Cuckoos – evolution of a parasitic arms race

reed warbler feeds a cuckoo chick

There are over 100 species of cuckoo which show a wide range of breeding behaviours, but brood parasitism is extremely common, occurring in 59 species. This is where eggs are laid in another birds nest, so the cuckoo doesn’t have to build its own nest, incubate the eggs, or feed and protect the young until they fledge. The common cuckoo (a summer migrant in Europe and Asia which winters in Africa) is the most well know of these. How this mode of breeding first evolved, and how the cuckoo has adapted to maintain this parasitic strategy, are intriguing questions.

Evolving Brood Parasitism
There are many cases of peculiar reproductive cycles in the cuckoo family, which indicate possible routes for the evolution of cuckoo parasitism. In 2 New World species; the Smooth-Billed Ani and the Guira cuckoo, breeding occurs in groups using a single nest. They occasionally parasitize the nest of a neighbouring group. In the case of the Coucals, an Old World species, males are responsible for nest building and for incubating and feeding the young. The female has several clutches a year, often with various males. The females produce more clutches if there is a glut of food, and if she cannot find enough males with nests she lays in the nests of other birds. The owners of these nests may be fooled into incubating the eggs. These behaviours may be similar to those of parasitic cuckoos ancestors, and act as a precursor for a purely parasitic lifestyle.

Populations of birds parasitized by cuckoos have generally evolved to reject foreign eggs, but those not parasitized, such as birds in Iceland, do not show this behaviour. Therefore making the step from laying in nests of other members of their own species, to laying in nests of another species, may have been relatively easy. Maintaining this parasitism after the host species had evolved egg rejection behaviour must have been the real challenge. It has led to an ongoing evolutionary battle, which has lasted for around 10 million years and given rise to some fascinating adaptations. 

Egg Mimicry

A crucial adaptation has been egg mimicry, whereby cuckoos lay eggs of similar colour and patterning to the eggs of their host species. There is great variation in the level of this defence, for example the dunnock represents one extreme, lacking any egg rejection behaviour. As there is no evolutionary pressure in this case for egg mimicry, the cuckoo eggs laid in dunnock nests have a radically different appearance to those of the dunnock. Cuckoos tend to most highly parasitize those species which show a high level of acceptance of foreign eggs.

A neuronal growth cone sets out on its journey

Spring 2012 Newsletter of the Faculty of Life Sciences (The University of Manchester)

I wanted to show my photo - “A neuronal growth cone sets out on its journey” - which is appearing on the cover of our Faculty of Life Sciences newsletter. It is of a nerve cell taken from a fruit fly (Drosophila melanogaster) embryo and grown on a glass cover slip for easy visualisation. The cell body is at the bottom, with an axon growing from it and ending in the growth cone (top). 

 Left: Precise wiring of the nervous system. Right: The 1901 network of submarine telegraph cables

Shaking hands with aliens

It is intriguing to consider the consequence that shaking hands with an alien could have, whether this was from a literal, E.T.-esque encounter, or perhaps more plausibly, from a metaphorical ‘handshake’, for example if we discovered alien microbes on mars and studied them in the laboritory back on earth. It is even more intriguing to imagine what such encounters could teach us about the fundamental principles of life. However could they also pose a risk to life on earth? I am not referring to a War of the Worlds style alien invasion, but for example could an extra terrestrial virus, inadvertently released, go on to parasitize our cells? Could such a life form even swap genes with our planet’s organisms, dramatically altering the course of evolution on earth?  These possibilities may be rather far fetched, but perhaps they are not entirely implausible.

The earth is home to an incredible diversity of life, perhaps 100 million species, broadly divisible into three domains; the Eukaryotes (everything from amoeba to blue whales), Bacteria, and Archaea (superficially similar to Bacteria but perhaps evolutionarily closer to Eukaryotes). In a sense, however, the earth only possesses one form of life. That is, all species seem to descend from a single common ancestor, and all share the same basic molecular machinery.

Amateur Biology

I want to talk about something that runs as a thread through our history, and is currently growing very strong, yet is often overlooked. It is the part that amateurs play in science – here I will focus on biology. I would argue that this phenomenon is of great value, the ripples of which spread beyond the immediate work done by amateurs, carrying an understanding of and engagement with science far beyond what professional scientists alone could achieve. This is important - science after all is an endeavour in which we are all stakeholders, we contribute to it with our taxes and ultimately its advances impact upon our lives.

Amateur science has come in many forms, from the fashion for amateur science amongst the Victorians, to the boom in so-called citizen science of the last few decades, fuelled and enabled by the internet. Many amateur science projects make use of the power that large numbers of enthusiastic volunteers can bring, to collectively achieve tasks that would be too time consuming for professionals alone. At the same time there are many amateur scientists with a great deal of experience in a particular area, sharing much of the specialist knowledge of professional scientists. Indeed some important biological advances were made by amateurs.

One great example is Gregor Mendel, considered the father of genetics. He was a monk, albeit one in a somewhat unusual monastery. It was headed by Cyrill Napp, who himself was involved in science, and at the time the monks’ duties included teaching mathematics at the Philosophical Institute of Brüun (now Brno) in Moravia.

Left: Gregor Mendel, Right: example crossing experiment

Mendel had attended the Philosophical Institute in Olomouc but could not afford to continue to University. It was this that led him to his life as a monk, however he did not take well too it, reportedly being too shy to deal with the parishioners. Abbot Napp had him sent to teach Greek and mathematics to children, which Mendel took too well, however he repeatedly failed the tests to become an accredited teacher, and eventually returned to the monastery. Here he was allowed to carry out experiments that turned at last to those using the garden pea, which would make Mendel famous. Abbot Napp even had a new greenhouse built for Mendel’s work.

Hen's teeth

From Chicken Run

What is wrong in this picture? Clearly it is the chickens' endearing Wallace style grins. No living bird possesses teeth and the youngest toothed fossil birds are the diving bird Hesperornis regalis and the flying bird Ichthyornis dispar which lived about 80 million years ago.

Left: Hesperornis regalis skeleton  and skull. Right: Ichthyornis dispar

In 1980 the (now late) evolutionary biologist Stephen Jay Gould published Hen's Teeth and Horse's Toes, a collection of essays which explores biological adaptations and their relevance to evolutionary theory. It includes one essay of the same name which discusses a phenomenon termed atavism – the reappearance of lost ancestral traits. One example given is that of the occasional appearance of additional horse toes, resembling those of the horse like creatures in the fossil record. The other part of the essay discusses an experiment which was very recent at the time, suggesting that hens could still possess the ability to form teeth.

Early stages of tooth development

During embryonic development, a tissue called the ectoderm forms which (among other things) gives rise to skin. In some places it contacts specific types of another tissue – the mesenchyme. Molecular signals pass between the two tissues which induce the ectoderm to grow into a specific structure dependent on the type of mesenchyme. In this manner, molar mesenchyme induces the ectoderm to develop into a tooth.

In the experiment discussed by Gould, tooth mesenchyme from a mouse and ectoderm from a chick were removed and grown together. Neither of these alone can form teeth, but when combined, tooth like structures were formed. This suggested that during the evolution of birds the inductive signal from the mesenchyme was lost in one way or another, but that the developmental programme for tooth formation remained, in an inactive state. This experiment has remained controversial ever since. Could, for example, the mouse mesenchyme been contaminated with mouse ectoderm, and the chick ectoderm played no part in the tooth formation observed? We will never know for sure, but thankfully biological science has progressed rapidly in the last few decades, shedding light on the issue of hen’s teeth.

A type of cells called the neural crest migrate through the developing embryo and contribute to the development of many structures, with a subset forming the tooth mesenchyme. In one experiment neural crest cells from mice were used to replace those of chicks, which then continued to develop. These cells migrated into the chicks jaw and tooth precursor structures formed. In this case contamination with mouse ectoderm is unlikely to be a problem, as the neural crest cells were allowed to migrate along their specific route, and other cell types would be unlikely to do this.

In another study researches showed that a number of molecules involved in tooth development are not switched on in the developing chick jaw. Artificially adding one of these - a signalling molecule named BMP4 - again set in motion the formation of teeth precursors. This is strong support for the notion that what is missing in birds are the initial molecular signals to induce tooth formation.

More recently it was found that chicks with two copies of a mutation named talpid² grew tooth precursors. The mutation causes the chicks to die before they have even hatched, but thankfully they reach a stage where the precursor teeth have appeared.

Chick beaks, with talpid² mutant on right

This finding is intriguing, as in this case nothing new has been introduced into the chick. The gene effected by this mutation, and the molecular basis of the reactivated tooth development are not yet known, but it is likely that the mutation results in the inactivation of a gene. A number of explanations could explain this finding, for example a gene could act to suppress initiation of tooth development in birds, and this gene could be lost in talpid² mutants. Alternatively the effect could be indirect, for example in birds the potential tooth mesenchyme may exist, but never makes contact with the ectoderm. In this case could talpid² cause tissue rearrangements, bringing them back into contact? This study raised the possibility that birds could re-evolve teeth.

Unfortunately evidence now suggests that this is an impossibility. If the tooth precursors described in the chick experiments were to develop further they would lay down a rigid core of dentin, coated with hard enamel. By searching in the chicken genome for four genes involved in dentin and enamel production, scientists demonstrated that all four were either absent, or had gained mutations which would render them useless. Of course the very presence of corrupted tooth specific genes is further evidence of evolution of birds from a toothed ancestor.

Bird’s inability to regain teeth is consistent with Dollo’s law of irreversibility, proposed in 1893. This is the ideas that evolution is a strictly one way process, and so once lost a structure cannot be regained in its original form. We now know that genes acquire mutations over time, and that any gene no longer used by an organism will rapidly gain mutations that are not selected against, rendering it useless. In light of this, the ability of birds to even grow tooth precursors seems surprising. The reason may be that many genes involved in early tooth formation are, for example, signalling molecules involved in the development of many other structures, which have therefore been well preserved. This exposes a loophole in Dollo’s law.

So a recent study has shown that the frog Gastrotheca guentheri has regained functional teeth on their lower jaw after more than 200 million years of absence. This is made possible by the retention in frogs, of upper jaw teeth. All of the genes involved in tooth formation have therefore been well preserved, allowing lower jaw teeth to be reacquired. Birds may never regain functional teeth, but then we do not expect the atavistic legs occasionally found in whales to ever allow them to walk out of the sea. That is not really why these phenomena are of such interest.

In 1856, two years after On the Origin of Species was published, the first Archaeopteryx fossil was discovered. This toothed fossil appeared to be a dinosaur in many respects, yet the impressions left by feathers were clear. In 1880 Darwin described the newly discovered Hesperornis and Ichthyornis fossils as “the best support for the theory of evolution”. These much younger fossils were essentially modern birds, yet still retained teeth. So they added huge support, specifically for the evolution of birds from toothed dinosaurs, but also generally for what Darwin termed “descent with modification” which lies at the heart of the concept of evolution.

Archaeopteryx Lithographica

So in 1980, Gould jumped on this evidence that tooth formation ability had not been entirely erased during 80 million years of bird evolution. Further insights have confirmed this finding, and it provides one of many strands of evidence linking birds back through close relatives of Ichthyornis and Archaeopteryx to dinosaurs.

Selected links:

Ed Yong article – Return of the supersoldier ants
Bird evolution

Vestigial structures and atavisms