It's all take and no give

Scientists used to think that mussels and fish enjoyed a mutually beneficial relationship. A new study reveals that the truth couldn't be more different. Simon Hadlington reports

This is not one of Aesop's fables, but it might well have been: "There were once two fish, one male and one female, who wished to find a safe and secure place to lay their eggs and hatch their young. The male fish saw a mussel lying at the bottom of the lake. 'You could lay your eggs inside the mussel!' he cried. 'They would be safe and secure!' So the two fish asked the mussel if they might lay their eggs inside it. The mussel said: 'That is all well and good, but what do I get out of this arrangement? What's in it for me?' 'What would you like?' asked the fish. 'Well, you can swim and I cannot,' said the mussel. 'When my own offspring hatch, I would like you to carry them far and wide across the lake to find new places to live. In return for this, I will agree to guard your eggs.'

This is not one of Aesop's fables, but it might well have been: "There were once two fish, one male and one female, who wished to find a safe and secure place to lay their eggs and hatch their young. The male fish saw a mussel lying at the bottom of the lake. 'You could lay your eggs inside the mussel!' he cried. 'They would be safe and secure!' So the two fish asked the mussel if they might lay their eggs inside it. The mussel said: 'That is all well and good, but what do I get out of this arrangement? What's in it for me?' 'What would you like?' asked the fish. 'Well, you can swim and I cannot,' said the mussel. 'When my own offspring hatch, I would like you to carry them far and wide across the lake to find new places to live. In return for this, I will agree to guard your eggs.'

"The fish thought this a splendid bargain. So the female laid her eggs inside the mussel and and the eggs remained safe and secure until they hatched and the new born fish swam away. And when the mussel's own offspring appeared, they clasped themselves to the fish and were carried to fertile new homes in other parts of the lake. And the world marvelled at this wonderful cooperation between these animals. Textbooks held it up as an ideal of creatures working together to mutual advantage."

And that would have been the happy ending until a scientist took a closer look at the relationship between the fish and the mussel. He discovered that in fact the mussel can become so packed with these eggs - which incidentally are enormous - that the mussel stops growing. Furthermore, the mussel's own larvae are unable to cling to the fish, so they cannot be transported around the lake. In other words the benefits are all one-way. The fish indeed has somewhere safe for its eggs, but the mussel receives nothing from the arrangement except hardship.

The moral of the story: surrogacy agreements are fraught with pitfalls.

The scientist who uncovered the true nature of the relationship between the fish and the mussel is Dr Carl Smith, a zoologist at the University of Leicester. For the past 10 years Dr Smith and his colleagues have been studying the spawning behaviour of a fish which is rather small and rather unusual called the European bitterling. The bitterling is a member of the carp family, and while the 44 or so known species of bitterling live in and around China, one species, the European bitterling, which measures 4 or 5cm long, has become established in lakes and rivers in central and eastern Europe.

The strange spawning habits of the bitterling were first noted by naturalists in the 1800s. In early April the male develops bright colours and aggressively defends an area of the lake or river bed measuring about a square metre or so, that contains mussels.

Soon afterwards the females grow a peculiar long tube that hangs from their abdomen. This is called an ovipositor and its purpose is to deliver the eggs. A male approaches a female, displays his colours and performs a mating dance. If the female shows interest she is led to a mussel.

The female inserts her ovipositor in the opening through which the mussel exhales - its "exhalant siphon" - and into the mussel's gills, where she then deposits two or three eggs, each a relatively large 3mm in diameter. The male then releases sperm into the "inhalant siphon" of the mussel. The sperm are drawn in where they fertilise the eggs. Two or three days later, the eggs hatch and develop into embryos and emerge from the mussel about a month later as small fish which are about a centimetre long.

"For many years it has been received wisdom that the relationship between the mussel and the bitterling was a mutually beneficial one, and is routinely cited in textbooks and encyclopaedias as an example of what is termed 'mutualism'," says Dr Smith.

"When the eggs of a mussel hatch they release microscopic larvae called glochidia. These are tiny hinged structures that snap shut on a passing fish and in this way will get transported to different parts of the lake or river." Because bitterling are always in close proximity to mussels, it was long assumed that they would act as couriers for the glochidia.

"But when I started looking more closely at this I began to realise that the whole story was a lot more complicated than it at first appears," Dr Smith adds.

Many females lay their eggs in the same mussel, and in some cases the mussels are literally bulging with hundreds of these large eggs. "We have shown that the mussel can become so overloaded with eggs that it stops growing," says Dr Smith.

Furthermore, studies have shown that the bitterling does not carry glochidia. "It is extremely rare to find them attached, and even if they do become attached to the fish, the glochidia very quickly drop off," says Dr Smith. Far from being a relationship of mutualism, the bitterling is in fact a parasite of the mussel.

Having set the record straight on that aspect of the bitterling's relationship with the mussel, Dr Smith has turned his attention to other aspects of the behaviour of the bitterling and has revealed a raft of unusual phenomena. Working with his colleagues Dr Martin Reichard of the Czech Academy of Sciences and Dr Mirek Przybylski of the University of Lodz in Poland, Dr Smith has shown that the males and females have polarised attitudes towards mating. The male is first and foremost interested in ensuring that it is his sperm that fertilises an egg, come what may. The female is much more keen to ensure that her eggs have a good chance of surviving, and is less bothered about the quality of the male that fertilises her eggs.

To show this, the research team set up a series of blind dates among the fish, presenting the female with males of varying quality - as measured by the gaudiness of their mating colours. "We found that the females preferred high-quality males," says Dr Smith. "But when the male invited the female to inspect the mussels he'd been guarding, she was fussy about their quality. She would only lay in good-quality mussels and if he didn't have any that were up to scratch she would lose interest and go elsewhere."

Many males attempt to fertilise eggs in the same mussel. The researchers presented males with good-quality mussels that had already been visited by other males and with poor-quality mussels that had not. "We found that the male would prefer to deposit its sperm in the poor-quality mussel," says Dr Smith. "In other words the survival of the egg was less important to the male than the possibility that he fertilise it. So the male and female have very different priorities. This is a nice example of what biologists call intersexual conflict."

The scientists have recently started to look at bitterling species in China. Curiously they have shown that the mussels there are much more reluctant to accept eggs than those in Europe, and that around half of all eggs that are deposited in the mussels' gills are ejected.

"We suspect that the Chinese mussels have evolved to reject the eggs, whereas the European bitterling is probably a relatively recent invader and is able to take advantage of the native mussels' naivety," says Dr Smith. "In China the mussels are less heavily parasitised. It looks as though the fish and the mussel have evolved at the same rate, and that there is an evolutionary arms race going on, with each animal evolving new strategies to cope with the other. We are not yet seeing this arms race in Europe - the bitterling has the upper hand at the moment."

So it would seem that the textbooks will need to be rewritten. While the bitterling and mussel can no longer be cited as a neat example of mutualism, they may yet find an entry under "intersexual conflict" or "evolutionary arms race". Alas, the story has unfolded 2,500 years too late to be included in Aesop's fables.

LET'S STICK TOGETHER: RELATIONSHIPS IN NATURE

* Parasitism

One organism living at the expense of another. Parasites can live inside or outside the host species and can range in size and life cycle from the malaria microbe ( right) to the cuckoo.

* Symbiosis

This is when two species live in a partnership where both benefit. The hermit crab Pagarus and the sea anemone Adamsia palliata are an example, with the anemone carried on the crab's shell to get food scraps and the crab obtaining camouflage in exchange.

* Commensalism

When two species live in close association with little or no obvious advantage or disadvantage to either. Some bacteria living on human skin seem to answer to this definition.

Steve Connor