It’s not every day that you hear about spy missions that involve a lack of sex, but clearly parasitic wasps don’t pay much attention to Hollywood clichés.
These insects merge the thriller, science-fiction and horror genres, They lay their eggs inside other animals, turning them into slaves and living larders that are destined to be eaten inside-out by the developing grubs. To find their victims, they perform feats of espionage worthy of any secret agent, tapping into their mark’s communication lines, tailing them back to their homes and infiltrating their families.
Two species of parasitoid wasp – Trichogramma brassicae and Trichogramma evanescens – are particularly skilled at chemical espionage. They’ve learned to home in on sexual chemicals used by male cabbage white butterflies. After sex, a male coats the female with anti-aphrodisiac that turns off other suitors and protects the male’s sexual investment. These chemicals are signals from one male to another that say, “Buzz off, she’s taken.”
But the wasps can sense these chemicals. They feed on the nectar of the same plants that the cabbage white visit and when they do, the wasps jump her. They are tiny, smaller even than the butterfly’s eye (see the image below), and they hitch a ride to the site where she’ll lay her eggs. There, they lay their own eggs inside those of the butterfly. Amazingly, the wasps use the same trick for different species of cabbage white butterflies, which secrete very different anti-aphrodisiacs. They can even sense when the anti-aphrodisiacs are wafting among the general scent of a freshly mated female. It’s all part of a sophisticated “espionage-and-ride” strategy.
Walk through the rainforests of Ecuador and you might encounter a beautiful butterfly called Heliconius cydno. It’s extremely varied in its colours. Even among one subspecies, H.cydno alithea, you can find individuals with white wingbands and those with yellow. Despite their different hues, they are still the same species… but probably not for much longer.
Even though the two forms are genetically similar and live in the same area, Nicola Chamberlain from Harvard University has found that one of them – the yellow version – has developed a preference for mating with butterflies of its own colour. This fussiness has set up an invisible barrier within the butterfly population, where traits that would typically separate sister species – colour and mate preferences – have started to segregate. In time, this is the sort of change that could split the single species into two.
Heliconius butterflies defend themselves with foul chemicals and advertise their distasteful arsenal with bright warning colours on their wings. The group has a penchant for diversity, and even closely related species sport different patterns. But the butterflies are also rampant mimics. Distantly related species have evolved uncanny resemblances so that their warnings complement one another – a predator that learns to avoid one species will avoid all the ones that share the same patterns. It’s a mutual protection racket, sealed with colour.
The result of this widespread mimicry is that populations of the same species can look very different because they are imitating different models. This is the case with H.cydno – the yellow form mimics the related H.eleuchia, while the white form mimics yet another species, H.sapho.
How can we be sure that the pairs of butterflies that look alike aren’t in fact more closely related? For a start, scientists have shown that the frequencies of the yellow and white versions of alithea in the wild match those of the species they mimic. Genetic testing provides the clincher. It confirms that the two mimics are indeed more closely related to each other than they are to their models.
Genetics also tells us how alithea achieves its dual coats. Colour is determined by a single gene; if a butterfly inherits the dominant version, it’s white and if it gets two copies of the recessive one, it’s yellow. Pattern is controlled in a similar way by a second gene. These variations aside, there are no distinct genetic differences between the two alithea forms. They are still very much a single population of interbreeding butterflies.
But that may change, and fussy males could be the catalyst. Chamberlain watched over 1,600 courtship rituals performed by 115 captured males. Her voyeuristic experiments showed that yellow males strongly preferred to mate with yellow females, although white males weren’t so fussy.
This isn’t just a whimsical preference – Chamberlain thinks that the colour gene sits very closely to a gene for mate preference. The two genes may even be one and the same. Either way, their proximity on the butterfly’s genome means that their fates are intertwined and they tend to be inherited as a unit. That’s certainly plausible, for the same pigments that colour the butterflies’ wings also serve to filter light arriving into their eyes. A change in the way those pigments are produced could alter both the butterfly’s appearance and how it sees others of its kind.
To see what happens when this process goes further, you don’t have to travel far. Costa Rica is home to another H.cydno subspecies called galanthus, and a closely related species called H.pachinus. They represent a further step down the road that alithea is headed down. Galanthus and H.pachinus look very different because they mimic different models – the former has white wingbands reminiscent of H.sapho, while the latter has green bands inspired by H.hewitsoni.
Nonetheless, the two species could interbreed if they ever got the chance. Two things stand in the way. The first is geography – H.cydno galanthus stays on the eastern side of the country, while H.pachinus remains on the west. The second is, as with alithea, sex appeal. Males prefer females bearing the same wing colours as they do so even if the two sexes of the two species were to cross paths, they’d probably fly right past each other.
Genetically, these species have also diverged far further than the two forms of alithea have. They differ at no less than five genes involved in colour and pattern, two of which are practically identical to the ones that causing alithea to segregate. They also provide more evidence that the genes for colour and mate preference are closely linked, for crossbreeding the two species yields offspring with half-way colours and half-way preferences.
These butterflies are by no means the only examples of speciation in the wild. In this blog alone, I’ve discussed a beautiful case study of diversity creating itself among fruit flies and parasitic wasps, explosive bursts of diversity in cichlid fish fuelled by violent males, and a giant predatory bug that’s splitting cavefish into isolated populations.
But Heliconius butterflies may be the most illuminating of all these case studies. They’re easy to capture, breed and work with. And as Chamberlain’s study shows, they can marshal together the contribution of experts in genetics, ecology, evolution and animal behaviour in an effort to understand that most magnificent of topics – the origin of species.
Reference: Science 10.1126/science.1179141
More on speciation:
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.
In 1979, somewhere in Dartmoor, a butterfly died. That would hardly have been an exceptional event, but this individual was a Large Blue butterfly (Maculinea arion) and it was the last of its kind in the United Kingdom. Over more than a century, the Large Blue’s population had been declining and it was finally declared nationally extinct 30 years ago.
Now, it’s back. A bold conservation effort managed to work out the factors behind the butterfly’s decline, and resurrect this vanished species. The Large Blue’s reintroduction has been one of conservation’s flagship successes and it was the first time that efforts to save a declining butterfly had actually paid off.
The victory hinged on strong science. Rather than relying on speculation and optimistic measures, a team of scientists led by Jeremy Thomas, David Simcox and Ralph Clarke carefully analysed the factors behind the butterfly’s decline to find the best ways of reversing it. Work started in 1974 and the butterfly staged its comeback in 1983. Now, on the 25th anniversary of its reintroduction, Thomas, Simcox and Clarke describe their efforts to bring the charismatic Large Blue back to England’s green and pleasant lands.
The Large Blue butterfly has a very strange lifestyle. When it hatches in July, its caterpillar feeds on thyme plants for three weeks and then drops to the ground to begin a more leisurely existence. The caterpillar so strongly mimics the smells and sounds of the ant Myrmica sabuleti that it is carried to the colony and cared for as if it were an actual ant. It spends the next 10 months of its life in this sheltered environment, and its mimicry ensures that its surrogate parents leave it alone, even when it eats their young.
Ants are among the most successful of living things. Their nests are well-defended fortresses, coordinated through complex communication systems involving touch and chemical signals. These strongholds are stocked with food and secure from the outside world, so they make a tempting prospect for any burglars that manage to break in.
One species of butterfly – the mountain alcon blue (Maculinea rebeli) – is just one such master felon. Somehow, it manipulates the workers into carrying it inside the nest, feeding it and caring for it. The caterpillar does so little for itself that it packs on 98% of its eventual adult weight in the company of ants. How does it do it?
Partly, the caterpillar secretes chemicals that imitate those found on ant larvae, and it mimics their actions too. But that can’t be the only explanation for ant workers will actually rescue alcon blue caterpillars over their colony’s genuine larvae. And if food is short, they will even kill their own young to feed the parasitic impostors. In the entire colony, only one individual is treated with as much respect as the caterpillars – the queen.
Now, Francesca Barbero from the University of Torino has found out how the alcon blues manage to get the royal treatment – they “sing” in the style of queens, producing uncanny cover versions using instruments built into their bodies.