hatchery-reared steelhead trout caught during their migration to spawning grounds in the Hood River, Oregon. First generation trout are released as juveniles after a year in the hatchery, and typically do not return upriver to spawn until they are four years old. The release of these first-generation fish has been ongoing since 1992 in an effort to boost the threatened Hood River steelhead population.

The purebred (wild males crossed with wild females, and hatchery males crossed with hatchery females) and hybrid (wild fish bred with hatchery fish) larvae were reared in identical conditions to minimize the impact of any parental effects (which we’ve discussed on Oceanbites earlier this year). Once they reached the free-swimming stage, the fry were prepared for RNA-sequencing (RNA-seq), an analytical technique that allows scientists to measure gene expression.

Gene expression & RNA-seq

The central dogma of molecular biology. DNA is used to produce RNA, which contains the same information as the copied stretch of DNA (the gene), but is able to be moved throughout the cell. RNA is then provides instructions to special cellular machinery to produce proteins. Photo adapted from Wikimedia Commons.

The central dogma of molecular biology. DNA is used to produce RNA, which contains the same information as the copied stretch of DNA (the gene), but is able to be moved throughout the cell. RNA is then provides instructions to special cellular machinery to produce proteins. Photo adapted from Wikimedia Commons.

Gene expression is a process by which special cellular machinery reads information contained within an organism’s DNA and produces a gene product (usually a protein). Proteins are responsible for just about everything that happens in a cell, so knowing which genes are being activated or deactivated can give us a good sense of what is going on inside a cell.

In order for a gene to be expressed, the DNA has to be copied into RNA (ribonucleic acid). RNA, unlike DNA, can be transported outside the nucleus and into other areas of the cell, where it is used to provide instructions about which amino acids should be assembled into a a polypeptide chain. Producing these long strings of amino acids is the first step of assembling a functional protein).

RNA-seq is a new technology that allows researchers to measure the amount of RNA in a biological sample at a specific moment in time. The power of RNA-seq is that it allows researchers to look at all the RNA in a cell (instead of being limited to a few specific genes), giving a complete picture of gene expression inside a cell. By knowing the RNA in a cell, researchers can infer which genes are sending signals to other parts of the cell.

Adapting to crowded conditions 

When the team completed RNA-seq analysis of the offspring of wild fish and first-generation hatchery fish, they found some 723 genes that were differentially expressed. Remarkably, this means the effects of a single year of early life in a hatchery produced heritable changes in their offsprings’ gene expression. These differentially expressed genes may represent the early genetic underpinnings of the long process of domestication.

Summary table of major categories of genes found to be expressed differently between wild and hatchery fish. Gene functions are coloured coded into wound healing, immune response, and metabolism. PFDR is the likelihood that the result is a false positive (that the gene is actually not differently expressed between the two populations). A PFDR below 0.05 (5%, or “5 e -2,” for “5 to the exponent of -2” in the notation of the table) is considered a statistically significant result. Gene count (%) gives the percent of all 723 differentially expressed genes that fall into that category. Table adapted from Christie et al., 2016.

Summary table of major categories of genes found to be expressed differently between wild and hatchery fish. Gene functions are coloured coded into wound healing, immune response, and metabolism. PFDR is the likelihood that the result is a false positive (that the gene is actually not differently expressed between the two populations). A PFDR below 0.05 (5%, or “5 e -2,” for “5 to the exponent of -2” in the notation of the table) is considered a statistically significant result. Gene count (%) gives the percent of all 723 differentially expressed genes that fall into that category. Table adapted from Christie et al., 2016.

Interestingly, a large proportion of these genes fell into one or more of three major functional categories: wound healing, immune response, and metabolism. Modification of these processes may be advantageous in crowded conditions, when the risk of injury or infection may be increased, or when fish have to grow fast to complete for limited resources. This suggest that the earliest stage of domestication may involve some adaptation to the high stocking densities characteristic of many fish farms and hatcheries.

Fish farms often hold fish in high density to maximize production. [PublicDomainPictures]

Fish farms often hold fish in high density to maximize production. [PublicDomainPictures]

Being able to detect the effect of domesticated parents in offspring raises questions about the effectiveness of using hatchery programs to prop up threatened species, and by extension the role of captive breeding and reintroduction programs in conservation programs (click for a description of the ongoing efforts of the Toronto Zoo). How long do these domestication effects remain in the population? Are animals born in zoos able to compete with wild stock? As habitat loss, climate change, and human activity continue to threaten species around the world, such questions will be at the forefront of new ecological protection efforts.

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