The sex life of treefrogs: how females build better nests by mating with multiple partners

African grey foam-nest treefrogs (Chiromantis xerampelina) are common across the savannahs and dry forests of south-eastern Africa. Despite their unremarkable outward appearance, these small animals display some of the most intriguing reproductive behaviours known to science. Most notably, the females are highly polyandrous, constructing elaborate foam nests and mating with many different male partners in a breeding season.

Until the 1990s, evolutionary biologists thought that polyandry was extremely rare in nature. Having one mating partner, monandry, was considered to be the norm. However, with the advent of molecular techniques for testing paternity, it quickly became apparent that females across a diversity of animal groups (from bed bugs to blue whales) routinely mate with multiple males during a breeding season. Understanding the benefit of polyandry rapidly became a profound evolutionary puzzle.

Over the past few decades, observational and experimental research by behavioural ecologists has shown that polyandrous females can benefit in many ways. Mating with multiple males may ensure eggs are fertilised, ensure extra nutrients or paternal care for offspring, or increase the genetic diversity of offspring, making them more resilient to future challenges.

Our recent paper introduced a new idea, the “nesting-assistance” hypothesis, as a novel explanation for the evolution of polyandry.

Our team (composed of four prominent herpetologists with expertise in behavioural ecology, evolutionary biology and molecular ecology) theorise that in species where females are primarily responsible for nest construction, and males display some form of nesting assistance, mating with multiple males leads to the production of more viable nests and improved offspring survival or performance.

By studying the reproductive behaviour of a wild population of African grey foam-nest treefrogs for an entire breeding season, we obtained strong support for the “nesting-assistance hypothesis”. As predicted, extra males helped polyandrous females to build a better nest, giving tadpoles a much greater chance of surviving until they hatched.

The mating process

In African grey foam-nest treefrogs the mating process is a protracted and captivating affair. Come hot and steamy summer nights in the wet season between October and February, females begin their reproductive quest by climbing onto tree branches overhanging water. Once a suitable site is chosen, they build a foam nest into which they lay hundreds of eggs.

For the eggs to be fertilised, females must engage with a male and receive sperm over the five to six hours that it takes to build the nest. This is where things get interesting. While some females mate with just one male during this period, most will attract and mate with multiple partners, and all at once.

A female typically mates with five males simultaneously, although groups of 10 to 15 are not unusual. Scientists call this mating system “simultaneous polyandry”.

Female foam-nest treefrogs build their nests by mixing water with secretions from their reproductive tract and whipping the mixture into a dense foam using their hind legs. The finished nest protects eggs from the intense African heat for almost a week until the tadpoles hatch and drop into the water below. However, if the foam dries out too quickly the entire clutch dies.

Tree frogs calling. Author supplied 403 KB (download)

By analysing , we found that males didn't simply fertilise the eggs, they also helped to build the nest. During polyandrous matings, several males synchronised their hind-leg movements with the female, and the level of synchrony and churning effort was higher when more males were present. This led to the construction of larger nests that retained moisture for much longer than nests built by a single male and female (monandrous pairs).

The difference had a massive effect on the parents' reproductive success. Small nests produced by monandrous pairs almost always dried out before the tadpoles hatched, whereas the larger nests built with help from several males were far more likely to remain viable. While polyandrous females benefited by producing more surviving offspring, participating males were rewarded by gaining a share of paternity.

Nesting assistance and polyandry in other species

Across a diversity of invertebrates and vertebrate species where multiple paternity has been reported, males have been observed to show some form of direct or indirect “nesting assistance”. This ranges from males helping to collect and deliver nesting materials through to males investing heavily in excavating nest sites and/or building nests. At present, there is anecdotal evidence for male nesting assistance in solitary bees and wasps, various bird species, sediment and cave-spawning fishes, canids (Arctic foxes and gray wolves) and new-world monkeys (tamarins and marmosets).

Yet, behavioural ecologists have completely overlooked the possibility that help from “male builders” could supply females with a direct benefit that favours polyandry. That is, nobody has previously checked whether more offspring survive when males help build nests. Given this knowledge gap, we now strongly encourage additional tests of the “nesting-assistance hypothesis” across a diversity of animal groups.

We forecast that by enlisting the help of multiple “construction workers”, females in various species might benefit from “home improvements” that elevate the survival and/or performance of their offspring. If this proves to be true, “nesting assistance” may be an important yet currently overlooked explanation for why polyandry is so widespread in nature.

Phillip Byrne receives funding from the Australian Research Council (ARC)

Aimee Silla receives funding from the Australian Research Council (ARC).

By Phillip Byrne, Associate Professor School of Earth, Atmospheric and Life Sciences (SEALS), University of Wollongong And

Aimee Silla, ARC DECRA Fellow School of Earth, Atmospheric and Life Sciences (SEALS), University of Wollongong