Every night, glass frog fathers face a tough choice: care for the eggs they have already fertilized, or abandon them to get busy with other females. Fortunately, the eggs—which rely on their dads to moisten them nightly as they develop on leaves—have figured out a way to take care of themselves. New research shows that abandoned glass frogs deal with delinquent dads by hatching early, thus avoiding the chance of death by desiccation.
The work "makes us think about embryos as cognitive organisms that can assess their environment and make some sort of appropriate response rather than just passively being on a timetable [for hatching]," says Karen Martin, a physiological ecologist at Pepperdine University in Malibu, California, who was not involved in the study.
In the 1990s, Karen Warkentin, an integrative biologist at Boston University (BU), discovered a tropical frog that can hatch early in response to vibrations from snakes and other would-be predators. More recently, another team has discovered that lizard embryos do likewise. Other scientists have shown that temperature—such as the warmth provided by birds incubating eggs—can also speed up development. But Jesse Delia, now a graduate student at BU, wanted to know whether the loss of parental care had any effect on when an egg hatched.
Even before becoming a graduate student, Delia was fascinated by glass frogs, which are native to Central and South America and named for their translucent skin. The male glass frog, in particular, has quite the nightlife. After dark, he kicks things off by fighting with other males and calling to lure in females. But he won’t wait forever: If no female visits him before midnight, he spends the rest of the night hopping from leaf to leaf to visit the clutches of eggs he previously fertilized. He waters each for up to a half-hour before moving on to the next, likely preventing the delicate embryos from drying out. But when a female does show up, the male glass frog forgets all about his paternal duties, climbs up on her back, and spends the next few days in the thrall of mating. "During that time, all the other clutches get neglected," Delia says.
To assess the consequences of dad delinquency, Delia removed 40 males from their clutches between 2 and 8 days after the eggs were laid. He monitored how well the abandoned embryos did, how fast they developed, and when they hatched. He compared that data with similar information collected about the clutches of 50 males who were faithful to their duties. And to make sure his laboratory experiment accurately reflected what happened in nature, Delia stayed up night after night near a remote stream in Colombia monitoring 18 wild males and their clutches.
Removing a male just 2 days after the eggs were laid was fatal to the embryos, Delia and his colleagues found. If a dad stuck around between 3 and 8 days, on the other hand, the embryos survived—having become sufficiently hydrated—but hatched after about 12 days, the team reports online today in the Proceedings of the Royal Society B. Well-cared-for eggs took twice as long to hatch, he notes. By examining the embryos, he determined that development didn't speed up in the abandoned eggs. Instead, they simply hatched at a less mature stage: Their guts were simpler and they continued munching on the egg’s yolk for nutrients even after hatching.
At 12 days, "they are ready to hatch, but they can wait a few days," Martin explains. "If conditions are good—it’s nice and wet and there's still yolk available—the simplest thing to do is to stay as they are. If not, then it’s probably good to move on."
"It's really amazing that these tiny frog embryos can detect changes in parental care and adjust their behavior in response to whether dad is present or not," says Hope Klug, an evolutionary biologist at the University of Tennessee, Chattanooga, who was not involved in the study.
The work "opens up a new way to think about parent-offspring interaction," says Suzanne Alonzo, an evolutionary biologist at Yale University. Thanks to studies like Delia’s, she says, scientists must now consider how a parent's actions can influence the evolution of an embryo's behavior. If a parent always tends the eggs, there's no need to evolve flexibility in hatching time. But if the parent, like the male glass frog, is unpredictable, then this “hatching plasticity” comes in handy.
Delia’s result "exemplifies how parental and offspring strategies coevolve," says Tobias Uller, an evolutionary biologist at the University of Oxford in the United Kingdom, with the evolution of parental care affecting the evolution of the embryo. And, Martin adds, "If you really think about it, for many animals the most vulnerable stage is early in life, and that’s probably where a lot of evolution is occurring. [Embryos] are not just a life stage that is waiting to become an adult."