Quantifying fitness benefits of polyandry in Atlantic salmon

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


Why do females of so many species mate with multiple males, when they gain nothing from this 'polyandry' apart from spermatozoa, and mating with only one male is sufficient to ensure full fertility? This remains an enduring question in evolutionary biology, because significant costs have been measured for females when they multiply mate. We now know that the mechanisms operating at the gamete level between mating and fertilization are much more complex than previously supposed. Under polyandry, with bigger and more diverse populations of spermatozoa competing for fertilization, there is even more selective opportunity for adaptations that promote sperm competitive ability, and / or cryptic female choice. Recent experimental research suggests that polyandry allows females to 'capture' genetic benefits at the gamete level for their resulting offspring. Such benefits may arise because of links between sperm quality and general fitness, or because females have evolved mechanisms that allow selection of sperm that carry intrinsically superior genes or undamaged DNA, or there may be cryptic choice for sperm that carry genes that are more compatibile to the female/egg genotype. We propose to quantify benefits of polyandry in a system using carefully controlled in vitro fertilizations to create offspring batches from the same female that only differ according to whether they were fertilized by five separate males singly, or by the same five males but in simultaneous sperm competition. Our experimental model will be the Atlantic salmon, in which females naturally mate with up to 16 males at once, and where external fertilization allows us to conduct in vitro fertilizations that control or eliminate a number of important confounding effects on offspring fitness, such as biased or variable maternal investment in egg quality. Our previous work on salmon in vitro fertilization dynamics will allow us to ensure that fertility is not a limiting factor for each egg batch. For each female, we will create 5 egg batches which were fertilized by sperm from 5 different, single males (=monandrous condition), and 5 egg batches that were fertilized by homogenised mixes of sperm from the same 5 males (= polyandry condition). These paired comparisons will be repeated 25 times, using 25 females and 125 males. The design will control for adult identity and egg effects, and generate offspring batches that only differ according to fertilization in the presence or absence of sperm competition and/or egg choice. After fertilization, the offspring batches will be measured for survival and growth across key stages of embryo development, egg hatch, alevin development, fry emergence, and parr survival, success and growth. These fitness measures will all be conducted in experimental stream sections that allow environmentally-relevant selection to operate. Use of the Ims salmon field station in Norway will provide access to facilities that enable experimental control, while rearing eggs and fry in semi-natural conditions with selection from many of the normal forces that operate on salmon eggs, embryos, fry and parr. It is essential that we measure egg and offspring perfomance under conditions that present some selection from the natural environment, because this is where fitness benefits will be most important. At the conclusion of the project, we will have measured what fitness benefits can be gained under polyandry, and what life stages these gains occur in salmon. The results will be of central importance to a pure understanding of the genetic benefits of polyandry. Importantly, our work will have applied relevance for salmon hatchery breeding strategies. To conserve genetic diversity, hatchery protocols now use enforced monogamy to maximize the number of male breeders involved in reproduction. However, there may be important polyandry benefits that are excluded by these protocols, and our project will measure how important these benefits might be.
Description We discovered that allowing eggs choice of a range of males' sperm did not improve subsequent offspring fitness in the hatchery or semi-natural streams. The research allowed a powerful external fertilisation experimental test where we balanced male and female genotypes but allowed one treatment to be fertilised by a mix of 8 males' sperm, and the other to be fertilised by 8 different males separately. We repeated this for multiple egg batches, split between individual females.
Exploitation Route The results indicate that fish hatcheries, under normal conditions, do not give offspring batches genetic quality benefits by mixing sperm from multiple males.
Sectors Agriculture, Food and Drink,Environment

Description Results are published; impact will be achieved by informing salmon hatchery protocol designs through our ongoing work with hatchery collaborators and land catch salmon farming ltd. The conclusion of the publication (which is Open Access) identifies a route to preserving genetic diversity while minimising risks of infertility within hatchery artificial fertilisation protocols.
First Year Of Impact 2016
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.

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 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