'Nemo' and the evolution of helping behaviour

Anemonefish are one of the most recognised of all coral reef fish, and have found a place in the hearts of divers and non-divers alike following the success of the Pixar film, ‘Finding Nemo’. But did you know that these beautiful fish have helped scientists better understand the evolution of cooperative behaviour?

With their bright colours and frenetic behaviour, anemonefish are easily spotted by both scuba divers and snorkelers. The 30 different species are found from the Indian Ocean across to the Pacific - some endemic to isolated islands or atolls, others distributed across the oceans. But all are found living with an anemone host. In fact, the anemonefish and their host form one of the most famous examples of a symbiotic, mutualistic relationship; one in which both sides of the partnership benefit.

How does the partnership work? The anemones’ venomous tentacles help to protect the fish, and the host also provides food in the form of scraps left over from the anemones’ meals. In return, the fish defends its home from any big predators looking to make a snack of the anemone, and provides nutrient-rich faeces for the algae that live in the tissues of the anemone. The anemonefish’s activity also increases water circulation around the anemone, aerating the tentacles.

It's not entirely understood how anemonefish survive surrounded by their partner’s venomous tentacles, but it is highly likely that the fishes’ mucus covering plays a vital role. The latest research has delved into the population of microbes that live within this mucus, as well as on the anemone host, and how these microbes may alter the chemistry of the fishes’ protective coating so that it resembles that of the anemone. Whether this new chemical identity inhibits the stinging cells from firing, or is simply identified as being part of the anemone is still uncertain.

As well as having a fascinating relationship with their hosts, the sex lives of anemonefish have also long intrigued scientists. Within the anemone, these fish live in groups dominated by a breeding male and female pair, and several smaller, nonbreeding males which help defend and maintain the anemone. Within the group there is a hierarchy of dominance based on size; the breeding fish are the largest, and the nonbreeders get progressively smaller. And like many other reef fish, anemonefish are sequential hermaphrodites. If the breeding female dies, the next largest male changes sex, rapidly grows in size and starts to reproduce with the dominant male.

At first glance, anemonefish groups appear to be similar to other animal societies where individuals forgo reproduction and help others to do so. Such cooperative behaviour has evolved many times throughout the animal kingdom - from birds to bees - but Darwin struggled to include such behaviour within the framework of natural selection. It wasn’t until modern genetics and the development of kin selection theories in the 1960s that scientists began to understand how such cooperative behaviour might evolve.

Essentially, there are two ways for individuals to pass their genes to the next generation; either directly, by producing their own offspring, or indirectly, by enhancing the offspring production of their relatives. Helping relatives can be favoured by kin selection because the related offspring share copies of the helper’s genes. And when this gene-level view is taken into account, two critical predictions can be made: first, that helpers enhance the fitness of breeders; and second, helpers are closely related to breeders.

Whilst these two predictions have been shown to be true across many examples of cooperative behaviour, incredibly, recent research on anemonefish has revealed that their situation is entirely different, and the theory of kin selection and cooperative behaviour has been turned on its head.

The first startling discovery showed that the individuals in an anemone are, in fact, not closely related at all! After anemonefish eggs hatch, the larvae are dispersed by the currents and settle elsewhere - and it is very unlikely that a juvenile will settle on the same anemone as its parents. The second discovery revealed that the nonbreeding fish actually have no impact on the survival or reproductive success of the breeding pair. Both results challenge the predictions that have been shown to be true in so many other species. So what is going on?

What scientists have discovered is that it is the likelihood of future success - so called future selection - that underpins the evolution of cooperative behaviour in groups of unrelated animals such as anemonefish. Research by Peter Buston and his team from Boston University revealed that within a group, the largest nonbreeding individual always moves up and inherits the breeding vacancy. There is no fighting over the empty slot, and no outsiders ever take over. Peter Buston has described this as the ‘perfect queue’ and one of the clearest demonstrations yet that individuals will adopt nonbreeding positions in a group based on the potential for reproductive success in the future.

But the story is not quite complete. What is also needed is an explanation as to why nonbreeding individuals don’t go elsewhere to produce young, and why they don’t try to usurp the breeding individuals from their positions - a coup within the anemone.

Once again, Peter Buston’s team found that the risk of trying to locate another anemone, let alone one that is vacant, is so high that the benefits of staying far outweigh those of leaving. There are simply too many predators on the reef. This ecological constraint suggests that if an individual’s independent breeding options are so poor, the only way to reproduce is to settle into an anemone as a nonbreeder and join the queue, even when you’re not closely related to the dominant breeding pair.

Social constraints also play their part. Why wait for the larger fish to die? Why not oust the breeding pair and stage a coup? The team discovered that dominant individuals will sometimes evict nonbreeding fish if they become very close in size. And that size differences are strictly defined and seem to be actively maintained by growth regulation - nonbreeding fish will actually slow down their growth by fasting so as to reduce the risk of being evicted. Taken together, these two pieces of evidence suggest social constraints - the hidden threat of eviction - also play a major role in explaining why an anemonefish might take on a nonbreeding role.

The classic explanation for the evolution of nonbreeding roles and cooperation is based on kin selection - helping behaviour amongst related animals can be favoured because the relatives’ offspring share copies of the helper’s genes. But anemonefish groups have forced scientists to look at this theory with fresh eyes.

For divers and snorkelers, anemonefish are a captivating species darting around its anemone host. But for Peter Buston and his team, they are a living laboratory that has shed light on the evolutionary framework behind helping behaviour in animal groups.