Category: Evolutionary arms races

Museum butterfly collections chronicle evolutionary war against male-killers

By Ed Yong | September 10, 2009 12:00 pm

The drawers of the world’s museums are full of pinned, preserved and catalogued insects. These collections are more than just graveyards – they are a record of evolutionary battles waged between animals and their parasites. Today, these long-dead specimens act as “silent witnesses of evolutionary change”, willing to tell their story to any biologist who knows the right question to ask.

This time round, the biologist was Emily Hornett, currently at UCL, and her question was “How have the ratios of male butterflies to female ones changed over time?” You would think that the sex ratios of insects to mirror the one-to-one proportions expected of humans but not if parasites get involved.

The bacterium Wolbachia is arguably the world’s most successful parasite, infecting around 20% of all insects, themselves an extraordinarily successful group. It can infect eggs but not sperm, which means that females can pass the bacteria on to their offspring, but males cannot. As a result, Wolbachia has it in for males – they are evolutionary dead-ends, and the bacterium has many strategies for getting rid of them. It can kill them outright, it can turn them into females and it can prevent them from mating with uninfected females.  As a result, populations infected with Wolbachia can be virtually male-free.

To study the effect of Wolbachia on butterfly populations, Hornett (great name for an entomologist)turned to collections of the blue moon butterfly (Hypolimnas bolina). This beautiful species was heavily collected by entomologists between 1870 and 1930 and their efforts have stocked the museums of the world with specimens. While these were long dead, Hornett found that many of them contained viable DNA and she used them to develop a genetic test for Wolbachia infections.

She validated her Wolbachia test by using butterflies collected by the entomologist H.W.Simmons in Fiji over 70 years ago. Simmons carefully recorded the numbers of males and females in his butterflies and noted some very unusual all-female brood. Sure enough, Hornett confirmed that only mothers who tested positive for Wolbachia produced these skewed clutches, while those that were infection-free gave birth to the standard bisexual broods.

Satisfied that her test was accurate, Hornett cast her net further. She looked at specimens collected from five populations of blue moon butterflies collected from the Phillippines, Borneo, Tahiti, Fiji and Samoa between 73 and 123 years ago. The butterflies are well studied to this day, so Hornett could compare the proportion of Wolbachia infections then and now. In butterfly time, this represents a gap of 500 to 1000 generations separating the specimens from their modern descendants.

The results show that the butterfly and the bacterium have been engaging in a heated evolutionary battle throughout the Pacific. The male-killer’s dominance has fluctuated greatly, rising in some areas and falling in others, while the butterfly has repeatedly evolved to resist its sex-skewing antics. 

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Virus and bacteria team up to save aphid from parasitic wasp

By Ed Yong | August 21, 2009 10:00 am

Viruses and bacteria often act as parasites, infecting a host, reproducing at its expense and causing disease and death. But not always – sometimes, their infections are positively beneficial and on rare occasions, they can actually defend their hosts from parasitism rather than playing the role themselves.

In the body of one species of aphid, a bacterium and a virus have formed a unlikely partnership to defend their host from a lethal wasp called Aphidius ervi. The wasp turns aphids into living larders for its larvae, laying eggs inside unfortunate animals that are eventually eaten from the inside out. But the pea aphid (Acyrthosiphon pisum) has a defence – some individuals are infected by guardian bacteria (Hamiltonella defensa) that save their host by somehow killing the developing wasp larvae.

H.defensa can be passed down from mother to daughter or even sexually transmitted. Infection rates go up dramatically when aphids are threatened by parasitic wasps. But not all strains are the same; some provide substantially more protection than others and Kerry Oliver from the University of Georgia has found out why.

H.defensa‘s is only defensive when it itself is infected by a virus – a bacteriophage called APSE (or “A.pisum secondary endosymbiont” in full). APSE produces toxins that are suspected to target the tissues of animals, such as those of invading wasp grubs. The phage infects the bacteria, which in turn infect the aphids – it’s this initial step that protects against the wasps.  

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One jump from chimps to humans – the origin of malaria

By Ed Yong | August 3, 2009 5:00 pm

Blogging on Peer-Reviewed ResearchSwine flu has made the world all too aware of the possibility of diseases making the leap from animal hosts to human ones. Now, we know that another disease made a similar transition from chimpanzees to humans, several thousand years ago. This particular infection is caused by a parasite, and a very familiar and dangerous one – Plasmodium falciparum, the agent responsible for malaria. 

Transmitted by the bite of mosquitoes, P.falciparum infects over 500 million people every year. Its closest relative is a related parasite, Plasmodium reichenowi, which infects chimpanzees. Leading an international research team, Stephen Rich from the University of Massachussetts has discovered that P.reichenowi is no mere relative – it’s actually P.falciparum‘s ancestor.

Rich compared the genes of the two species to build a Plasmodium family tree, which showed that all of the 133 known strains of P.falciparum, from all parts of the world, are united one a single branch on the P.reichenowi lineage. The stem of that branch represents a single event where P.reichenowi crossed the species barrier from chimps to humans.

The new study was possible because of eight newly collected samples of P.reichenowi from wild and captive chimps. Until now, only a single sample of this species had ever been isolated. Armed with fresh samples, the team focused their attention on three genes – cytB, clpC and 18s rRNA. They found that those of P.reichenowi are very varied, much more so than its genetically uniform cousin P.falciparum (even though we have over 16 times as many samples of the latter). Chances are that any two samples of P.reichenowi are more genetically distinct that either one is to P.falcarium.

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Snails get sexy when parasites are around

By Ed Yong | July 24, 2009 10:00 am

Blogging on Peer-Reviewed ResearchIn Lake Alexandrina, New Zealand, a population of snails is under threat from a parasitic flatworm, a fluke aptly known as Microphallus. The fluke chemically castrates its snail host and uses its body as a living incubator for its larvae. But the snails have a weapon against these body-snatching foes – sex.

The New Zealand mud snail Potamopyrgus antipodarum is found throughout island’s freshwater habitats. They breed either sexually or asexually through cloning, and the two strategies vary in prevalence throughout the lake. In the shallower waters round its margins, sex is the name of the game, but in the deeper waters towards the lake’s centre, snails are more likely to opt for cloning.

Kayla King from Indiana University has shown that it’s the concentration of the local parasites that drives this gradient of sex. The flukes spend their adult lives in ducks and they rely on the birds inadvertently scooping up their larvae while feeding. In Lake Alexandrina, ducks only feed in the shallow waters around the lake’s margins so these areas are hotspots for parasites, and for co-evolutionary wars between them and their snail hosts. Sex provides the snails with the genetic ammunition they need to stay in the game.

The snails and their parasites beautifully support and illustrate the principles of the Red Queen hypothesis, which suggests that one of the chief benefits of sex lies in providing the genetic innovation necessary to outfox parasites in evolutionary arms races.

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Traumatic insemination – male spider pierces female's underside with needle-sharp penis

By Ed Yong | April 28, 2009 7:00 pm

Blogging on Peer-Reviewed ResearchThe courtship rituals of the spider Harpactea sadistica start innocently enough, with a dance and a hug. The male spider taps the female gently with his front legs and embraces her. But from that point onwards, things for the female go rapidly downhill. The male bites her and she becomes passive, allowing him to manoeuvre her into position. Like all spiders, his genitals are found next to his head, on a pair of appendages called the pedipalps. But unusually, his penis ends in a needle-sharp tip called an embolus.

The embolus sits at the end of a loop called the conductor. The male hooks one of these loops around the opposite embolus to steady it. Then, by rotating the anchored needle, he drives the point straight through the female’s underside and ejaculates directly into her body cavity. On average, he does this six times, moving slowly downwards and alternating between his two penises. The entire cringeworthy sequence lasts about 15 minutes and throughout it, the male spider never penetrates the female’s actual genital opening.

The species was discovered in Israel last year by Milan Rezac from the Crop Rsearch Institute in the Czech Republic. He named it well. H.sadistica practices a style of sex that’s understandably known as “traumatic insemination“. It’s disturbingly common among insects and other invertebrates, and is most famously practiced by bedbugs. But this is the first time that the behaviour’s been seen among the chelicerates – the group of animals that includes spiders, scorpions and mites.

You can see it happening in the videos below. In the first, the male spider bites and incapacitates the female. In the second, he hooks the conductor of one pedipalp around the embolus of another and, with rotating motions, drives it into the female. These videos aren’t pretty – you’ve been warned.

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The rebellion of the ant slaves

By Ed Yong | April 1, 2009 8:30 am

Blogging on Peer-Reviewed ResearchHumans aren’t the only species that have had to deal with the issue of slavery. Some species of ants also abduct the young of others, forcing them into labouring for their new masters. These slave-making ants, like Protomagnathus americanus conduct violent raids on the nests of other species, killing all the adults and larva-napping the brood.

When these youngsters mature, they take on the odour of their abductors and become the servants of the enslaving queen. They take over the jobs of maintaining the colony and caring for its larvae even though they are from another species; they even take part in raids themselves. But like all slave-traders, P.americanus faces rebellions.

Some of its victims (ants from the genus Temnothorax) strike back with murderous larvae. Alexandra Achenbach and Susanne Foitzik from Ludwig Maximillians Universty in Munich found that some of the kidnapped workers don’t bow to the whims of their new queen. Once they have matured, they start killing the pupae of their captors, destroying as many as two-thirds of the colony’s brood.

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Parasites can change the balance of entire communities

By Ed Yong | February 28, 2009 12:00 pm

Blogging on Peer-Reviewed ResearchConspiracy 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’.

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. And by changing the behaviour of their hosts, parasites can change the face of entire habitats. Chelsea Wood and colleagues from Dartmouth College have found compelling evidence for this, by showing that a tiny flatworm can alter the structure of a tidal habitat by infecting small marine snails.

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Mud time capsules show evolutionary arms race between host and parasite

By Ed Yong | February 11, 2009 8:30 am

This is the fifth of eight posts on evolutionary research to celebrate Darwin’s bicentennial.

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Life can sometimes be 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.

These 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.

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.

The lake is home to a small crustacean called a water flea (Daphnia magra) and a parasitic bacteria Pasteuria ramosa that lives inside it. Both species can undergo dormant states, and Decaestecker found that the lake’s sediment preserves members of this sleeping fauna from up to 39 years ago. Every layer of sediment acts as a time capsule, preserving members from previous generations

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Of flowers and pollinators – a case study of punctuated evolution

By Ed Yong | February 10, 2009 8:30 am

This is the fourth of eight posts on evolutionary research to celebrate Darwin’s bicentennial.

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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.

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 accurately predicted the extraordinary but matching lengths of moth tongue and orchid spur, but his explanation for them is another story.

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 use in explaining the relationship between flowers and pollinators has been called into question.

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. In this group, the duo found that evolution happened in a stop-start ‘punctuated’ way, as the flowers encountered new pollinators with increasingly long tongues.

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Butterflies evolve resistance to male-killing bacteria in record time

By Ed Yong | February 9, 2009 2:00 pm

This is the third of eight posts on evolutionary research to celebrate Darwin’s bicentennial.

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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.

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. But 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 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. In just ten generations, they evolved resistance to the parasite – a dramatic example of natural selection in action.

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