In December 2007, Marie-Anne Félix was taking a small cruise along the southwestern coast of India when she found herself docked in a remote lagoon in the backwaters of Kerala. Félix half recalls kingfishers foraging in the brackish waters around her, and pandanus shrubs creating a lush, green hue along the shore, but her gaze was mostly fixated on the brown, decaying matter on the ground.
"I had the whole boat crew looking at me, and there's a beautiful landscape, but I was more interested in rotting fruit," she says. "Usually, it requires a lot of explanation."
The explanation is that Félix, a developmental biologist at the Jacques Monod Institute in Paris, was hunting for microscopic nematode worms related to Caenorhabditis elegans.
C. elegans was the first organism to have its complete genome sequenced. But when it comes to finding functionally important genes or understanding greater evolutionary patterns, one genome alone is simply not enough. "The problem with Caenorhabditis," explains Félix, "is that the species relationships are so distant that we can't do informative comparative studies." Researchers have long suspected that additional closely related species exist; they just didn't know where to look.
"The turn of the whole thing was when we realized that the ecology of almost the whole genus is in rotting fruits," Félix says. Her first success of the year was a worm that crawled out of a citrus fruit from Ghana sent to her last June by Matthias Herrmann of the Max Planck Institute for Developmental Biology in Tübingen, Germany. In Kerala, Félix found two new species: one from decaying flowers in a botanical garden in the state capital, Trivandrum; the other from multiple rotting delicacies, including coffee grains, nutmeg, banana leaves, and a local fruit called bilimbi.
Most recently, Félix found a new Caenorhabditis species earlier this year in rotting torch ginger flowers, a relative of edible ginger root, from the island of Réunion, off the east coast of Madagascar. The flowers were sent to her from colleague Valérie Robert of the School of Higher Education (ENS) in Paris, but they were originally collected on a hike through the rainforest by Robert's 8-year-old nephew, Loïc Sablé. This species has both triggered young Sablé's interest in biology and revealed clues about the evolution of hermaphroditism, according to Félix.
The new species from Réunion reproduces in the same peculiar way as C. elegans and its relative C. briggsae, primarily by self-fertilizing hermaphrodites but occasionally as males. Félix sent her worms to Karin Kiontke, an evolutionary biologist at New York University, who sequenced several genes to reveal phylogenetic relationships. Based on her analysis, Kiontke says that hermaphroditism probably evolved three separate times in the Caenorhabditis genus. "Every [other explanation] is too complicated," she says. "The most parsimonious reconstruction is to have hermaphroditism evolve three times independently." This indicates that something in the ecology of these worms is driving them to "go it alone" in reproduction, Kiontke says.
Félix is also excited about the new species from the Trivandrum botanical gardens, as it provides the first incidence of fertile hybridization in the genus. When females of this species mate with C. briggsae males, they produce viable females, sterile males, and no hermaphrodites. Eric Haag, a developmental geneticist at the University of Maryland in College Park, had been trying unsuccessfully for years to obtain viable Caenorhabditis hybrids to map the genes underlying hermaphroditism. "About a month after I decided the hybrid approach was dead, I got this E-mail from Marie-Anne [Félix]," says Haag. "I couldn't believe this was possible; it was like an angel dropped this worm out of the sky."
All these new species are filling in the missing gaps in the Caenorhabditis phylogeny. Still, based on Kiontke's analysis, none of Félix's new worms are very closely related to C. elegans on an evolutionary timescale. "It's important to have a closer species," says Félix. "That would be the dream - both to do hybridization studies, and for molecular evolution." For now, she'll keep looking. "We're just scratching the surface."
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