How red phalaropes end up caring for another male’s offspring

A test of the sperm storage hypothesis

January 31, 2022

In a few bird species, only the males take care of the brood. Females can then have several partners in succession and lay eggs for each of them. The sperm storage hypothesis states that females can use sperm from previous partners to fertilize eggs that are attended by their current mate. Researchers at the Max Planck Institute for Ornithology studied the red phalarope in its breeding habitat in Alaska in three summers. They found that only four percent of the young were unrelated to the male raising them. In most cases, these "cuckoo chicks" could be explained by extra-pair copulations. The storage of sperm from previous partners does not seem to play a major role.

Only less than one percent of all bird species are socially polyandrous. In this mating system, males typically pair only once with a female during a breeding season, whereas females can form pair bonds with several males. Moreover, the typical sex roles are reversed: males take care of the brood alone, while females are more aggressive and compete for mates and resources. After a brief relationship that ends when the eggs are laid, the female pursues another male who will care for eggs and young. The red phalarope (Phalaropus fulicarius) is one of these rare sequentially polyandrous bird species.

For behavioural ecologists, a polyandrous mating system is particularly interesting, because it allows testing evolutionary theory. For example, it has been shown that sexual selection through competition over mates can also act on females and is thus not linked to the sex but to the sex role. This is reflected by the plumage and the beak of the red phalarope: both are more brightly colored in females, which is why females were originally thought to be males.

Despite their intriguing behavior, red phalaropes have rarely been studied. An older study on the polyandrous spotted sandpiper (Actitis macularius) concluded that polyandrous females store sperm from previous partners for up to 30 days and use it to fertilize eggs from the clutch of a subsequent partner. Scientists led by Bart Kempenaers studied the red phalarope over three summers in its breeding habitat in Utquiaġvik, Alaska and found little evidence to support this sperm storage hypothesis.

To test the hypothesis, the scientists captured all red phalaropes as soon as they arrived at the study site from their wintering grounds. They marked each bird with an individual combination of color rings for easy identification in the field, and took a small blood sample for paternity analysis. During the courtship period, the researchers observed the birds' behavior, and noted which individuals mated with each other. After the female laid the fourth and final egg in the nest, which is nothing more than a small depression in the tundra, the research team exchanged the real eggs for plastic replicas – an indistinguishable difference for the caring male. The real eggs were incubated in the laboratory so that a drop of blood could be taken for paternity analysis from each newly hatched chick. Chicks where then returned to the father's nest, who took care of them without further ado.

Based on the combination of behavioral observations and paternity analysis, the researchers were able to gain surprising insights. "Interestingly, we found that only about seven percent of the observed females were polyandrous – much less than originally assumed. The majority of females laid eggs for only one partner in a breeding season and they didn`t have the opportunity to form further pair bonds," explains Johannes Krietsch, lead author of the study. One reason for this could be the short Arctic breeding season. In two of the three years, increased snowfall resulted in a longer period of snowmelt so that breeding habitat remained unavailable until late in the season. With a restricted time window, only few females were able to acquire multiple mates and lay eggs for them.

The researchers also found that four percent of the offspring were not fathered by the care-giving male. However, these "cuckoo chicks" were rarely fathered by a previous mate and hence the study largely rejects the sperm-storage hypothesis. Rather, the pair bonds of polyandrous females appear to be highly dynamic and overlap more than previously thought. While the female is still laying eggs for her current partner, she already starts meeting with potential future mates. In addition, the female typically copulates with several males before establishing a new pair bond. "We also observed that females and males have an opportunity to cheat on their partner from time to time, even though the members of a pair guard each other intensively," says Bart Kempenaers. "These observations suggest that eggs in a clutch can come from different fathers without the need to store sperm for a long time," adds Johannes Krietsch. Next, the scientists want to evaluate extensive GPS data to analyze mutual mate guarding in more detail.

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