Drop dead! Female mate avoidance in an explosively breeding frog

New research on European common frogs, published in Royal Society Open Science, shows that females can avoid males. Previously thought to be passive, explosive breeding frog females show active strategies to escape unwanted attention. We spoke to the authors, Dr Carolin Dittrich and Dr Mark-Oliver Rödel, to learn more. 

How did this study come about? 

Breeding within this amphibian species usually takes place in early spring within a few days to two weeks, depending on weather conditions. This means that hundreds of individuals gather at the pond at this time. The males fight for access to the females, which are usually the rarer sex in these breeding aggregations. It was previously thought that females were unable to choose or defend themselves against this male coercion. 

In a previous study we found that pairs were size sorted so that females and males that formed a couple were of similar size. This made us think that male selection might be a reason for this pattern. From an evolutionary point of view, this would make sense, as larger females would have more eggs, which would be an advantage in terms of number of offspring and passing on their genes. To test this hypothesis, we conducted mate choice tests in which a male could choose between two females of different sizes. We found that males do not choose a female based on her body size. In the videos we made of this experiment, we then detected the female mate avoidance behaviour that we describe in the current paper. This was not expected based on the previous belief that females in these breeding aggregations were passive. 

Were there any surprising findings in this study? 

As mentioned above, females in this species are thought to be passive during mating, so we did not expect to see any of the described mate avoidance behaviours. 

The most common behaviour was turning, where a female tries to turn on her own axis to escape the male's grip. The second behaviour was calling. Females produced two different calls, a deeper, low frequency 'grunt' sound, which is an imitation of the male's release call (when a male is grabbed by another male, they give this release call, it signals that it is a male) and a higher frequency 'squeak' sound, where we are not sure what the communication signal is. The final and most astonishing behaviour was tonic immobility, where females stiffly extend their arms and legs away from their body. 

Tonic immobility in the context of mating is quite unusual or probably less frequently observed. We know of only a few studies where tonic immobility has been found in a mating context, for example in spiders or dragonflies. Traditionally, it is thought to be a predation avoidance strategy, as many predators depend on the movement of their prey. Detectability is reduced when individuals are immobile. In the literature, tonic immobility is described as a “defence of last resort”. This immobility can last several minutes. On one of our videos, we saw that a male is dragging an immobile female until he lets her go. She stayed in that immobile position for a couple of minutes until she turns and swims away. 

What was your experience like publishing with the Royal Society Open Science? 

The overall experience of publishing with Royal Society Open Science has been very positive. The peer review process provided constructive feedback on some aspects of the study and improved the quality of the paper. In addition, the Subject Editor and Associate Editor were very helpful and supportive. Through the Read and Publish licence, the financial part was easily resolved with our home institution's library staff. The media response to our article has been overwhelming and we are very grateful to the Royal Society Open Science for promoting our article. 

What is next for your research? Where would you like to see this field in the future? 

In our specific species, the European common frog, females can only increase their reproductive fitness by participating in mating over several breeding seasons, so the selective pressure to survive the breeding season should be very strong. Although we did not test this hypothesis, there is literature suggesting that younger females may be more stressed during this breeding period. 

We think that these mate avoidance strategies are due to a stress response that females experience during this time. It may be that younger females are less experienced and the strong stimulus of males clinging to them leads to the tonic immobility we observed more often in smaller females. 

Larger females are older and may have previously participated in breeding. It may be that they are less stressed (although this has not yet been tested) and therefore show less avoidance behaviour. For example, larger females call more often when grabbed by a male. They use an imitation of the male's release call, which is usually produced when a male grabs another male. We think that larger females may be better able to defend themselves against male attempts to grab them, and that they may be more experienced at mating in general. 

These hypotheses have not yet been tested but would be very interesting and could enrich some aspects of how we perceive sexual conflict and the role of experience and age. 

We assume this behaviour to occur in other frog species that experience similar selection pressures of dense breeding aggregations, skewed sex ratios and a short breeding season. If there is strong selection pressure for access to the rare sex, which includes fighting in the more common sex and the possibility of death, mate avoidance strategies could increase the chances of survival for the rare sex. This may also be possible in other animal groups, and a thorough review of the available literature and extensive studies involving different sex ratios and age classes might be worthwhile! 

In general, I (Carolin) would like to see more female perspectives in sexual selection research, but I think we are well on the way to including this important aspect more in the future. 

About the authors 

Dr Carolin Dittrich, Konrad Lorenz Institute of Ethology, University of Veterinary Medicine, Vienna 

This work was part of my PhD project at the Museum für Naturkunde Berlin, where my research interests focused on sexual selection and reproductive behaviour. In other projects I have investigated adaptation to climate change and tested new methods for the detection of wild collected frog legs in international trade. My current postdoc in Vienna has given me further insight into the field of ecological and evolutionary genomics. This is a promising technology that gives me the opportunity to look at the evolutionary forces behind some behaviours. 

Dr Mark-Oliver Rödel, Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Berlin 

My main research interest is focusing on species‘ and species assemblages reactions to environmental change, usually using amphibians as a model system. In my lab we are for instance studying the effects of logging of tropical rainforests on frogs and frog communities, including aspects such as differences between logging techniques, forest types and the potential of used forest ecosystems to recover. Currently I am particularly involved in researching if and how species-interactions (re)establish along a recovery gradient from pasture to mature rainforest in western Ecuador. Our studies also involve long-term (monitoring) projects such as on the European Common Frog or on a viviparous toad species in western Africa. It is often these long-term projects where we gather unexpected biological insights that open new views on even ‘well-known’ species, such as in the paper we just published in your journal.

Royal Society Open Science is an open access journal that welcomes the submission of all high-quality science. More information about the journal and the submission process can be found on our webpage. 

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Image credit:davemhuntphotography, iStock.