A well-developed eye for males

The females of some cichlids in  Lake Victoria have adapted their eyes to differences in the light spectrum, and therefore fall for differently coloured males, as Martine Maan has discovered.  This has led to the formation of new species.  Her next question is:  Does this also apply to Panamanian poison frogs?

Pollution and turbidity
For more than thirty years, Leiden biologists have been conducting research into cichlids in Lake Victoria - these are fish which are well known for the enormous diversity of their species.  This richness reduced dramatically as a result of the introduction of the Nile perch, and the pollution and turbidity of the water. 

The cichlids have no reason to complain about public interest.  Biologist and writer Tijs Goldschmidt reported on the drama in his book 'Darwin's Pond', and director Hupert Sauper last year made a film entitled 'Darwin's  Nightmare', in which he denounced the international fish trade.  Even though the evidence is relatively small and the water equally turbid, it does seem as if a few species are appearing.  Whether or not these are new species is not yet clear.

In harmony with one another
An important aspect of the Leiden cichlid research, including that of Martine Maan, is focused on the mechanism of species formation.  This is something which is still not fully understood by evolutionary biologists.  It is understandable that species formation comes about if animals from one species migrate to new locations, thereby making contact between the members of the species impossible.  But how can such a variation come about within one area like Lake Victoria, where the new species co-exist in harmony with one another? 

Rubicon
'I'm not looking at the extinction of the species, but am more concerned with the turbidity of the water,' says Maan.  For her dissertation she examined the relationship between partner selection based on colour and species formation in two cichlid species.  On Thursday 11th May she will obtain her doctorate, under the supervision of Jacques van Alphen and Ole Seehausen. Maan discovered that the visual system of these cichlids has become adapted to the environment, whereby species formation can take place by means of partner choice based on colour.  She has been invited by the American biologist Molly Cummings, well known for her innovative work in the field of frog colours, to visit Texas to apply to frogs what she has learned from her study of these fish.  She has been awarded a Rubicon subsidy from NWO to carry out this reseach.  Rubicon is a new subsidy which enables recently qualified PhD candidates to carry out research abroad.  

Partner selection based on colour
Martine Maan: 'The members of the cichlid species which I study are very similar in terms of shape.  In an aquarium, it's difficult to tell them apart.  But the males have completely different colours:  one species is red and the other blue.  We often see this with fish:  two species which are the same apart from their colour.  Colours play a role in partner selection by females, but the question is: how does this work?  And moreover:  how could this choosiness lead to the formation of new species?'  

Males and females of the cichlid species pundamilia pundamila and pundamilia nyererei. This last species was named after President Nyerere. The males are either red or blue.

Mouth brooders
With most types of cichlids, the females are the choosy ones.  Maan:  'They are careful with their selection of a male because procreation is an enormous investment on their part.  They incubate the eggs in their mouths.  They keep them in their mouths for three weeks, which means they are unable to eat for this period of time.  Even once they have spat out the young fish, the females continue to care for them.  This is also a reason why these cichlids are very popular with people who keep aquariums; their breeding behaviour is interesting to watch.  But the males do absolutely nothing to assist in the brooding process, apart from mating.  So, you don't just choose a male on a whim; there has to be a good reason.' 

Bright colours
First of all, Maan researched whether females of the red species did actually look at the colour of the males.  They did.  'We found that the females choose the most brightly coloured red males.  They don't fall for very large males, or for males with a lot of yellow on their sides.  Their preference is for the most brightly coloured males of their own species.'

Good progeny
In evolutionary biology, nothing happens just because it looks good. Maan: 'The next question is: what extra do those brightly coloured males have to offer the females?  Since in terms of fatherhood, little is expected of them, can it only be a matter of genetic effects?  These males in some way or another have to guarantee good progeny.'

Less parasites
One important genetic advantage is resistance to parasites. Maan: 'Just as with many other animals, these fish are involved in a continuous battle with parasites.  So males with few parasites have a definite advantage.  I therefore decided to look at the number of parasites carried by males and did indeed find that for both types, the blue and the red, the more brightly coloured males were less strongly infected.  This suggests that the females choose particular males because they have a better immune system, or are better able to avoid parasites.  The offspring can inherit these qualities from the father.'

And the females?
That's another bit of the puzzle solved.  But an evolutionary biologist is still not happy, because what is then the connection with species formation? 'There is a lot of literature about partner selection,' according to Maan, 'but it is still not clear why females differ in their selection.  They must differ somewhere because if all females were to choose the same evolutionary advantage, you wouldn't get any new species.' 

Sensitive eyes
The difference, she discovered, is in the eyes.  The eyes of the females have adapted to their environment, and have become sensitive to different colours of light.  Maan explains: 'The blue and red types are not found at the same depth of water.  The blue fish swim one metre deep, and the red six metres deep. Not all light wavelengths are able to penetrate so deep in the turbid water of Lake Victoria. Blue light is soon lost, and the deeper you go, the more red the light spectrum becomes.  The species at one metre deep still has a broad light spectrum, but at six metres underwater the spectrum is more red.  At one metre deep blue is more easily discerned, and at six metres, red is more noticeable.'

Double advantage
'Then I asked:  have the eyes of the fish also adapted to the light spectrum?  And indeed, we saw in experiments that the visual systems differ.  The eyes of the fish in deep water are more sensitive to red light, so that bright red stands out more, and the fish in shallow water are more sensitive to blue light, so that bright blue attracts attention.  If you, as a male, want to be seen, then it's better to be red or blue, and not something in between, because then you won't be noticed anywhere.  The in between group gets ignored, which means the red and blue are left.  The offspring of these brightly coloured males and colour-sensitive females have a double advantage:  from their father they inherit resistance to parasites, and from their mother they get a good eye for the local conditions and the right partner.  Species formation can occur as a result of adapting the eyes of the females to the micro environment.' 

A different lens
The results of Maan's research attracted the attention of American biologist Molly Cummings, who conducts research into the function of colour in poisonous frogs, and who is also very interested in the adaptation of the optical system to environmental factors.  Cummings persuaded Maan to join her in Austin to conduct a joint project on the poison dart frog.  Maan is looking forward to the move.  'I find fish very interesting and you can do some excellent work with them, but I also have to consider my career.  I want to avoid being seen as only a fish expert.  Also, if you look at a different system, you do so through a different lens than the established researchers. So, you look for something that has some overlap, yet is also different.  And I love working with colour.  I met Molly Cummings at a congress in Finland and found her very inspiring.  She was extremely enthusiastic when she heard my account of the cichlids, and we devised this project to do together.'    

Predators 
The project concerns frogs which live on the numerous islands of West Panama.  Maan: 'There are many colour variations, which is a bit mysterious.  The frogs are poisonous, and their extremely bright colours are intended to repel predators.  The idea is that if a predator once tries to eat one of these frogs, it will be enough to stop him trying it again.  But poisonous prey often have only a limited range of colours, such as black, red and yellow.  Just like wasps and bees.  A predator only has to make the mistake once and he will subsequently avoid anything that's black and yellow.  So, the enormous variation is rather strange. There are a lot of ideas about this, and one of the ideas is similar to my cichlid theory: that partner selection takes place on the basis of colour and that the optical system of these frogs is therefore adapted to environmental factors.'  

Orange with orange
'It's very exciting,' she continues, 'because with the fish I had more information in advance, whereas much less research has been done with these frogs.  For the time being I will only be looking at the females, and I will be trying to find answers to the following questions: 'Do they want males from their own species?  Do they want the most striking of these males? And if so, why?'

'I do have a couple of starting points.  Unlike with the cichlids, the male and female frogs look the same, but like the cichlids, they want to mate within their own colour range:  orange with orange, for example.  I will be conducting experiments on partner selection, and will then be looking at the visual characteristics of the animals: I will have them follow a stimulus in a dark room and highlight it with a green light, for example, that steadily becomes weaker, so that I can see which colours they are most sensitive to.'

'A brightly coloured frog: get away!'
Unlike many other frogs, these creatures are active in the daytime.  Maan will take a boat to the islands to take spectrum measurements of the light conditions.  'Finally, but that will only be in the second year, I will be looking at the predators.  We will just use chickens for this.  It might be that this colour variation makes no difference to them, and they simply react with:  'A brightly coloured frog: get away!'  Molly Cummings recently wrote in Nature that predators tend to generalise.  For example: if prey with a yellow and black pattern of colours are very poisonous, the predators tend to avoid yellow.  But how broadly do they generalise?  This is an important point, because if the colour of the frogs isn't important for the prey, then natural selection by predators isn't a problem.  In this case, colour variation may simply be a response to sexual selection.'  

Poisonous frogs in West Panama:  Dendrobates pumilio ('strawberry poison frog') Photo's : Kyle Summers

(9 May 2006/HP)