Why are some fathers left holding the baby?

Sex-role reversal in the animal kingdom, where it’s the father, not the mother that takes care of its young has mystified researchers since Darwin. But new research at Bath and Sheffield Universities may shine light on this biological puzzle

One of the principle patterns of animal social behaviour is that males compete for females whereas females look after the young. In a number of insects, fishes and birds, however, these conventional sex roles are reversed: the males look after the eggs and young, whereas the females compete for males. In the latter species the females are often larger, more ornamented and more pugnacious than the males, whereas the males may have specific adaptations to look after the offspring. These sex role reversed species have caught the eyes of various naturalists including Charles Darwin since they appear to defy behavioural features that are often associated with “maleness” and “femaleness”.

Why sex role reversal evolved has puzzled sociobiologists and evolutionary biologists ever since Darwin, since it is not clear what ecological and life history variables have triggered the conventional sex roles to flip into sex role reversal. A large number of hypotheses have been proposed, for instance food availability may be limited for the female so that she is exhausted by producing the offspring, and thus she delegates the caring role to her mate so that she can replenish her resources. The empirical evidence, however, is scant for all of these hypotheses, since no environmental or life history variable has been found that would consistently distinguish the conventional species from the sex role reversed ones. Indeed, conventional and sex role reversed species often breed side by side in so contrasting habitats such as tropical marshes and Arctic tundra where they must share much of the ambient environment.

Recent theoretical models, however, emphasise the impacts of social environment on sex roles. Theory predicts that when there are many males in a population, the female should capitalise from the enhanced mating opportunities and abandon her family to seek out a new partner. For the male, however, the best is to stay with the offspring. The male behaviour has nothing to do with sacrificing his own Darwinian fitness for the sake of his partner: he would simply face stiff competition should he leave her and the offspring. Therefore, the best option for a male at male-biased sex ratio is to stay put and make most out of his existing family.

We recently tested these propositions using shorebirds (plovers, sandpipers and allies) as model organisms1. Whilst no shorebird has been studied to the same details as any of the traditional genetic or developmental model organisms (e.g. domestic mouse, zebra fish, fruit fly or Caenorhabdis elegans), shorebirds have an immense advantage over the latter model organisms having extremely variable sex roles that are well documented in nature. Shorebirds have diverse and well-studied courtship behaviours, and their body size dimorphism – an indicator of sexual selection – ranges from male-biased size dimorphism to female-biased size dimorphism. In addition, most shorebirds breed in open habitats that can be easily surveyed and therefore, assessing their social environment is less error prone than in other species that breed in dense habitats or in places that are difficult to access.

As theory suggested, we found strong relationships between adult sex ratio (an indicator variable of social environment) and sex roles. In populations where males outnumbered females, sex role reversal was common: the females competed for males whereas the males looked after the young. In female-biased populations the opposite pattern prevailed: the males competed for access to females, and the females looked after the young. These phylogenetically controlled results were robust to different phylogenetic hypotheses, and remained persistent in sensitivity analyses.

These exciting results have implications beyond birds, and suggest that adult sex ratios may influence courtship, mating and parenting behaviour in many organisms including humans. For instance, with increasing bias toward more men in the population, one may expect increased social pressure by unmated males since seeking out and competing for females often result in violence. Females may also respond to biased adult sex ratios by being more demanding in partnering relationships given that they have more man to choose from.

The study raises two intriguing questions. First: how does biased adult sex ratio emerge in the population? Adult sex ratios have not been studied in vast majority of organisms, and to answer this question one needs to investigate the genetic, developmental and physiological mechanisms that create male-biased sex ratios in some populations whereas in others female-biased sex ratios. Pilot studies from birds, fish and mammals suggest that closely related species can exhibit vastly different adult sex ratios, and these different sex ratios may have immense impact on social behaviour. Second: is the observed relationship between sex roles and sex ratios indirect and does it emerge via numerous incremental steps, or a direct (causal) relationship? To test the latter proposition one needs to manipulate adult sex ratios experimentally, and find out how the shift in sex ratio induces courtship behaviour, mating systems and parental behaviour.

Taken together, the recent work by Liker et al. has opened a Pandora’s Box in social evolution by showing that adult sex ratio predicts sex roles in birds. Further studies are urgently needed to establish the causes of adult sex ratio bias in natural populations, and to explore the full implications of sex ratio bias for social behaviour including pair-bonding, courtships and parenting.

 

Reference

1. Liker, A., R. P. Freckleton & T. Székely. 2013. The evolution of sex roles in birds is related to adult sex ratio. Nature Communications (in press).

Author: Tamás Székely Department of Biology and Biochemistry, University of Bath. Tamas is an evolutionary biologist interested in evolution of social behaviour. His team is investigating mating system and parental care in birds.

Contact:T.Szekely@bath.ac.uk