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Coming through in the clutch
European frog found to use novel mating strategy

| 16 September 2004


A male European common frog embraces a female tightly in a mating grip called amplexus. After quite a bit of this, the female lays a clutch of eggs, which are fertilized not only by the favored male, but shortly thereafter by as many as three other male bystanders. (Miguel Vences photo)
The European common frog, Rana temporaria, has long been thought to have a straightforward breeding strategy — one lucky male grabs the female and fertilizes her eggs as soon as she releases them into the water. End of story.

Spanish researcher David R. Vieites, now a postdoctoral fellow at Berkeley, found that that’s not the end of the story. In high-altitude ponds in the Pyrenees, on the border between Spain and France, so many males are vying for fatherhood that they pirate the egg clutches after they’re laid. Grasping them as they would a female, they release sperm in the floating clutches, often successfully fertilizing the eggs left unfertilized after the initial encounter. In one pond studied, 84 percent of all clutches had been fertilized by more than one male.

In addition, numerous male frogs typically gang around the egg clutch for their turn at fertilization. Genetic analysis of the eggs in a single clutch shows fertilization by as many as four separate males, including the male that actually had its arms around the female.

Vieites also noticed that many females delayed release of their eggs until no other males were around, while others released their eggs underneath other clutches to hide them from prowling males.

While studying high-altitude populations of the European common frog, or brown frog, in an attempt to understand how they adjust to short breeding seasons and survive dry, freezing temperatures, Vieites was surprised to see males embracing clutches. With some colleagues, he spent two years in the field observing this behavior, and took tissue samples to test the paternity of the eggs in numerous clutches.

What they uncovered was a strategy apparently linked to the unusually skewed “operational” sex ratio (i.e., the ratio of eager males to available females) in the Pyrenean ponds. For every female frog there were between four and ten male frogs in a pond about half the size of an Olympic-size swimming pool. Since male frogs fertilize the female’s eggs only after they’re laid, there is no opportunity for more than one male to impregnate a female. And unlike the females of some frog species, the common frog will not lay eggs if clasped by two males.

Since as many as one-third of the eggs may not be fertilized by the first male, however, the opportunity exists for other males to fertilize the remaining eggs in the clutch. The researchers found that without clutch piracy, between 65 and 85 percent of eggs — and sometimes as few as 20 percent — were fertilized. The percentage was about the same with clutch piracy, but averaged 90 percent if, as Vieites observed, one or more of the later frogs forced open the clutch and fertilized the interior eggs.

Vieites found that, because of the overabundance of males, each breeding female in a pond typically is surrounded by a half-dozen or more eager males vying to embrace the female frog in a tight, sometimes suffocating grip called amplexus. Even after the female has allowed a male to clasp it, the surrounding males will often jostle the pair in an attempt to dislodge the male.

After as much as two days of amplexus, the female will lay a clutch of eggs, which are immediately fertilized by the male. During this time, however, various males typically follow the pair around the pond and, after the female has laid the eggs and the parents have left, embrace the clutch and fertilize it again. At other times, gangs of males would search the pond for newly laid clutches and fertilize them again within an hour or two of being laid. Often, males who had fertilized a clutch in the normal way would later join a gang to engage in clutch piracy.

To determine the paternity of the fertilized eggs, which can number between 300 and 3,000 in this species, Vieites gathered 16 separate clutches and took tissue samples from the original parents and the pirates. With colleagues at the University of Konstanz, Germany, and the University of Amsterdam, The Netherlands, he analyzed the tissue samples genetically to show that clutch piracy leads to a greater percentage of fertilized eggs in the clutch, as well as clutches with as many as four fathers.

Vieites noted that this unusual mating strategy is a good way for the frog population to ensure that as many genes as possible are passed on to succeeding generations, particularly when there are far more males than females. Despite the lack of reports of similar behavior elsewhere in Europe, clutch piracy may even be common in Rana temporaria, he said. Vieites plans to continue his studies in the Circo de Piedrafita area of the Pyrenees in Spain, in order to understand better the origin of the behavior, and to investigate the importance of the male-female ratio.

“This could be a good model to help us understand how sexual selection arose in vertebrates, such as amphibians, that developed external fertilization,” he said.

Vieites recently joined the Berkeley-based AmphiaWeb project (elib.cs.berkeley.edu/aw) to sequence four genes from each of the 524 known species of salamanders and the 168 known species of their close relative, the caecilians. The goal is to fully understand the evolutionary tree of amphibians, all the way down to its roots.