African Grey Foam-Nest Treefrogs (Chiromantis xerampelina) are unremarkable in their physical appearance. In fact, given their ability to effectively blend into their background and hide from predators, they are difficult to even see. This somewhat plain first impression belies a spectacular mating system, and some of the most intriguing reproductive behaviours known to science. Come hot and steamy summer nights across the savannahs and dry forests of south-eastern Africa, females begin their reproductive quest by tenaciously climbing onto tree branches overhanging water. Once a suitable location is identified, females quickly commence the construction of a foam nest into which they lay their eggs. During the nesting process, each female must be embraced by a male (amplexus) and receive a delivery of sperm needed to fertilise the egg clutch. This is where things get interesting! While some females engage with just a single partner during nest construction, most will mate with many males. On average, a female will mate with five males at once, but it is not uncommon to see females mating with between 10 and 15 different males. Scientists refer to this mating system as 'simultaneous polyandry', and studying such systems has shed new light on the process of sexual selection and how reproductive behaviours evolve.
How common is polyandry in nature?
Until the 1990s polyandry was thought to be extremely rare in nature, with monogamy considered to be the norm. However, with the advent of powerful molecular techniques for testing paternity, it became increasingly apparent that multiple paternity was extremely widespread. Across a diversity of taxa, ranging from bed bugs to blue whales, evidence quickly grew that females were routinely mating with multiple males during a breeding season. Given females typically invest far more in reproduction than males, and that mating carries high costs (such as increased exposure to predators and disease), the adaptive benefit of polyandry quickly became a profound evolutionary puzzle.
What are the adaptive benefits of polyandry to females?
Early explanations for the evolution of polyandry centred on the idea that males might be forcing copulation against female interests (termed sexual conflict), or that females may be accepting superfluous copulations to reduce costs associated with resistance (termed convenience polyandry). While certainly true for some species, these theories were unable to explain cases where females were actively seeking multiple mating partners. Perplexed scientists became fixated on finding answers, and a wave of research followed. Through this work, we now know that a remarkable diversity of benefits can favour polyandrous mating. Females may benefit directly if mating with multiple males supplies extra nutrients that help them produce more viable eggs or offspring. The ways this can be achieved makes for some great dinner-time conversation. For example, males may provide females with nuptial food gifts in exchange for matings, or females may even have the ability to sequester nutrients from male ejaculates. Direct benefits may also flow if multiple paternity creates male confusion over paternity and lowers the risk of infanticide, or if mating with multiple males safeguards against females pairing with a male who is a poor father or has low fertility (females don't always make good choices and there are dud males in every species). Indirectly, polyandrous females may also gain benefits by elevating offspring genetic diversity and adaptability, reducing the risk of inbreeding depression or improving offspring genetic quality, viability, or even sexual attractiveness.
Do polyandrous female African Grey Foam-Nest Treefrogs gain benefits?
The benefits of polyandry in this frog are truly multifarious, with multiple-male mating known to yield both direct and indirect fitness gains. Our early research revealed that polyandrous females were ensuring the fertilisation of their clutch. While polyandrous females always displayed clutches with moderate to high fertilisation success, the clutches of monandrous females often went unfertilised. This likely occurs because a high proportion of males in the population either suffer low fertility, or become sperm depleted after mating too much, a reproductive risk that is reduced when females mate with multiple males. In a follow up study, we discovered that more genetically diverse clutches produced from polyandrous matings generate offspring with a significantly higher chance of survival. In combination, these benefits could easily explain why polyandry is so strongly favoured in this frog species. Yet, the benefits keep coming. In a recent study [1] we made the remarkable discovery of a novel link between polyandry and the nesting strategy, and uncovered a new benefit to females of mating with multiple males.
Nesting assistance: a new hypothesis for the evolution of polyandry
To build their nests, African foam-nest treefrogs release a mix of oviducal secretions and water and use their hind legs to rhythmically beat the viscous blend into a foamy spherical or ellipsoid structure. During nest construction, eggs are released in discrete deposition bouts (accompanied by bouts of energetic leg churning) and are externally fertilized as they are integrated into the growing nest. Once nests are complete, the outer foam layer dries to create a rigid 'foam home' that protects developing tadpoles from the hot African sun. This home must remain viable for five to six days to allow tadpoles to hatch and drop into water bodies below, otherwise a female's entire clutch will desiccate to death. This makes the architecture and quality of a nest critical for female reproductive success. Here, polyandry plays a critical role by facilitating 'home improvement'. By analysing video recordings of nesting frogs, we discovered that males involved in polyandrous matings moved their hind legs in synchrony with bouts of female leg movement, and that there was more overall leg movement compared to monandrous matings [1]. More remarkably, matings that involved more males and leg beating led to the construction of much larger nests, and these nests were far more resistant to desiccation. The small nests built with one male almost always failed before tadpoles could hatch. As an outcome, polyandrous females had substantially more of their offspring survive through to hatching. By assisting with nest construction and helping females to produce more viable nests, males also gained a major fitness boost because they were rewarded with a share of paternity [1]. Such paternity sharing may have relaxed selection pressure for male-male competition because there was a distinct absence of physical aggression between males during mating, which is rarely seen in nature. However, this apparent 'reproductive harmony' might also be favoured because any interference with the nesting process could compromise nest viability and impose major fitness consequences upon both sexes. All the fathers behave to keep the family home intact! Beyond extending our knowledge about the reproductive ecology of an amazing African amphibian, the findings are also extremely exciting because they have precipitated the formulation of a new theory for the evolution of polyandry, one we have coined 'the nesting-assistance hypothesis'.
Could nesting assistance explain the evolution of polyandry in other species?
Most definitely! Across a diversity of invertebrate 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. Yet, behavioural ecologists have completely overlooked the possibility that help from 'male builders' could supply females with a direct benefit that favours polyandry. Moving forward, 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.
Does understanding reproductive ecology matter for conservation?
Absolutely! Amphibians display remarkable reproductive diversity. Gaining a comprehensive understanding of the reproductive ecologies of species, why each mating system has evolved, and the importance of specific reproductive behaviours to the generation of viable offspring, is fundamental to amphibian conservation. Without these insights it is unlikely that conservationists will be able to provide the social and environmental conditions necessary to successfully breed threatened species in captivity or effectively recover wild populations.
Acknowledgments
Thanks go to Dr Les Minter for guiding us to the study site, Petra Terblanch and Eilands Ecospar for providing accommodation, and Andrzej Kilian and Diversity Arrays Technology (DArT) for SNP development and genotyping work at cost. Permission for this work was granted by the Department of Economic Development, Environment & Tourism, Polokwane, Limpopo Province.
References
- Byrne, P.G., Whiting, M.J., Silla, A.J., & Keogh, J.S. 2026. 'Nesting assistance': a new hypothesis for the evolution of polyandry and a test in an African foam-nesting treefrog. Evolution qpag071. https://doi.org/10.1093/evolut/qpag071