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Coral reef fish shape our understanding of social evolution

Periodic Reporting for period 1 - SoEvoFish (Coral reef fish shape our understanding of social evolution)

Reporting period: 2019-08-15 to 2021-08-14

Complex society, where some individuals get to reproduce and others don't, are an evolutionary mystery. It is not clear how genes for cooperation get passed on if individuals do not have offspring themselves. The problem my project aims to address is that most of our knowledge of how complex societies evolve comes from terrestrial animals like birds, mammals and insects. However, there are complex societies in very different organisms, such as coral reef fishes as well. I use clown anemonefishes and emerald coral gobies as model organisms to broaden out understanding. Both species live in groups with strict size hierarchies, where only the largest two fish get to reproduce. So the question is, why do the non-breeders accept their situation? and why do the dominant breeders accept the subordinates to share their space and resources?

Understanding how animals evolved to be group living means understanding one of the big transitions in the history of life. This project will also help us understand the close mutualism between coral reef fishes and their anemone or coral hosts better, a relationship that is foundational to coral reef ecosystems.

The overall objective of the action is to create a more general framework of social evolution, including all major social, ecological and genetic hypotheses. I aim to address whether coral reef fish live in groups with relatives, whether there are feedback loops between the fish and the anemone and finally create a theoretical framework that includes mutualism.
The first objective of the project was to figure out whether coral reef fishes that live in complex groups are related. In other animals such as birds, mammals and insects, group formation is often explained by the group members being close relatives, such as siblings or parents/offspring. In coral reef fishes we assumed for a long time that group members would not be related, because most coral reef fishes have a larval dispersal phase where they travel long distances in the open ocean before settling onto a reef. It is not clear whether the larvae, after they travelled for so long, have a chance to settle close to their close relatives. To address this question, I travelled to Papua New Guinea and took genetic samples from 17 groups of emerald coral gobies. I used DNA fingerprinting to find out how closely related the fish were. The results were surprising, because I did find that fish in the same group are closer related than fish that are further apart. This helps us understand why dominant breeders might accept the non-breeding subordinates: they are relatives that will eventually inherit the territory they live on.

To address the second objective of the project, I used laboratory experiments to find out if vertebrates can adjust their growth rate in response to their mutualistic partner. Anemonefish and anemones live in a close mutualistic relationship. The fish and the anemone exchange nutrients and they protect each other from predators. There is a lot about this relationship we do not understand yet and we do not know how this mutualism might impact the social evolution of the fish. By looking at the growth rate of juveniles in different sized anemones, we can begin to understand what effect a larger healthier host (anemone) has on the fish. I found that clownfish do change their growth depending on how large the anemone is that they live in. The juveniles in the larger anemones grew faster than the ones in the smaller anemones. This is the first time this flexibility in response to a mutualistic partner has been shown in any animal and it helps us to begin to understand the big impact fish and anemones have on each other.

I wrote a literature review to summarize the current state of the art in social evolution of coral reef fishes, and to identify crucial knowledge gaps and the most interesting future research directions. For this review I worked together with colleagues from Australia and the US. We summarized what we know about social evolution in coral reef fishes and all the experiments that have been done on anemonefish, gobies and other species that live in complex social systems. We identified some crucial research directions that deserve more attention, such as addressing the question of why dominant breeders accept subordinate non-breeders in their territories, how different species compare to each other, using new analysis techniques to understand more complex groups, and addressing how climate change will impact the social live of coral reef fishes. The review is already widely read and will help move this research field forward.

These results of all objectives so far were published (or are under review) in high impact journals, and they were disseminated through news reports, conference talks and invited seminars, both for the scientific community and the wider public.
The work conducted on the project so far has solved some mysteries of social evolution and led us closer to a social evolution framework that is relevant for all vertebrates living in complex societies.

We now understand that fish in these social groups might be closer related than the population overall, which helps explain why dominant breeder accept non-breeders to share their territory and resources.

We also understand more of the immense impact the anemone has on the fish. This topic will open a whole new research direction into effects of the anemone or coral host on the social evolution of coral reef fishes.

We are getting closer to having a general framework for the social evolution of coral reef fishes, but some crucial knowledge gaps remain, as our literature review uncovered.

The next part of the project, using mathematical modelling to create a social evolution framework that includes mutualistic partners, will make the work applicable not just to our model organisms or coral reef fishes in general, but to any animal that lives in close mutualistic relationship with another organism.
A breeding pair of A. percula and their anemone host in Kimbe Bay, Papua New Guinea
Dr Theresa Rueger measuring an anemone in Kimbe Bay, Papua New Guinea
Amphiprion percula and their anemone host in Kimbe Bay, Papua New Guinea.