Aphids can make their own carotenoids -- organic pigments that serve a variety of functions in animals, but until now, were believed to be produced only by bacteria, plants, and fungi.

Pea aphids with genetically based differences in carotenoid content. Green and red individuals represent a naturally occurring polymorphism; yellow-green individuals are mutants derived from a red parental line. Image: Charles Hedgcock, R.B.P

The small insects appear to have acquired the carotenoid-making ability via lateral gene transfer from a fungal species, according to a study published this week in Science.

"This is the first documentation of animals being able to produce their own carotenoids," said evolutionary biologist Alex Badyaev of the University of Arizona, who did not participate in the research. "This is a huge deal because carotenoids are [some] of the most diverse biological compounds [and have] a tremendous variety of important functions in animals -- everything from vision to immunocompetence to ornamentation."

In addition, this is the "first clear cut demonstration of lateral [gene] transfers providing a new gene function," added evolutionary geneticist Jack Werren of the University of Rochester, who was also not involved in the study. "There's mounting evidence that animals do pick up DNA from bacteria and [other] simple organisms, such as yeast and fungi," but until now, there has been little evidence that these genes have any function in their new hosts, he said.

Aphids are small, plant-dwelling insects that drill into the plants' vessels to feed on the sap inside. Like many animals, they harbor various carotenoids in their bodies, which give them their green or red color. Until now, however, scientists have assumed that they acquired these pigments either from their diet or the symbiotic bacteria that reside in specialized cells called bacteriocytes.

But the types of carotenoids found in plants differ from those found in aphids, and none of the most common bacteria living in symbiosis with aphids contain any genes related to the synthesis of carotenoids, suggesting that aphids must have a different way of acquiring these compounds. Curious, evolutionary geneticist Nancy Moran and her colleague Tyler Jarvik of the University of Arizona decided to scour the recently sequenced aphid genome for evidence of carotenoid-producing genes.

Sure enough, the researchers found all the necessary genetic machinery needed to build carotenoids. Based on sequence and structural analyses, they determined that the genes were most closely related to those found in certain types of fungi, suggesting aphids had acquired the genes directly from a fungal species sometime in their distant evolutionary history.

It's a "very clever way of doing it," Badyaev said. "Instead of getting this enzymatic pathway built step by step, they simply just lift the whole machinery from fungi." After acquiring this "complete set of equipment," he added, "they put it to immediate use," which probably helps explain why those genes were maintained over time, rather than being lost from the aphid genome.

The carotenoids in aphids determine whether the animals will be brownish-red or pale green -- a color dimorphism that is maintained in populations because of the advantages (and disadvantages) to each, Moran said. "The red ones were more susceptible to predators, [such as] lady bird beetles [which are] better able to find and eat the red ones," she said. On the other hand, "little parasitoid wasps, [which are a] major natural enemy of aphids, [are] better able to find and attack the green ones."

The different colors, the researchers discovered, are determined by a difference in a single locus on one of the seven aphid carotenoid genes identified. One allele contains a large deletion which inhibits the animals' ability to produce torulene -- the compound that gives the red aphids their color. Thus, individuals containing two copies of this smaller allele are pale green, while individuals with at least one intact allele are red. Because this polymorphism "is maintained by selection," so are the carotenoid genes, Badyaev said.

"Here we have a case of ancient transfer [that] ties in so beautifully with the biology of the organism," Werren said. "It's one of the first definitive cases of [gene transfer with a] functional significance to the animal."

N.A. Moran and T. Jarvik, "Lateral transfer of genes from fungi underlies carotenoid production in aphids," Science:328:624-7, 2010.


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