California's Sierra Nevada mountains are dotted with populations of checkerspot butterflies that belong to the same species but lead separate lives. The populations are differentiated by the host plants where females lay their eggs, with one type favoring Collinsis torreyi (blue-eyed Mary) and the other favoring Pedicularis semibarbata (pine lousewort). Other than that, the checkerspots are much the same. They are alike morphologically and genetically, and can also interbreed and produce hybrid offspring. So what does keep them apart? New work by Carolyn McBride and Michael Singer in this issue of PLoS Biology reveals it is traits that let each type get the most out of its chosen host plants, but put hybrids at a disadvantage on either plant.
Such divergence of populations, where offspring are viable but maladapted due to intermediate traits not suited to either ecological niche, is called extrinsic postzygotic isolation (EPI) and is thought to be an early stage in the formation of new species. However, there are few examples of EPI and most are in cases where strong barriers to mating already exist, leaving the extent of EPI's contribution to speciation in question. The apparent lack of mating barriers between the Sierra Nevada checkerspot populations makes this a particularly good system for teasing out the relative strength of EPI as a driver of speciation.
The traits that distinguish the butterfly populations stem from key differences in the two host plants, which grow intermingled on the western slopes of the mountains. Blue-eyed Mary is a short-lived annual with leaves that die from the bottom up, and female checkerspots adapted to this host plant lay their eggs on the nutritious new growth near the top. In contrast, pine lousewort is a perennial that stays green all summer and grows new leaves from the base, and females adapted to this host plant lay their eggs near the bottom.
To see if EPI is nudging these butterfly populations apart, McBride and Singer asked whether hybrids were intermediate for traits that distinguish the parents, including where females lay their eggs, clutch size, where larvae forage, and larval growth and survival. The researchers discovered that hybrids were somewhere in the middle for all traits tested. For instance, whereas the two parent populations prefer the host plants to which they are adapted, hybrid females readily lay their eggs on either host.
Next, the researchers asked whether these intermediate traits put hybrids at a disadvantage in the wild. Hybrids were perfectly healthy when raised in the laboratory, indicating that they had no intrinsic defects, but fared poorly under natural conditions. Field tests revealed that each intermediate behavior was maladaptive, with intermediate egg laying behaviors being the most disadvantageous. Whereas “blue-eyed Mary” females preferred plants that were still in bud, hybrids preferred blue-eyed Mary plants that were already in bloom, and laying eggs on these older plants cut offspring survival 70%. Moreover, whereas “blue-eyed Mary” females lay their eggs near plant tops and “lousewort” females lay theirs near the ground, hybrid females lay theirs at intermediate heights on lousewort, and larvae there grew roughly 50% slower than those near the ground. Measuring larval growth on lousewort entailed individually super-gluing about 30 eggs to leaves and there were 12 such clutches at each of 14 field sites, making this perhaps the most painstaking of the tremendous amount of work behind these field tests.
In addition, “blue-eyed Mary” females lay relatively small clutches of up to 20 eggs and “lousewort” females lay larger clutches of up to 100. But hybrid females lay medium-sized clutches that are at a disadvantage on both host plants: larval survival was higher for smaller clutches on blue-eyed Mary and for larger clutches on lousewort. This difference is likely due to higher rates of egg predation on lousewort.
To visualize how the distinguishing traits isolate the two butterfly populations, the researchers constructed an “adaptive surface” or fitness landscape by plotting host preference and clutch size against offspring survival. The resulting landscape neatly displays two fitness peaks separated by a maladaptive valley, with one of the parent butterflies on each peak and hybrids lying in the valley.
Ecological selection against hybrids has been demonstrated in a few species including threespine sticklebacks and Darwin's finches. However, it has been difficult to sort out the relative impact of EPI from other forms of reproductive isolation such as mating barriers and geographical separation. By showing that behavioral differences alone are enough to keep the Sierra Nevada checkerspot populations apart in the wild as well as by demonstrating that hybrids fare poorly in the wild due to intermediate traits, this work makes a compelling case that EPI can play a strong and perhaps even primary role in the onset of new species formation.
Other cases where diverging populations produce hybrids with adverse intermediate behaviors include the European blackcap, a migratory warbler that winters in southern Europe and Africa. Some of these birds migrate southeast and others southwest, and hybrids between the two choose an intermediate direction that can lead to daunting flightpaths over the Alps, the Mediterranean Sea, and the Sahara Desert. Because adaptation to new niches is often accompanied by preferences for that niche, such maladaptive intermediate behaviors may be a widespread driver of EPI amongst animals. Furthermore, most previous estimates of EPI are from laboratory studies that fail to account for real-world challenges such as predators and pathogens, raising the possibility that the impact of ecological selection has been underestimated. Taken together, these considerations suggest that EPI may be a more significant driver of speciation than previously suspected.
McBride CS, Singer MC (2010) Field Studies Reveal Strong Postmating Isolation between Ecologically Divergent Butterfly Populations. doi:10.1371/journal.pbio.1000529
How did lager beer come to be? After pondering the question for decades, scientists have found that an elusive species of yeast isolated in the forests of Argentina was key to the invention of the crisp-tasting German beer 600 years ago.
It took a five-year search around the world before the scientific team discovered, identified and named the organism, a species of wild yeast called Saccharomyces eubayanus that lives on beech trees.
“We knew it had to be out there somewhere,” said Chris Todd Hittinger, an evolutionary geneticist at the University of Wisconsin-Madison and a co-author of the report published in the Proceedings of the National Academies of Sciences.
Their best bet is that centuries in the past, S. eubayanus somehow found its way to Europe and hybridized with the domestic yeast used to brew ale, creating an organism that can ferment at the lower temperatures used to make lager.
Geneticists have known since the 1980s that the yeast brewers use to make lager, S. pastorianus, was a hybrid of two yeast species: S. cerevisiae— used to make ales, wine and bread—and some other, unidentified organism.
Searching through collections of wild yeasts from Europe, researchers —including Hittinger and his collaborators— tried to identify lager’s missing link but again and again were stumped. “There were a few candidates, but none fit particularly well,” Hittinger said.
So he and his colleagues began “sampling more systematically,” collecting soil and bark, sap and abnormal growths called galls from trees on five different continents.
Team member Diego Libkind, of the Institute for Biodiversity and Environment Research in Bariloche, Argentina, found S. eubayanus in galls on southern beech trees in Patagonia. The galls were particularly rich in sugar, which yeast like to colonize and consume.
Patagonian natives used to make a fermented beverage from the galls— a definite clue that the scientists were on the right track, Hittinger said.
When the team brought the yeast to a lab at the University of Colorado and analyzed its genome, they discovered that it was 99.5 percent identical to the non-ale portion of the S. pastorianus genome, suggesting it was indeed lager yeast’s long-lost ancestor.
“The DNA evidence is strong,” said Gavin Sherlock, a geneticist at Stanford University who has studied lager yeast but was not involved in this study. But Sherlock wondered how S. eubayanus could have traveled the nearly 8,000 miles from Argentina to Germany.
“We all know that in 1492, Columbus sailed the ocean blue,” he said. “Lager was invented in the 1400s. It’s not really clear how that progenitor would have gotten from South America to Europe.”
The beech forests where the team found S. eubayanus are cool, with an average year-round temperature of 43 to 46 degrees Fahrenheit, said Hittinger. Genes that permit the yeast to thrive in such a chilly environment probably provided S. pastorianus’ ability to ferment at relatively lowtemperatures— conditions not too terribly different from those prevalent in the Bavarian cellars where monks created the golden brew back in the 15th century.
The researchers compared the DNA of the wild Patagonian yeast with that of lager yeast used in breweries to see what changes had evolved over the years. They found changes in genes that regulate sugar and sulfite metabolism, processes that contribute to the fermentation and preservation of beer. Scientists could exploit such knowledge to improve biofuels, he said.
And of course, tinkering with yeast genes might make wine or beer taste better, too, said Hittinger, who is “a lager man.” Co-author Mark Johnston, a molecular biologist at the University of Colorado School of Medicine, prefers ales.
Like Coke versus Pepsi, tropical land ecosystems come in two choices: forest or grassland. New research shows these two options can switch abruptly, and there’s rarely any in-between.
If so, then many of these ecosystems are particularly vulnerable to future changes such as rising temperature, scientists say. With just slight shifts in rainfall or other factors, people living in what is now tropical rainforest might suddenly find themselves in scrubland populated by a different mix of plants and animals — where people’s livelihoods might have to change dramatically.
“That transition is not going to happen smoothly,” says Milena Holmgren, an ecologist at Wageningen University in the Netherlands. “The evidence is showing there are these big jumps.”
Holmgren and her colleagues describe the finding in the Oct. 14 Science. Another group, from Princeton University and South Africa’s national research council, report similar conclusions in a second paper in the same journal.
In theory, the relationship between rainfall and tree cover should be straightforward: The more rain a place has, the more trees that will grow there. But small studies have suggested that changes can occur in discrete steps. Add more rain to a grassy savanna, and it stays a savanna with the same percentage of tree cover for quite some time. Then, at some crucial amount of extra rainfall, the savanna suddenly switches to a full-fledged forest.
But no one knew whether such rapid transformations happened on a global scale. Separately, both research groups decided to look at data gathered by the MODIS instruments on board NASA’s Terra and Aqua satellites, which sense vegetation cover and other features of the land surface. This information included how much of each square kilometer of land was covered by trees, grasses or other vegetation. Both teams focused on the tropics and subtropics of Africa, South America and Australia, because those areas are thought to be least disturbed by human activity.
Looking at the numbers, Holmgren’s group identified three distinct ecosystem types: forest, savanna, and a treeless state. Forests typically had 80 percent tree cover, while savannas had 20 percent trees and the “treeless” about 5 percent or less. Intermediate states — with, say, 60 percent tree cover — are extremely rare, Holmgren says. Which category a particular landscape fell into depended heavily on rainfall.
Fire may be another important factor in determining tree cover, as the second group found. Led by Princeton ecology graduate student Carla Staver, this team studied how fire helped differentiate between forest and savanna. Fire spreads quickly in savannas because of all the grasses and slowly in tree-dense forests. “There’s a tipping point between where you get fires spreading easily and where you don’t,” Staver says.
That point, she and her colleagues found, sits at a tree cover of about 40 to 45 percent. Below that number, fires spread easily and prevent new trees from establishing themselves. Above that number, trees work to maintain a thick canopy that acts as a barrier to stop fire from spreading.
“These two papers tell us that these feedbacks really do operate at all scales,” says Audrey Mayer, an ecologist at Michigan Technological University in Houghton. “They’ll make us have to redo some of our assumptions about how things are going to change in the future.”
Many global climate models, for instance, assume a smooth transition between savanna and forest as temperature and rainfall change. But the new work suggests that forests could appear or disappear quickly, Mayer says, especially if people complicate the picture. “You can’t just plant a couple of trees and they’ll grow up and the forest will come back,” she says. “You have to fight those internal feedbacks.”
Staver and her colleagues are now searching for savanna-forest transitions that are occurring right now. “These things are definitely happening,” she says, “and the new work tells us it could be even more widespread than we’d thought.” Studying where landscapes are changing could help the scientists better understand what causes ecosystems to tip from one category to the other.
For their part, the Dutch scientists have developed “resilience maps” that show which places are most likely to tip from savanna to forest or vice versa. Farmers scratching out a living in western Africa or ranchers running cattle on the fringes of the Amazon might use such maps to learn how viable their livelihoods are likely to be in coming decades.
Locals could thus spend more time and energy working to keep the ecosystem the way it is, perhaps by building extra capacity for storing water or by cutting back on logging. Or residents could cut down more trees to tip a forest into a grassy rangeland for their animals. “These maps can be a tremendous tool for all kinds of organizations,” Holmgren says.
Mayer says she’d like to see the analysis extended into the Northern Hemisphere, where she suspects the results might be the same. Across parts of Illinois and Indiana, for instance, stretches a narrow strip of tallgrass prairie surrounded by forests dubbed the “prairie peninsula.” The peninsula was probably kept grassy by centuries of fire and grazing management — because otherwise it, too, would revert to forest.