Aphids got their colours by stealing genes from fungi

By Ed Yong | April 30, 2010 9:30 am

Aphid_red_greenAphids, those sap-sucking foes of gardeners, come in a variety of colours. We usually think of them as green, but pea aphids sometimes wear a fetching red ensemble. That may not strike you as anything special; after all, lots of animals are red. But the aphid’s colour is unique in a couple of extraordinary ways.

The colour comes from pigments called carotenoids. Animals use them for all sorts of purposes; they act as antioxidants, and they contribute to red, orange and yellow colours. But the pea aphid is one of only a few known species (all aphids) that manufacture their own carotenoids; everyone else gets theirs from their food. But it’s the source of the pea aphid’s ability that’s truly remarkable – it stole the skill from fungi. By integrating fungal genes into its own genomes, it gained a superpower that almost all other animals lack.

These sorts of “horizontal gene transfers” go on all the time in bacteria, but they’re supposedly a rarity among more complex creatures like animals and plants. And yet, scientists have recently documented several examples of such transfers. Rotifers smuggle genes from fungi, bacteria and plants. “Space Invader” genes have jumped across animals as diverse as lizards and bushbabies. One bacterium, Wolbachia, has even inserted its entire genome into that of a fruit fly. And parasites can transfer their genes to humans.

In most of these cases, it’s unclear whether the imported genes are actually doing anything useful. But the story of the pea aphid, told by Nancy Moran and Tyler Jarvik, is very different. The colour of a pea aphid determines the predators that target it. Ladybirds (one of their major enemies) prefer to attack red aphids on green plants but parasitic wasps are more likely to lay their eggs in green aphids, to fatal effect. Colour clearly matters to an aphid, so here is a clear example of a transferred gene shaping an obvious trait in its new host and in doing so, shaping its evolution.

Moran and Jarvik knew that both red and green pea aphids have carotenoids, but their source was a mystery. These pigments dissolve easily in fat but not water, and they’re unlikely to be found in the plant sap that the aphids suck. Aphids carry beneficial bacteria but none of their genomes carry any traces of the genes required for creating carotenoids. And aphids that are cured of their hitchhikers don’t lose their colour. So where do the carotenoids come from?

Fortunately, Moran and Jarvik knew what to look for, since all organisms that make carotenoids, including plants, fungi and bacteria, do so with a common set of genes and enzymes. They also knew where to look, for the genome of the pea aphid had been recently sequenced. Their search yielded seven genes that are clearly involved in producing carotenoids. But to their surprise, none of this septet matched any gene in any other animal genome. Instead, their closest relatives are found in fungi.

Moran and Jarvik think that the original donor was a species of fungus that either infected the ancestors of today’s pea aphids, or formed an alliance with them. Either way, we know that this mystery donor transferred at least two genes to the insects, which have since duplicated into the current seven. And we know that the relocation happened before the pea aphid diverged from the related peach-potato aphid, which has the same genes.

Today, the genes explain the two hues of the pea aphid. The green aphids have carotenoids that are yellow in colour. The red ones do too, but their palette is bolstered by two bright red carotenoids that the green aphids lack. The greens can’t make these extra pigments because one of their seven fungal genes is missing a small sizeable chunk. This broken gene means that the green aphids can’t complete a chemical reaction that converts one of the yellow carotenoids into the two red ones.

The pea aphid’s story tells us that genetic swaps between complex species like fungi and animals are possible, although probably still rare. Before now, scientists did actually try to search the pea aphid genome before for genes transferred from other species. But they only looked for genes of bacterial origin; no one considered that the donors might be fungi, so the carotenoid-making genes were never found.

When Moran and Jarvik searched for other fungal genes, they didn’t find any, demonstrating that such swaps are the exception rather than the rule. But what fascinating exceptions – and the growing number of full animal genomes will surely help us to discover more.

Reference: Science http://dx.doi.org/10.1126/science.1187113

Image: by Charles Hedgcock

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