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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Ground squirrels use infrared signals to fool heat-seeking rattlesnakes

Rattlesnakes can track their prey using the infrared light given off by the warm bodies. But ground squirrels can use this super sense against the snakes. By pumping blood into their tails, they give off infrared signals that fool the snakes’ heat-seekers.

Ground squirrels use infrared signals to fool rattlesnakesIt seems like an uneven match. In one corner, the unassuming California ground squirrel (Spermophilus beechyi), 30cm in length. In the other, the northern Pacific rattlesnake (Crotalus oreganos), more than twice the length of the squirrel, and armed with hinged fangs that pack a lethal venom. But thanks to a cunning adaptation, the squirrel often gets an unexpected upper hand in this bout.

Squirrels vs snakes

Ground squirrels live in a series of burrows that keep them out of reach of most predators. Snakes, however, have exactly the right body plan for infiltrating long sinuous tunnels, and it’s not surprising that they are the squirrels’ major predators. It’s equally unsurprising that the squirrels have developed ways of defending themselves against snakes.

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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

Of flowers and pollinators – a case study in punctuated evolution

Darwin predicted that flowers and pollinators are engaged in an evolutionary arms race. But that’s not always the case. In a group called columbines, evolution happened in a stop-start ‘punctuated’ way, as the flowers encountered new pollinators with increasingly long tongues.

Charles Darwin was a visionary in more ways than one. In 1862, Darwin was studying a Malagasy orchid called Angraecum sesquipedale, whose nectar stores lie inaccessibly at the bottom of a 30cm long spur (tube). Darwin predicted that the flower was pollinated by a moth with tongue long enough to raid the spur.

Darwin’s moth, perfectly adapted to drink from a long-spurred orchid.Few people believed him, but in 1903, zoologists discovered Darwin’s predicted moth, Xanthopan morgani praedicta, and it did indeed have a very long tongue. Darwin’s accurately predicted the extraordinary but matching lengths of moth tongue and orchid spur, but his explanation for them is another story.

The arms race model

He suggested that the two species were locked in an ‘evolutionary arms race’. Orchids and pollinators gradually co-evolved over time, lengthening both tongues and spurs in response to each other.

Orchids with the longest spurs have an advantage. Their nectar stores are only just within reach of pollinators, so they are tempting but don’t sacrifice too much valuable nectar. For pollinators, the advantage belongs to those with the longest tongues because they have access to the most food.

The arms race model has become widespread and popular since Darwin’s time. It helps to explain relationships between predators and prey, parasites and hosts and even males and females. But its original function – to explain the relationship between flowers and pollinators – has just been called into question.

Columbines

Justen Whittall and Scott Hodges from the University of California, Santa Barbara, tested the arms race theory by looking at another long-spurred flowering plants – the columbines (Aquilegia sp). In these flowers, every petal carries its own elongated nectar spur and the advent of these spurs coincided with the recent and rapid diversification of this group.

Columbines of North America have a great range of spur sizesWhittall and Hodges charted the evolutionary relationships between the 25 North American columbine species, whose spurs range form barely a centimetre in length, to just over twelve. They found that this great variety of lengths was driven by changes in pollinators, rather than gradual races against a single one.

The flowers with the shortest spurs were pollinated by short-tongued bumblebees. Hummingbirds, whose tongues are longer, pollinate columbines with longer spurs, while hawk-moths, with the longest tongues of all, carry the pollen of the longest-spurred flowers.

There is no overlap between these three groups and once a lineage switches pollinator it doesn’t go back. Over the course of their evolution, the columbine lineages went from bumblebees to hummingbirds, and then to hawkmoths, lengthening their spurs with every jump.

The ‘pollinator shift’ model

Based on these observations, Whittall and Hodges put forward an alternative to Darwin’s arms race model. They imagined a columbine ancestor that was well adapted to the tongue length of a specific pollinator (say, a bumblebee).

In part of its range, the flower started to be visited by a second pollinator (say, a hummingbird) with a much longer tongue. In this area, the plant rapidly evolved a longer spur in response to its new partner and over time, this led to two species with different spur lengths and different pollinators.

In this model, the columbines’ spurs evolved in a ‘punctuated’ stop-start way, very different to Darwin’s model of gradual change. Each pollinator shift triggered a large evolutionary rush, as the species lengthened their spurs in response to the longer tongues of their new partners. In between these shifts, the pace of evolution slowed down considerably.

A columbine flower - its long spurs are driven by evolutionary shifts between pollinatorsBut Darwin’s arms race idea isn’t out for the count yet. Whittall points out that columbines that are pollinated by hawkmoths have a great variety of spur lengths themselves that were most likely the result of an arms race. And the moths themselves evolved long before the columbines did, so the variations in their tongue lengths must have evolved in relationships with other plants.

An adaptive valley

The stop-start model also explains a difference between columbines around the world. Those in Europe and Asia have a much smaller range of spur lengths than their North American cousins, and none of them are pollinated by hawkmoths. Whittall and Hodges have an answer for this too – it’s because Eurasia has no hummingbirds.

Imagine if flowers tried to make the evolutionary leap from bumblebee to hawkmoth without the intermediate stepping stone of hummingbirds. At the intermediate spur length, the flower would have excluded its old pollinator, whose tongues would now be too short to reach any nectar. But it would have no advantage over its new pollinator, whose amply long tongues could drink the flowers dry.

Between bumblebee and hawkmoth lies an ‘adaptive valley’, where intermediate-length flowers have no advantage and are ignored by natural selection. In Eurasia, there is not enough impetus for a species to cross it. But North America, the hummingbirds act as a stepping stone that allowed the columbines to ford this gap and evolve even more extreme flowers.

Reference: Whittall & Hodges. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447: 706-709.

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Images: Moth from MSN Encarta, columbine montage from Justen Whittall’s website.

Related stories about evolution:
Natural selection does a handbrake turn – quick evolution at work
Salamander robot walks, swims and sheds light on evolutionary step from sea to land
Human cone cell lets mice see in new colours
Living optic fibres bypass the retina’s back-to-front structure
Viruses evolve to be more infectious in a well-connected population
The evolution of animal personalities – they’re a fact of life

Orang-utan study suggests that upright walking may have started in the trees

A common theory of human evolution says that after our ancestors descended from the trees, they went form walking on four legs to two. But a new study in orang-utans could overturn that theory, by suggesting that our ancestors evolved a bipedal walk while they were still in the trees.

Did and upright posture evolve in a tree-dwelling ancestor?Walking on two legs, or bipedalism, immediately sets us apart form other apes. It frees our arms for using tools and weapons and is a key part of our evolutionary success. Scientists have put forward a few theories to explain how our upright gait evolved, but the ‘savannah theory’ is by far the most prolific.

It’s nicely illustrated by this misleading image that has become a mainstay of popular culture. It suggests that our ancestors went from four legs to two via the four-legged knuckle-walking gait of gorillas and chimps. Dwindling forests eventually pushed them from knuckle-walking to a full upright posture. This stance is more efficient over long distances and allowed our ancestors to travel across open savannahs.

But this theory fails in the light of new fossils which push back the first appearance of bipedalism to a time before the forests thinned, and even before our ancestors split from those of chimpanzees. Very early hominins, including Lucy (Australopithecus afarensis) and Millennium Man (Orrorin) certainly ambled along on two legs, but they did so through woodland not plains.

Our arms provide a further clue. Even though our ancestors’ back legs quickly picked up adaptations for bipedalism, they steadfastly kept long, grasping arms, an adaptation more suited to moving through branches. To Susannah Thorpe at the University of Birmingham, these are signs that bipedalism evolved while our ancestors were still living in trees.

Two legs good, four legs bad?

Orang-utans can go bipedal and our ancestors may well have done the same in the trees.But there is a snag – an adaptation must provide some sort of benefit. And, as many children painfully discover, it is hard to imagine how walking on two legs could benefit sometime in a tree.

But Thorpe has an answer to this too. She spent a year in the Sumatran jungle, studying the orang-utan – the only great ape to spend the majority of its life in the trees.

She carefully documented over 3,000 sightings of wild orang-utans moving through the treetops. On large sturdy branches, they walk on all fours (below right), and on medium-sized ones, they start to use their arms to support their weight.

But on the thinnest and most unstable branches, the apes use a posture that Thorpe calls ‘assisted bipedalism’ (below left). They grip multiple branches with their long, prehensile toes and use their arms to balance and transfer their weight. And unlike chimps which bend their knees while standing up, bipedal orang-utans keep their legs straight, just like humans do.

An orang-utan used both two-legged and four-legged postures.

It’s a win-win posture – the hands provide extra safety, while the two-legged stance frees at least one hand to grab food or extra support. With it, the apes can venture onto the furthest and thinnest branches, which provides them with several advantages.

As Thorpe says, “Bipedalism is used to navigate the smallest branches where the tastiest fruits are, and also to reach further to help cross gaps between trees.” That saves them energy because they don’t have to circle around any gaps, and it saves their lives because they don’t have to descend to the ground. “The Sumatran tiger is down there licking its lips”, she said.

A new view of ape & human evolution

With these strong adaptive benefits, it becomes reasonable to suggest that bipedalism evolved among the branches. Based on this theory, Thorpe, along with Roger Holder and Robin Crompton from the University of Liverpool, have painted an intriguing new picture of ape evolution.

It begins in the same way as many others – with the rainforests of the Miocene epoch (24 to 5 million years ago) becoming increasingly patchy. For tree-dwelling apes, the gaps in the canopy started becoming too big to cross. But in Thorpe’s view, these ancestral apes were already using a bipedal stance, and different groups took it in separate directions.

Our ancestors were bipedal long before they came down from the trees.The ancestors of orang-utans remained in the increasingly fragmented canopy and became specialised and restricted there. The ancestors of chimps and those of gorillas specialised in climbing up and down trees to make use of food both in the canopy and on the ground. The postures used in vertical climbing are actually very similar to those used in four-legged knuckle-walking and this became their walk of choice on the ground.

The ancestors of humans abandoned the trees altogether. They used the bipedal stance that served them well on thin branches to exploit the potential of the stable land environment. Over time, they brought in further adaptations for efficient walking, culminating in the human walking style that we now neglect by sitting at a computer all day.

Thorpe’s reconstruction is delightfully non-human-centric. It suggests that in the evolution of movement, we were conservatives who relied on a walk that had been around for millions of years. Chimps and gorillas with their fancy new knuckle-dragging gait were the true innovators.

Reference: Thorpe, Holder & Crompton. 2007. Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316: 1328-1331.

Image: Black and white image from Science magazine.

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Related stuff:
On ape and human evolution:
Chimps show that actions spoke louder than words in language evolution
Hidden ‘junk’ gene separates human brains from chimpanzees
Chimps have more adaptive genetic changes than humans

On the evolution of movement:
Salamander robot walks, swims and sheds light on evolutionary step from sea to land
Microraptor – the dinosaur that flew like a biplane

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Beetle and yeast vs. bee – how American bees are losing the evolutionary arms race

In America, the parasitic small hive beetle has gained the upper hand in its evolutionary arms race against the honeybee. It has formed an alliance with a type of yeast, and together, they use the bees’ own chemical communications against them.

Bees release alarm pheromones that draw small hive beetles towards the hive.Bee hives, with their regularly arranged honeycombs and permanently busy workers may seem like the picture of order. But look closer, and hives are often abuzz with secret codes, eavesdropping spies and deadly alliances.

African honeybees are victimised by the parasitic small hive beetle. The beetles move through beehives eating combs, stealing honey and generally making a mess. But at worst, they are a minor pest, for the bees have a way of dealing with them.

They imprison the intruders in the bowels of the hive and carefully remove any eggs they find. In turn, the beetle sometimes fools the bees by acting like one of their own grubs, and gets a free meal instead of imprisonment. In Africa, both species have found themselves in an evolutionary stalemate.

But in 1998, American beekeepers spotted the beetle in hives of their local European-descended honeybees. These insects are gentler versions of their aggressive African relatives, and in them, the beetles found more vulnerable victims.

In the last decade, they have spread through hives on the East Coast, causing much more destruction than they normally get away with. In some cases, the damage is so severe that the bees are forced to abandon their hive. As the bees suffer, so do the economically vital crops they pollinate.

The small hive beetle detects bee alarm pheromones and brings a yeast into the hive.Now, scientists from the International Centre of Insect Physiology and Ecology and the University of Florida have uncovered the secrets behind the beetle’s destructive ability.

Small hive beetles (right) hunt down beehives by hijacking their communications. When bees are stressed or confronted by threats, they release alarm pheromones into the air to alert their hive-mates of impending danger. But the beetles can also detect these chemical signals and use the bees’ own early warning system to locate their hives.

Baldwyn Tonto and colleagues found that the beetles are sensitive to much lower levels of these pheromones than the bees themselves are, and can detect a much wider ranger of airborne chemicals from the hive. With their superior senses, the beetles can home in on beehives before the bees themselves can sense the alarm.

But that’s not the whole story. Tonto found that honeycombs infested by beetles, but free of worker bees, were emitting a strange smell. It mimicked the bees’ alarm pheromones and strongly attracted even more beetles. But it wasn’t coming from the parasites themselves.

Instead, the source of the smell was a type of yeast that hitches a ride with small hive beetles into the bees’ home. Tonto found that the fungus was fermenting the pollen collected by the bees, and releasing chemicals that closely mimic the beetle-attracting alarm pheromones.

Domesticated European honeybees have been bred into helplessness against the small hive beetle.The beetles’ keen sensitivity to the bees’ chemical messages allows them to initially home in on a hive. As they arrive, they bring the yeast along for the ride and distribute it among the hive’s pollen stores. The yeast ferments the pollen and releases chemicals that mimics the bee’s alarm pheromone, attracting even more beetles .

Soon, the infection reaches critical mass, and the bees are forced to abandon their homes. They leave behind a sizeable store of pollen and honey, ideal breeding grounds for the unwitting partnership of yeast and beetle.

But the yeast also exists in Africa, where it is similarly spread to hives by hive beetles. Why does the alliance not wreak such havoc there? Tonto believes that domestication is the answer. Because of years of selective breeding, the European honeybee is a slightly dopier version of the African bee – more docile and less prone to swarming.

It faces a larger number of pests and problems that prevent it from concentrating on imprisoning invading beetles. And its poor sensitivity to its own alarm chemicals allows the beetle-yeast alliance to gain a strong foothold before the bees recognise the threat.

With bee populations mysteriously dying off across America, the threat of the small hive beetle and its fungal partner may be even more pressing than before.

 

Reference: Torto, Boucias, Arbogast, Tumlinson & Teal. 2007. Multitrophic interaction facilitates parasite-host relationship between an invasive beetle and the honey bee. PNAS 104: 8374-8378.

Image: Photo of small hive beetle by Jeffrey Lotz

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Related stories about parasites and symbiosis:
Aphids get superpowers through sex
Hatena: when two cells are better than one
Too few genes to survive – a bacteria with the world’s smallest genome
Parasites can change the balance of entire communities

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