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Research into the remarkable mating system of the bitterling fish carried out at the University of Leicester was recently reported in The Independent. Dr Carl Smith, Lecturer in Zoology at the University, reveals new insights into the amazing relationship between bitterling and mussels.

Recent research in the Department of Biology at the University of Leicester has revealed remarkable complexity in the mating system of a small species of freshwater fish called the European bitterling.

The bitterling fishes are a group within the carp family, and while the 44 or so known species of bitterling live in China, Korea and Japan, one species, the European bitterling, which measures 4 or 5 cm 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 riverbed, about a square metre or so, that contains mussels.

At about the same time the females grow a peculiar, long tube that hangs from her abdomen. This is called an ovipositor and it is through this that the female lays her eggs; the length of a female’s ovipositor can be equivalent to that of her own body. Males perform courtship displays to passing females, and if the female shows interest she is led to a mussel.

The female inserts her ovipositor into the opening through which the mussel expels water – its ‘exhalant siphon’ – and into the mussel’s gills, where she deposits two or three eggs, each an unusually large 3 mm in diameter. The male then releases sperm into the ‘inhalant siphon’ of the mussel. The sperm are drawn into the gill of the mussel where they fertilise the eggs. Two or three days later the eggs hatch and develop into embryos where they remain, emerging as small fish about a centimetre long, around a month later.

This interesting relationship between fish and mussel, though widely recognised, was little studied until Dr Carl Smith at the University of Leicester, along with Dr Martin Reichard and Dr Pavel Jurajda at the Institute of Vertebrate Biology of the Czech Academy of Sciences in Brno, began research in 1995. Incidentally, Brno is the home town of the Czech monk Gregor Mendel, whose experiments with pea plants led to the foundation of the science of genetics

Research started in a series of small lakes where mussels and bitterling were abundant. Initially, research aims were modest and directed at understanding how female bitterling made decisions about where to lay their eggs. Now research groups in Leicester and London in the UK, the Czech Republic, Poland, Russia, China and Japan are collaborating to understand more about the complex breeding system of bitterling.

For many years it was 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 a symbiotic mutualistic relationship. This symbiosis was supposed to be based on the bitterling using mussels as a foster parent for its eggs, and the mussel using bitterling to transport its own young called ‘glochidia’.

Glochidia are tiny, hinged structures that snap shut on the fins or gills of passing fish and in this way get transported to different parts of the lake or river. Because bitterling are always in close proximity to mussels, it was assumed that they would act as couriers for glochidia.

However, when researchers started looking more closely at this they began to realise that the whole story was a lot more complicated than it first appeared.

Many female bitterling lay their eggs in the same mussel, and in some cases the mussels are literally bulging with hundreds of these large eggs. Dr Martin Reichard, a Czech post-doctoral researcher based in Leicester, has shown that the mussel can become so overloaded with eggs that it stops growing.

Furthermore, studies in the Czech Republic by Dr Reichard and Dr Markéta Ondračková of the Institute of Vertebrate Biology in Brno have shown that the bitterling does not carry glochidia. It is extremely rare to find them attached in natural conditions, and even if they do attach to the fish, the glochidia very quickly drop off.

Far from being a relationship of ‘mutualism’, the bitterling is in fact a parasite of mussels; a rare example of a vertebrate parasitising an invertebrate.

Having set the record straight on that aspect of the bitterling’s relationship with the mussel, Dr Smith and his co-workers have turned their attention to other aspects of the behaviour of the bitterling and have revealed a raft of unusual phenomena.

Working with his colleagues in the Czech Republic and Dr Mirek Przybylski of the University of Łodz 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, 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. “So in that respect the David Beckhams of this world get the girl. 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 could 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 certainty that he fertilises it. So the male and female have very different priorities. This is a nice example of what biologists call an intersexual conflict.”

In another remarkable twist, experimental studies have shown that male bitterling that are unable to obtain territories or attract females have a tactic for getting to reproduce – they release sperm into the gills of mussels guarded by other males. Using DNA fingerprinting techniques developed by Professor Sir Alec Jeffreys in the Department of Genetics, Dr Reichard and Dr Bill Jordan at the Institute of Zoology in London found that 'sneaker' males that released sperm into a mussel prior to a female laying her eggs had a good chance of fathering some offspring. Incredibly, once released into a mussel, sperm remains viable for up to at least 20 minutes – far longer than in other fishes.

The scientists have recently started to look at other bitterling species in China and the Russian Far East and Japan. 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 in tandem, 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.” A Leicester postgraduate student, Shama Zaki, has begun research to investigate how and when the bitterling found its way to Europe.

Over the years this research has been supported by the Royal Society, The Leverhulme Trust, the Czech and Chinese Academy of Sciences, and the Natural Environment Research Council. The Natural Environment Research Council have also recently awarded a postgraduate studentship to the latest addition to the research group, Chris Pateman-Jones, who will investigate how fertilisation occurs inside the gills of mussels.

So it would seem that the textbooks will need to be re-written. 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’, ‘evolutionary arms race’, or even ‘making the best of a bad job’.

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