Differential fertilisation compatibility in Atlantic salmon: implications for farmed salmon gene introgression and hybridisation

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

One of the most important barriers to reproduction between different species is compatibility between sperm and egg. Biologists are trying to understand the evolution of recognition and compatibility between gametes, but for most species nothing is known about how sperm and egg co-evolve to recognise one-another for fertilization. Recent research shows that this process probably evolves very quickly, probably because of sperm competition between males to fertilise the eggs, and conflict between males and females to get the most out of reproduction. We will examine the compatibility between sperm and egg in Atlantic salmon, which is an ideal model to examine these questions for both pure and applied reasons. Salmon adults return to the river where they hatched to reproduce. This strategy means that genetic mixing between different populations is low, and biologists have shown that different strains have clear genetic differences, and have evolved specific adaptations for their own population (such as size, spawning age etc). These isolating conditions make salmon a likely species to have evolved differences between populations in sperm and egg compatibility, because of those rapid evolutionary processes just mentioned. We have found evidence for differences in fertilization compatibility between salmon strains, based on quite specific, but important immunity genes. In this project we plan to examine these differences in much more breadth by looking at how sperm and egg fertilization compatibility has changed between different populations, while also applying these theories to a key problem facing wild Atlantic salmon. Wild Atlantic salmon are an important fish for many reasons, but are unfortunately in severe decline. A major problem facing wild salmon stocks is the escape of farmed salmon, which occurs over the salmon's range at a very high level. Escaped fish can survive, and some make it onto wild salmon spawning grounds. Here they attempt to spawn with wild fish, presenting a major problem: farmed salmon have been domestically-selected for big genetic differences with wild fish. Offspring from farmed and wild salmon reproduction carry inferior farmed genes, and mean that important wild genes in different populations become diluted. Continual release of so many farmed fish could eventually genetically swamp wild genes, possibly permanently losing specifically evolved local adaptations forever. One could imagine a similar situation if domestic dogs were continually released into wolf populations to breed; eventually the pure, wild wolf genes would be lost if release occurred every year at high enough rates. A vital piece of information in understanding the level of the farmed salmon problem is how fertile are crosses between farmed and wild salmon? Domestication might have altered farmed salmon fertility, either up or down. Research has shown that farmed fish can successfully reproduce with wild fish, but that they are inferior at reproduction. However, exactly HOW inferior are farmed fish, and how does this inferiority vary when reproducing with different wild populations? This information is important to understand the risk of farmed fish to wild stocks. We will answer this question by measuring the fertility of farmed sperm and eggs with wild salmon sperm and eggs. We have developed trials that run fertilisations in controlled conditions, but which mimic the normal function of sperm and egg in a salmon river. We will also examine fertilisation success when wild and farmed sperm mix and compete for a batch of eggs, a process which occurs normally in the wild. We will also measure how fertile farmed salmon are with a close relative, trout, since this is another possible way for farmed hybrids to be produced. Our research will allow us to measure the relative fertility of farmed salmon, thus providing very useful information for governments balancing wild fish conservation with commercially important salmon farming.
 
Description Serious threats to wild salmon populations arise from hybridisation with escaped farmed salmon which causes genetic disruption, erosion and dilution of important locally-adapted wild traits. or trout. To establish the relative fertilization compatibility between these strains and species, and to allow us to understand basic processes controlling fertilization dynamics, we performed assays of sperm, fertility, competitiveness, and offspring fitness from crosses between these strains and species.

RESULTS SUMMARIES
1. Farmed salmon show equivalent sperm function, fertility, and sperm competitiveness compared with their wild ancestor. These results reveal no barrier to reproduction between farmed and wild salmon at the gamete level.

2. Salmon and trout are fully interfertile, but when sperm competition is invoked, conspecific sperm precedence is established with about 75% of the eggs fertilized by the homospecific male's sperm. This conspecific sperm precedence is completely controlled by the female's ovarian fluid, a protein-rich solution that is released with the eggs. The species identity of the egg plays no role in allowing a conspecific male to win precedence.

3. Conspecific sperm precedence is reduced when populations exist in sympatry with the hybridising species, compared with allopatry, suggesting that there is reinforcement of mechanisms that allow the egg to resist hybrid fertilizations when the risks of that are greater (i.e. in sympatry).

4. A range of reproductive and life-history assays in hatchery and semi-natural stream conditions reveal that trout x salmon hybrid offspring show almost equivalent fitness as the pure species, and male hybrids can be fertile when they reach reproductive maturity.

5. Variation in MHC immunorecognition genes explains a significant proportion of sperm precedence in sperm competition: males that are most similar at the MHC to the female win more of the fertilizations.



6. Salmon egg size shows natural variation, allowing us to test an important theory for the evolution of large eggs and numerous sperm under sperm limitation. Experiments revealed that larger eggs are indeed more fertilizable under conditions of sperm limitation.
Exploitation Route By appreciating the high risk of farm salmon introgression into wild populations, and the ecological disruption that can be caused by that.
Sectors Environment

URL http://onlinelibrary.wiley.com/doi/10.1111/eva.12148/full
 
Description To feed into the debate about escape farm salmon impacts, and to alert NGOs, policy-makers and the industry to the potential for employing triploid sterilisation to prevent farm salmon interbreeding.
First Year Of Impact 2009
Sector Agriculture, Food and Drink,Environment
Impact Types Societal

 
Description NERC Planet Earth podcast 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Interview on the project now online at Planet Earth website.

http://planetearth.nerc.ac.uk/multimedia/story.aspx?id=1423
Year(s) Of Engagement Activity 2013
URL http://planetearth.nerc.ac.uk/multimedia/story.aspx?id=1437&cookieConsent=A
 
Description New Scientist article 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact New Scientist article providing general coverage of research findings and implications for wild salmon and farm salmon improvement.
Year(s) Of Engagement Activity 2015
URL https://www.newscientist.com/article/dn25210-time-to-sterilise-farmed-salmon-to-save-wild-cousins/
 
Description Popular science article 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Article explained the threat from farm salmon escapes

Article referenced in newspaper articles about environmental incidents involving lost farm salmon
Year(s) Of Engagement Activity 2014
URL http://www.newscientist.com/article/dn25210-time-to-sterilise-farmed-salmon-to-save-wild-cousins.htm...
 
Description Salmon talks 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Talks to schools and public on hatchery visits about salmon biology, conservation, and our research with hands-on demonstrations of research and hatchery practice.
Year(s) Of Engagement Activity 2014,2015