Genetic flip produces two plants for the price of one

On the western coast of America, a combination of cool fog and salty sea spray keeps the soil moist all year round. In these wet conditions, you’ll find an unassuming plant called the yellow monkeyflower. Drive further inland, and the climate changes considerably. It’s hotter and drier, and every summer brings a harsh drought. But here too, the yellow monkeyflower blooms but its lifespan is shorter and its leaves are less luscious. Despite their different habitats and lifestyles, both groups of monkeyflowers are members of the same species. But that might eventually change.

David Lowry from Duke University discovered the secret of the monkeyflower’s dual identities lies in a flipped chunk of DNA. A large chunk of the plant’s genome, containing around 360 genes, has been flipped upside-down, effectively giving it two genomes for the price of one.

Since their discovery in 1921, scientists have found examples of these genetic inversions all over the place. For example, around 1,500 of them separate the chimp genome from our own. These inversions are created when a part of the genome breaks in two places and the floating chunk is welded back into place in the wrong orientation. The effect is like cutting out the middle of a recipe book and gluing it back upside down – all the same information is there, but some of it is in the wrong order.

Lowry found that one version is found in the inland plant, which is threatened by a yearly drought. With its life in peril every summer, this plant is an annual; it flowers as quickly as possible, produces seeds, and then dies as soon as the drought sets in. The other flipped version is found in the coastal perennial variety, which is never threatened by drought. Taking advantage of the year-round moisture, it can afford to give equal priority to growth and reproduction. It produces luscious leaves, flowers later, and lives for many years.

It seemed like the inversion was acting as a supergene, which allows the plant to survive in two very different habitats. But such claims have been made before and Lowry has provided more evidence for this than ever before. He has actually managed to swap the two versions of the supergene, putting the annual version into a perennial plant and the inverted perennial version into an annual plant, before testing the effects in the field.

Lowry was inspired by another monkeyflower experiment, which converted a hummingbird-pollinated plant into a bee-pollinated one through careful breeding. He wanted to see if he could do the same, transforming a late-flowering perennial into an early-flowering annual. That was not easy. Without any idea about which genes are involved, the only option is to carefully cross-breef plants from the two populations.

“I started breeding soon after I started grad school in 2005, and after ten generations of breeding and countless hours in the lab I finally had the plants I needed in 2009,” he says. “It was not until 2007 that I realized I was actually dealing with a chromosomal inversion.  That’s when things got interesting.”

Eventually, it became clear that the inversion plays a large role in the monkeyflower’s double life. Annual plants with the perennial inversion flowered later than they normally would, while perennial plants with the annual genes flowered much earlier.

To see how these changes affected the plants in the wild, Lowry planted his edited individuals, together with their normal parents, in both coastal and inland sites. A year later, it was clear that in both locations, the native parent plants did far better than their cross-bred edited offspring. They were more likely to survive long enough to produce flowers, and they produced more of them.

But it was also clear that the inversions were also adapted to the different habitats. Lowry says, “The inland annual orientation of the inversion outperforms the coastal perennial orientation in inland habitat.  The opposite pattern occurs at the coast.” Lowry also found that some inland plants carry the inversion that’s usually found in their coastal kin, but only if they grow in areas with lots of moisture, like riverbanks or high mountains. It’s yet more confirmation that the inverted genes have adapted to different local conditions.

But the inversion does more than that – it also prevents the two types of monkeyflower from mating with one another. For a start, the coastal plants flower much later than their inland cousins, so there are few occasions where pollen from one group can reach the blossoms of the other.

More importantly, as Lowry showed, immigrants from one habitat do very badly in the other. Annual plants do poorly in the coast where their flower-early-die-young lifestyle can’t beat perennial plants that take their time to grow and exploit the plentiful moisture. Meanwhile, the perennial plants are ill-suited to an inland life because their relaxed flowering schedule sees them succumbing to the summer drought before they seed the next generation.

This means that even though both types of yellow monkeyflower are found along the same stretch of the American coast, they are effectively isolated from one another. Neither type does well in the conditions that the other thrives in and, as a result, their genes don’t have a chance to mingle. In time, the two varieties could split into separate species.

This is one of the clearest examples yet that genetic inversions can contribute to the origin of species. Without the inversion, it’s possible that the monkeyflower would eventually have adapted to the two different habitats and split into different species (and indeed, other genetic differences separate the annual and perennial varieties). But inversions can greatly accelerate that process.

During sex, chromosomes from both parents are united in an embryo and shuffled together, in a process called recombination. But to do this, they first need to align with one another and they can’t do that if one of them has a massive flipped segment. That’s exactly what Lowry found in the monkeyflower. When he cross-bred the inland and coastal plants, he found that one specific part of their genome refused to recombine, even though it had no problem doing so when plants from the same area were crossed.

Without the ability to recombine, the inverted genes are free to evolve on their own terms. If these genes allow species to adapt to their local environment, then individuals that carry the inversion will start to dominate a specific habitat, becoming separated from their cousins with the normal version.

Reference: PLoS Biology http://dx.doi.org/10.1371/journal.pbio.1000500

PS: David Lowry is married to Sheril Kirshenbaum, one of my excellent fellow Discover bloggers. You can read her writing at The Intersection if you don’t already.

More on the origin of species:

• Spots plus spots equals maze: how animals create living patterns
• Holy hybrids Batman! Caribbean fruit bat is a mash-up of three species
• British birdfeeders split blackcaps into two genetically distinct groups
• Discriminating butterflies show how one species could split into two
• Giant insect splits cavefish into distinct populations
• How diversity creates itself – cascades of new species among flies and parasitic wasps