If you were to look closely at a prickly pear in mainland western Mexico, chances are you would find a population of flies—Drosophila navojoa, to be exact.
Despite their colloquial name of “fruit fly,” many of the over 1,500 species of Drosophilid flies breed in everything from toxic mushrooms to slime flux, the bacteria-infected sap that can sometimes be seen oozing from diseased oak trees. Flies like D. navojoa breed and feed in particular species of cacti, making them part of the cactophilic Drosophila model system. There are over 100 cactus-loving Drosophilid species, of which some are specialists and some generalists, that have radiated throughout North and South America. This parallel radiation is part of what makes them so intriguing to researchers.
“It’s great, because you really have a naturally-replicated experiment,” said Dr. Therese “Teri” Markow, Professor Emeritus at University of California San Diego. “So you can ask, ‘What happened down south? And what was the process compared to up in the north?’”
Markow has spent over 40 years studying the cactophilic Drosophila model system. Markow had originally intended to study humans, doing her undergraduate studies in physical anthropology at Arizona State University (ASU). Thanks to a compelling senior year genetics class and a persistent professor, Markow ended up diving into the world of Drosophila as a PhD student, doing her doctoral research on the classic fruit fly model system, Drosophila melanogaster.
While a postdoc at ASU, Markow connected with the lab of University of Arizona’s Dr. William Heed, who studied cactophilic Drosophila. Markow jumped at the chance to go out in the field with Heed’s lab, and she was enthralled by what she found.
“There the flies were on the cactus, mating and feeding and everything! You could actually link the genetics with ecology,” Markow said.
Heed’s lab pioneered the work on the cactophilic Drosophila model system. The unique system drew attention from people in many different subdisciplines. Some researchers were interested in characterizing the host plants’ chemistry, some in Drosophila speciation events. Still others were interested in the bacteria that enabled the relationship between the cacti and the flies.
In 1982, an international group of those researchers met outside of Tucson, Arizona, to share their data. This meeting resulted in a book, Ecological Genetics and Evolution: The Cactus Yeast Drosophila Model System (Barker and Starmer 1982).
Three decades later, not long after D. melanogaster’s genome was sequenced, Markow hosted a meeting for the Drosophila research community in order to discuss sequencing additional Drosophila species. Everyone had their favorite pet species, Markow said. Some wanted species closely related to D. melanogaster, while others favored ecologically-unusual Drosophila species.
The result of that meeting was a 2007 analysis of 12 Drosophila genomes. One of those genomes was that of Drosophila mojavensis, one of the original species that Heed had studied.
“If you were interested in looking at a fly that has a really unique ecology and can breed easily in the lab, Drosophila mojavensis was a logical one,” Markow said. “Once we had a sequence for Drosophila mojavensis, it became kind of the keystone cactophilic species.”
Within D. mojavensis, there are four geographically-isolated subspecies with varying degrees of reproductive isolation. This is part of what makes the cactophilic Drosophila model system not only fascinating but also incredibly useful for studying speciation, Markow said.
“You can capture the whole evolutionary trajectory from very little divergence to complete divergence,” Markow said. “Speciation is a continuum. When you capture populations like D. mojavensis that are along that continuum, you’re able to look at speciation as it’s happening, as opposed to after it happened.”
Cactophilic Drosophilids are also ideally suited for studying adaption. The environment they live in is harsh—the flies must be able to withstand their host plants’ potential toxicity, as well as their environment’s heat and dryness.
“Not a lot of organisms can live like that in the desert,” Markow said. “What genes and genetic interactions have been important in their ability to live in the desert? It’s especially interesting with global warming—if the flies are already at the upper limit of their physiological tolerances, what’s going to happen in the future?”
These questions about speciation and adaptation are two of the drivers of current and future research. In February 2018, the cactophilic Drosophila researchers had another meeting, this time in Alamos, Sonora, Mexico. Markow expects transcriptomics to play a major role in future research. But she also hopes that studying this system will get people out into the field more. That, after all, is how Markow was first drawn into the model system.
“I was just captivated by actually seeing where the flies live. You could actually see the ecological and evolutionary drivers of the phenotypes. Hopefully more people will go and actually measure ecologically in the field—it is important to put what you find at a molecular level in an ecological context,” Markow said.
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Therese Markow is a Review Editor for Journal of Heredity.
— Chantal Cough-Schulze