Evolutionary arms race turns ants into babysitters for Alcon blue butterflies

Blogging on Peer-Reviewed ResearchIn the meadows of Europe, colonies of industrious team-workers are being manipulated by a master slacker. The layabout in question is the Alcon blue butterfly (Maculinea alcon) a large and beautiful summer visitor and its victims are two species of red ants, Myrmica rubra and Myrmica ruginodis.

Myrmica rubra and an Alcon blue butterfly caterpillarThe Alcon blue is a ‘brood parasite’ – the insect world’s equivalent of the cuckoo. David Nash and European colleagues found that its caterpillars are coated in chemicals that smell very similar to those used by the two species it uses as hosts. To ants, these chemicals are badges of identity and so similar are the caterpillars that the ants adopt them and raise them as their own. The more exacting the caterpillar’s chemicals, the higher its chances of being adopted.

The alien larvae are bad news for the colony, for the ants fawn over them at the expense of their own young, which risk starvation. If a small nest takes in even a few caterpillars, it has more than a 50% chance of having no brood of its own. That puts pressure on the ants to fight back and Nash realised that the two species provide a marvellous case study for studying evolutionary arms races (which I’ve blogged about before here).

Theory predicts that if the parasites are common enough, they should be caught in an ongoing battle with their host, evolving to become more sophisticated mimics, while the ants evolve to become more discriminating carers. The two species make a particularly good model for this because their geographical ranges overlap in a fractured mosaic.

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Mud time capsules show evolutionary arms race between host and parasite

Blogging on Peer-Reviewed ResearchEvolution can sometimes be seen as a futile contest. Throughout the natural world, pairs of species are locked in an evolutionary arms race where both competitors must continuously evolve new adaptations just to avoid ceding ground. Any advantage is temporary as every adaptive move from a predator or parasite is quickly neutralised by a counter-move from its prey or host. Coerced onward by the indifferent force of natural selection, neither side can withdraw from the stalemate.

Mud time capsules show evolutionary arms race between host and parasiteThese patterns of evolution are known as Red Queen dynamics, after the character in Lewis Carroll’s Through the Looking Glass who said to Alice, “It takes all the running you can do, to keep in the same place.”

These arms races are predicted by evolutionary theory, not least as an explanation for sex. By shuffling genes from a mother and father, sex acts as a crucible for genetic diversity, providing a species with the raw material for adapting to its parasites and keep up with the arms race.

Watching the race

We can see the results of Red Queen dynamics in the bodies, genes and behaviours of the species around us but actually watching them at work is another matter altogether. You’d need to study interacting species over several generations and most biologists have neither the patience nor lifespan to do so.

But sometimes, players from generations past leave behind records of the moves they made. Ellen Decaestecker and colleagues from Leuven University found just such an archive in the mud of a Belgian lake.

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Is a virus responsible for the disappearing bees?

A group of scientists have found that a virus – IAPV – may be responsible for Colony Collapse Disorder, the mysterious condition that’s emptying the hives of European and American beekeepers.

A bee sits on a readout of its own genetic material.In 2006, American and European beekeepers started noticing a strange and worrying trend – their bees were disappearing. Their hives, usually abuzz with activity, were emptying.

Like honeycombed Mary Celestes, there was no trace of the workers or their corpses either in or around the ghost hives, which still contained larvae and plentiful stores of food. It seemed that entire colonies of bees had apparently chosen not to be.

The cause of the aptly named ‘Colony Collapse Disorder’, or CCD, has been hotly debated over the last year. Fingers were pointed at a myriad of suspects including vampiric mites, pesticides, electromagnetic radiation, GM crops, climate change and poor beekeeping practices. And as usual, some people denied that there was a problem at all.

But a large team of US scientists led by Diana Cox-Foster and Ian Lipkin have used modern genomics to reveal the main villain in this entomological whodunnit – a virus called Israeli Acute Paralysis Virus or IAPV.

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Foul-tasting ant parasitises the colonies of other species

An ant nest is sheltered, well defended and stocked with food, but one that takes time to build and protect. Which is why some species of ants don’t bother to do it themselves – they just squat in the nests of others.

These ants are ‘social parasites’ – they don’t feed off their hosts’ tissues, but instead steal their food, sleep in their homes and use their resources. They’re like six-legged cuckoos

Formicoxenus nitidulus escapes its hosts’ larger jaws by tasting foul.An ant colony is too dangerous a target to victimise lightly and the social parasites use several tricks to stop their hosts from ripping them apart. Some escape reprisal by chemically camouflaging themselves, either by mimicking their hosts’ odour, or by acquiring it through contact.

This specialised strategy ties the parasite’s fates into those of its host. Both are caught in an evolutionary arms race, with the hosts becoming more discriminating and the parasites’ deception becoming more accurate. But Stephen Martin from the University of Sheffield has found one ant species with a completely different and more flexible strategy – it tastes really, really bad.

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An entire bacterial genome discovered inside that of a fruit fly

Bacteria have the ability to transfer genes to one another. Now, scientists have found that one species, Wolbachia, has managed to transfer its entire genome into that of a fruit fly. These extreme gene transfers could be more common than we thought, and they have important consequences for genome-sequencing projects.

Wolbachia in yellow infecting insect cells in red.A humble species of fruit fly is the genetic equivalent of a Russian doll – peer inside its DNA and you will see the entire genome of a species of bacteria hidden within.

The bacteria in question is Wolbachia, the most successful parasite on earth and infects about 20% of the world’s species of insects. It’s a poster child for selfishness. To further its own dynasty, it has evolved a series of remarkable techniques for ensuring that it gets passed on from host to host. Sometimes it gives infected individuals the ability to reproduce asexually; at other times, it does away with an entire gender.

Now, Julie Dunning-Hotopp from the J. Craig Venter Institute and Michael Clark from the University of Rochester have found an even more drastic strategy used by Wolbachia to preserve its own immortality – inserting its entire genome wholesale into that of another living thing. Continue reading

Butterflies evolve resistance to male-killing bacteria in record time

Six years ago, the males of a Samoan butterfly were being killed off by a bacteria and made up only 1% of the population. Now, the males have returned in a dramatic comeback and the sex ratio is equal again. In just ten generations, they evolved resistance to the parasite, a powerful example of natural selection in action.

Males of the blue moon butterfly has staged an amazing comeback.In our world, there is (roughly) one man for every woman. Despite various social differences, our gender ratio remains steadfastly equal, so much so that we tend to take it for granted. Elsewhere in the nature, things are not quite so balanced.

Take the blue moon butterfly (Hypolimnas bolina). In 2001, Emily Dyson and Greg Hurst were studying this stunningly beautiful insect on the Samoan islands of Savaii and Upolu when they noticed something strange – almost all the butterflies were females. In fact, the vastly outnumbered males only made up 1% of the population.

Male-killers

The cause of this female-dominated world was an infection, an inherited bacterium called Wolbachia. Wolbachia is a strong candidate for the planet’s most successful parasite for it infects a huge proportions of the world’s arthropods, themselves a highly successful group. And it does not like males.

Wolbachia has an easy route of infection – it can be passed to the next generation through the eggs of an infected female. But it can’t get into sperm, and for that reason, male insects are useless to it and it has a number of strategies for dealing with them.

Sometimes, it allows females to reproduce without male fertilisation. At other times, it forces males to undergo sex changes to become females. But in cases like the blue moon butterfly, it simply kills the males outright before they’ve even hatched from their eggs.

In 2001, Dyson and Hurst noted that the islands with the fewest males were the ones with the most prevalent Wolbachia infections.

The butterflies fight back

Female blue moon butterflies dominated Samoa until recently, thanks to Wolbachia infectionsBut by 2005, things had changed. Sylvain Charlat from University College London, along with Hurst and others, found that males were increasing in number all around Upolu Island. A year later, a formal survey confirmed the males’ amazing comeback.

On Upolu, they equalled in the females in number. Within just 10 generations, the male butterflies had gone from being outnumbered a hundred to one to an equal footing with the females. “To my knowledge, this is the fastest evolutionary change that has ever been observed,” said Charlat.

Charlat found the same story at a site on Savaii Island close to neighbouring Upolu. On the other side of the island, the males were still in the minority and many failed to hatch. But at 7% of the population, they were doing better than they had done in five years before.

All the butterflies were still infected with the same Wolbachia strain that had slaughtered their males just a few years back. And the bacteria themselves had not changed – when Charlat mated infected females with uninfected males from a different island, the parasite’s male-killing nature resurfaced within a few generations.

Evolution in action

Charlat believes that the Upolu butterflies had gained a resistance gene (or several) that allowed them to shrug off the male-killing bacteria. It either evolves the trait itself, or gained it from South-east Asian populations that had already become resistant.

Whatever the origin, the mutation spread like genetic wildfire across the Upolu and onto neighbouring Savaii. Most mutations carry small benefits and spread slowly. But by levelling a populations sex ratio, a mutation that resists Wolbachia clearly provides a huge advantage.

Male blue moon butterflies have evolved resistance to Wolbachia in record time.Surviving males who carry the gene(s) would have had their pick of females, since most of their competition lay dead in their eggs. And females, that picked up the mutation would have had twice the number of surviving young.

Arms race

Charlat’s work highlights just how powerful an influence parasites have in the course of evolution. Just how powerful parasites can be in the course of evolution. Events like this may be very commonplace, but at such speed, they may have happened before researchers could spot them.

The butterflies’ newfound resistance is also marvellous example of the Red Queen hypothesis, where parasites and hosts are caught in an evolutionary arms race. Each is forced to acquire new adaptations and counter-adaptations just to stay in the same place.

In this particular arms race, the butterflies have won the battle against Wolbachia. But the war isn’t over. The parasite now faces renewed pressures to find innovative ways of doing away with the dead-end males. How long will it be before it evolves a retaliatory strike?

More on evolution in action:
Natural selection does a handbrake turn – quick evolution at work
Of flowers and pollinators – a case study in punctuated evolution

More on parasites and evolutionary arms races:
Parasites can change the balance of entire communities
Viruses evolve to be more infectious in a well-connected population
Beetle and yeast vs. bee – how American bees are losing the evolutionary arms race

More on animal sex and reproduction:
Virgin birth by Komodo dragons
When the heat is on, male dragons become females
Chimerism, or How a marmoset’s sperm is really his brother’s
Aphids get superpowers through sex

 

Reference: Charlat, Hornett, Fullard, Davies, Roderick, Wedell & Hurst. 2007. Extraordinary flux in sex ratio. Science 317: 214.

 

 

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Photos by Sylvain Charlat and Comacontrol

Parasites can change the balance of entire communities

By changing the behaviour of their hosts, parasites can change the face of entire habitats. Now, scientists have demonstrated how a tiny flatworm can alter the structure of a tidal habitat by infecting small marine snails.

Conspiracy theories, TV thrillers and airport novels are full of the idea that the world is secretly run by a hidden society. We have come up with many names for this shadowy cabal of puppet-masters – the Illuminati, the Freemasons, and more. But a better name would be ‘parasites’.

The fluke Cryptocytole lingua affects the entire tidal habitat by infecting snails.Every animal and plant is afflicted by parasites. The vast majority are simple, degenerate creatures, small in size and limited in intelligence. They affect our health and development, and even our behaviour and culture. And by pulling the strings of key species, parasites can change the face of entire habitats.

In a typical school textbook, an ecosystem consists of plants that feed plant-eaters, who in turn, line the bowels of predators. But parasites influence all of these levels, and as such, they can change the structures of entire communities.

The idea that nature is secretly manipulated by these tiny, brainless creatures is unsettling but manipulate us, they do.

Chelsea Wood and colleagues from Dartmouth College found compelling evidence for the influence of parasites by studying small animals that live on the coasts of the North Atlantic.

Snails and flukes

These tidal boundaries are home to the common periwinkle (Littorina littorea; below), a type of marine snail. It invaded America’s shores about two centuries ago and has spread successfully along the eastern seaboard. It acts as this habitat’s equivalent of cattle, grazing the ephemeral algae that grows in rocky tidal pools.

But they are not alone. The periwinkles are unwitting passengers for the parasitic fluke Cryptocytole lingua (above), a kind of flatworm. In most parts of the coast, the flukes are relatively rare, but in some parts of New England where seabirds are plentiful as many as 90% of periwinkles can be infected.The common periwinkle, crowded on a rock. Many will be infected by flukes.

Like most parasites, the fluke has an amazingly complicated life cycle. Snails become infected by accidentally eating eggs spread in the droppings of seabirds. The larvae develop in their bodies by eating the snails inside out. They eventually give rise to a free-swimming creature that finds and infects fish, which are then eaten by seabirds, completing the cycle.

Infected snails lose their appetites

By devouring the snails’ internal organs, the flukes wreck their hosts’ digestive and reproductive systems. Wood reasoned that the neutered and malnourished snails must be have altered feeding habits and tested this idea in the lab and the field.

She found that the flukes put infected snails on an involuntary diet, and they ate far less algae than uninfected ones. While many parasites can directly alter their hosts’ behaviour, Wood believes that nixing the periwinkles’ appetities is not part of Cryptocytole’s plan.

It’s just an incidental side effect of infection and happens because the snails’ crippled digestive glands could not cope with the normal amount of food. And because the parasites trashed their reproductive systems and several other organs, they needed less energy to begin with.

Even so, by reducing the snails’ feeding, the parasites could potentially affect the entire tidal community. Wood demonstrated this by setting up cages in the tidal zone containing uninfected snails or infected ones. Sure enough, after a month or so, cages that housed infected snails had about 60% more algae than those with uninfected ones.

In the long-term, these effects are likely to be even larger as the fluke castrates its unfortunate hosts and lowers their life expectancy. Over time, this would reduce the size of the whole snail population and give the algae an even greater chance to grow.

Ripple effects

Periwinkles grazing on algae - they are less hungry if infected by Cryptocotyle.These snails’ lost appetites ripple out through the entire habitat. Infected snails mean more algae, which provide more food for other invertebrates. The algae also crowd out the rocky real estate that barnacles attach themselves too, and the loss of barnacles reduces the numbers of blue mussels that coexist with them.

Even though it never comes into contact with these other tidal players, the fluke indirectly influences all of them. Nestled within the body of a snail, it pulls the strings of the entire ecosystem.

This is one of the few instances where the effects of parasites on ecosystems have been carefully documented. Millions of similar dramas must play out all over the world, for half of the planet’s species are parasitic. It’s not our world, it’s theirs.

Find out more: Carl Zimmer’s superb book Parasite Rex is an amazing journey through the world of parasites, how they affect other animals, and how they change entire habitats.

Reference: Wood, Byers, Cottingham, Altman, Donahue & Blakeslee. 2007. Parasites alter community structure. PNAS 104: 9335-9339.

Images: by Chelsea Wood and James Byers

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