The role of additive and non-additive genetic effects during animal contests in the beadlet sea anemone Actinia equina

Lead Research Organisation: University of Plymouth
Department Name: Sch of Biological and Marine Sciences


Variation between individual animals in their behaviour should be influenced by their genes and by their environment. Moreover, an animal's environment should interact with its genes modifying how they are expressed outwardly in the individual's phenotype. Understanding the relative contribution of these two sources of variation is key to understanding the evolution of critical behaviours. One of the most important areas of behavioural variation among individuals is in their fighting ability, because this determines their access to critical resources. In many examples of fighting animals we see variation in aggression and from an evolutionary point of view this is a puzzle. If evolution produces selfish individuals, and high aggression lets them win resources, why do we also see meeker individuals that cannot win against aggressive opponents? A set of theoretical arguments have been made that provide explanations for why we see this range of aggressive behaviour in animal populations. But without data on interactions between genes and environments we can't gauge how well these theories match the real world. Crucially, in fighting and other situations where there is a conflict of interest, an individual's rival (and therefore it's genes) form part of that individual's environment. To fully understand the evolution of aggressive behaviour we therefore have to understand not only the direct genetic contribution to an individual's aggressive behaviour; we also have to understand how this is modified by the behaviour and ultimately the genes of its rival. This effect is known as the 'genotype-by-genotype' interaction effect and at present very little is known about this for any animal, or for any type of conflict behaviour. He we will study genotype-by-genotype interactions in sea anemones. These are very common on the coasts of the UK and they are an excellent species to work on because they reproduce asexually, meaning that we can repeatedly look at fights between different clone-lines. Their fighting behaviour, as well as the outward characters that contribute to fighting ability are well understood. In this project, we will look at genotype-by-genotype interactions, variation in aggression within and between genotypes, the effects of past experiences of fighting and the effects of the degree of relatedness of fighting rivals. In this way we aim to solve long-standing questions about the evolution of aggressive behaviour. By the end of the study we hope to be able to explain why some individuals are more aggressive than others in animals.

Technical Summary

Aggression is very common in humans and non-humans. A full understanding of why aggression occurs, and persists, so widely across animal taxa requires that we also consider its evolution. A longstanding question is why variation in aggressive behaviour and fighting ability (RHP) is maintained in animal populations. Game theory proposes that negative frequency dependent selection can maintain a stable mix of strategies, but it does not account for the potentially complex genetic architecture that underlies variation in aggression. In particular indirect as well as direct genetic effects are likely to influence an individual's aggressive behaviour. Therefore we will study the role of additive and non-additive genetic effects (i.e. genotype-by-genotype interactions, GxG) for the first time in the context of animal contests. We have chosen the beadlet sea anemone Actina equina as out study system. These animals fight readily and reproduce asexually, allowing for the repeated contests between genotype pairs necessary for robust statistical analysis using mixed-effects models. GxG interactions will be studied from the perspective of both current and previous opponents, both of which are contribute to an individual's social environment. Recent studies show that consistent among individual and among genotype variation are partly dependent on within-individual consistency, and we will also assess the effects of genotype on this spontaneous intra-individual variation in aggression. Finally, we will use AFLP analysis to directly measure relatedness between genotype pairs, enabling us to assess how GxG interactions are modified by genetic similarity. The overall aim of this project is to resolve a longstanding question in animal behaviour; how is variation in aggression maintained in animal populations? We will use approaches from research on animal contests, animal personality, quantitative genetics and population genetics to answer this question.

Planned Impact

The wider impact of this research is likely to be in the areas of (1) enhancing the research capacity, knowledge and skills of businesses and organisations and (2) increasing public awareness and understanding of science.

Animal science is strongly aligned with research into methods of refining livestock production and the welfare of farmed animals (including aquaculture). Despite current advances in cloning vertebrates and potential future use of cloning as a means of enhancing livestock production, no research has yet been conducted on the potential for inter-individual aggression levels to be influenced by genotype by genotype interactions. Knowledge of genotype by genotype interaction effects could be used to enhance welfare and production by selecting individuals with compatible genotypes (i.e. combinations that will produce low aggression) for housing. Basic knowledge of whether this is likely to be a potential issue will be provided by our studies on a highly tractable model system. If genotype by genotype interactions influence aggression levels in sea anemones this would point to the need for future studies of additive and non-additive genetic contributions to aggression in other animals including livestock animals as well as ornamental animals used in the aquarium trade.

There is a huge public thirst for new information about the natural world, and in this project we will make new discoveries about a species that anyone living in the UK can readily encounter in its natural setting, and where related species are easily accessible globally. Furthermore, the core ideas underlying the research, the links between genes and behaviour, are of fundamental interest to the public and the concepts of animal personality and aggression are proven to attract the attention of the media. Therefore, this project is provides excellent opportunities for public engagement with science, in particular demonstrating the importance of fundamental science that can nevertheless be applied to tackling wider issues.


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Briffa M (2017) The role of skill in animal contests: a neglected component of fighting ability. in Proceedings. Biological sciences

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Lane SM (2018) What is a weapon? in Integrative and comparative biology

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Lane SM (2020) Analysis of direct and indirect genetic effects in fighting sea anemones. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

Description In our first experiment we looked at the effect of fighting experience (specifically winning or losing a fight) on subsequent fights, focussing on how these experiences can alter boldness, a measure of how individuals deal with risky situations. While an individual's boldness can change with experience, boldness is also a personality trait, in that individuals differ from one another in their average boldness. We investigated the relationship between fighting success and boldness (measured as recovery time when startled) across repeated contests in the beadlet sea anemones measuring boldness on five occasions before, between and after two contests. We found that boldness was generally robust to the effects of fighting experience, apart from a decrease in the immediate boldness of losers after their second fight. Furthermore, we found that while boldness before fighting significantly predicted fighting success and the level of aggression used in an individual's first fight, it did not predict victory or aggression in the second fight. Our findings indicate that different traits may be important in determining fighting success in consecutive fights and that fighting experience may alter which traits contribute to an individual's RHP. In this case, being bold is important for winning fights but only for 'rookies' - in more experienced fighters other aspects of fighting ability become important.
In our second experiment we investigated the costs of fighting, form the perspective of individuals that try to injure their rival and the perspective of individuals that receive those injuries. The ability to cope with these costs should depend on an individual's physiological condition. However, the experience of fighting itself may, in turn, affect condition, especially if there are injuries. Previous studies have found a correlation between immune state and fighting success, but the reason this relationship was unclear. Does immune state determine fighting success? Or does fighting itself influence subsequent immune state? Using the beadlet anemones we disentangled the cause and effect of this relationship, measuring immune response once before fighting and twice after a fight. In contrast to previous findings, pre-fight immune response did not predict fighting success, but rather predicted whether an individual used its weapons during the fight - individuals that showed signs of fighting an infection were less likely to use their weapons (stinging tentacles) in a fight compared with those in good condition. This is probably because as well as injuring the opponent, an individual's own tentacles also become damaged on use. Immune responses also changed following a fight. Individuals that used their weapons maintained a stable immune response following the fight, whereas those that fought without weapons did not. Although winners suffered a reduction in immune response similar to that of losers immediately after the fight, winners quickly began to recover to pre-fight levels. Our findings indicate that immune state can influence strategic fighting decisions and, that the chance of winning and levels of aggression behaviours used can affect subsequent immunity.

As well as internal (intrinsic) condition, an individual's performance in a fight can also be influenced by external (extrinsic) environmental conditions. Environmental contributions to fighting ability may be particularly important for animals living in habitats that are variable, especially if rivals have recently encountered different environmental conditions. Here, we investigated the relative importance of these extrinsic contributions to fighting ability and resource value on fighting in the beadlet sea anemone. We manipulated the extrinsic fighting ability of both opponents (through dissolved oxygen concentration prior to fights) and resource value (through seawater flow rate during the fight). Our results indicate that the extrinsic fighting ability of both opponents can interact with resource value to drive escalation patterns and that extrinsic drivers can be more important in determining contest dynamics than the intrinsic traits commonly studied. Our study highlights the need to combine data on intrinsic state and extrinsic conditions in order to gain a more holistic view of the factors driving contest behaviour.

Finally, we looked at the effects of how rival's genes influenced their fights. Evolutionary theory predicts that animals could differ not only in their boldness but in how they fight as well, for instance whether or not they deploy their weapons. However, the genetic basis for variation in fighting is poorly understood. We do not know whether it arises from individuals that always fight in a distinct way or from individuals 'flip-flopping' between different strategies from fight to fight, either at random or by tailoring their behaviour to match the opponent. One way to shed some light on this is to ask whether fighting is driven just by the genes of the individual (direct genetic effects, DGE) or whether the genes of the rival (indirect genetic effects + IGE) also have an effect so that the way the fight goes is the sum of both sets of genes (DGE + IGE). We also asked whether the effect of an individuals own genes on its fighting behaviour is modified by the genes of its opponent, so that fighting behaviour is the product of both sets of genes (DGE x IGE). Initially we thought that this could be done in a relatively straightforward way by using several offspring cloned from the same parent. However, a molecular analysis showed that the 'offspring' can often be unrelated to the 'parent' that has been brooding them, and they certainly cannot be assumed to be clones. This discovery clarifies a longstanding question about the reproduction of sea anemones but also meant that we had to change our approach to studying the genetics of fighting. Therefore we established the genotype of every anemone in our experiment and factored this information into the analysis. In the first ever study to look for DGE x IGE effects, we did not find any evidence that these exist in anemones. However, we did find that fighting is influenced by the genotypes of both individuals (DGE + IGE) and evidence that fighting ability can be inherited from parents. We also found that closer relatives fought for longer than more distantly related pairs. Overall, these results provide support for an important assumption of evolutionary theory - how an individual engages in a fight might be modified by recent experiences, internal condition or the external environment; but ultimately an individual's baseline mode of combat is fixed by its genes.
Exploitation Route Our studies have involved novel approaches to the analysis of fighting behaviour in animals, and we hope that other researchers will choose to build on our work by investigating on the links between immuno-status and aggression and the effect of external environments and aggression. The first experiment looked at how behaviour changes as a result of fighting across repeated fights and similar approaches could be used to investigate widespread 'winner and loser effects' in fighting animals. A key aim of the project was to understand the roles of direct and indirect genetic effects on fighting. We did this by incorporating molecular data into our analysis and the same approach could be applied to investigate direct and indirect genetic effects in other study systems. In addition, our specific result can be built on by theorists as provides support for a particular interpretation of basic evolutionary game theory. Finally, an unanticipated outcome of the project was to shed some light on an ongoing debate about the reproduction of sea anemones, which could now become a useful system for the study of alloparental care in animals.
Sectors Aerospace, Defence and Marine,Education,Manufacturing, including Industrial Biotechology,Culture, Heritage, Museums and Collections,Pharmaceuticals and Medical Biotechnology

Description One of the data papers published so far has been picked up in the press and a review article has been covered on a science blog. Video footage from the project has been used in a TEDx presentation. The BBC featured research on the current grant in the One Show.
First Year Of Impact 2017
Sector Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

Description BBSRC Standard Grants responsive mode
Amount £294,981 (GBP)
Funding ID BB/S004742/1 
Organisation University of Plymouth 
Sector Academic/University
Country United Kingdom
Start 12/2018 
End 11/2021
Description BBC one show 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact The One show, a daily magazine show on BBC 1, contacted me after picking up on a press release on one of the papers for this grant . They visited the lab at Plymouth and Dr. Sarah Lane and I set up some fights in sea anemones for them to film. As I've been interviewed a few times before for this TV show, we decided that it would be a good idea for Dr. Lane to do this one, so she was interviewed in the broadcast and was able to explain fighting in sea anemones and some of our research questions to the audience of the One show (average audience is 5 million viewers). The film crew and producer were very impressed with Sarah and we also captured some fabulous footage of anemone combat that was broadcast.
Year(s) Of Engagement Activity 2019
Description Public talks 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Dr Lane gave two public lectures on our research at local wildlife / voluntary organisations, in October 2018 at Wembury Marine Center, and January 2019 at Coastwise North Devon. Sarah reported engaged audiences who were surprised at how interesting sea anemone behaviour is. This has the potential to feed into 'rock pool safari' type events run for the public by these organisations, increasing public awareness of these animal behaviour.
Year(s) Of Engagement Activity 2018,2019
Description Science News website 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Our research on anemones was cited and featured heavily in a lay article (aimed at an informed audience) about fighting in animals, in Science News magazine, which is published by the Society for Science and the Public. The intended audience was the general public and scientists, and the article included direct quotes from an interview with them. The feedback I've had on this is from colleagues who have said that (a) the article should increase public interest in animal aggression and (b) that they can see how sea anemones are a model system for the study of aggression.
Year(s) Of Engagement Activity 2018