A male giant Australian cuttlefish, Sepia apama, (on left) mate guarding a female cuttlefish. Photo credit: Alistair Merrifield
Whether in combat with a rival male or canoodling with a female, most male cuttlefish show a bias to the left. These left-biased cuttlefish are more likely to be better lovers but less likely to be successful fighters, whereas right-biased cuttlefish are likely to show contrary patterns.
Behavioural biases are common in nature, with animals ranging from bees and octopuses to parrots and whales showing evidence for favouring one side over the other for specific tasks. Such biases are thought to have evolved because they often result in advantages, making individuals better at certain tasks. However, it is less clear why many populations have unequal numbers of left- and right-biased individuals. For example, 90% of the human population is right-handed!
Our new study, conducted on giant Australian cuttlefish, Sepia apama, shows that benefits that occur during fighting and mating might be driving this phenomenon. We used a game theory model to test whether unequal numbers of left- and right-biased cuttlefish can reach an equilibrium – a stable, but unequal, percentage of left- and right-biased individuals – based solely on fitness consequences incurred through interactions between members of the same species.
The specific model that we tested, termed the competition-coordination model, predicts that minority-type individuals exist because they are more likely to adopt unpredictable behaviours during competition such as fighting. The model also predicts that majority-type individuals exist because there is a fitness advantage in having their biases synchronized with other individuals during behaviours that require coordination such as mating.
Using observations of cuttlefish in the wild and in the laboratory, we showed that during fighting males with a left-eye bias (i.e. favour approaching rivals with their left eye) showed higher contest escalation; but minority-type individuals with a right-eye bias achieved higher fighting success. Such patterns are thought to emerge because minority-type individuals might hold an advantage in competitive interactions since they are more likely to surprise opponents with unpredictable and unfamiliar motions and tactics. This phenomenon has been observed in human sporting activities. For example, Southpaws, left-handed boxers, are likely to throw unexpected punches, and often catch their boxing opponent by surprise.
In contrast, we found that during mate guarding and mating attempts, male cuttlefish with a left-eye bias (i.e. favour keeping females on their left side) achieved higher mating success compared to right-biased males. This bias in male cuttlefish might be mediated by the behaviour of the female, as females were more likely to accept a mating attempt if a male approached her right side. At the same time, the bias might be influenced by an anatomical asymmetry, as male cuttlefish transfer spermatophores, small sacs of sperm, through a single specialized arm on their left side. Consequently, approaching a female’s right side may increase coordination during the transfer of sperm from his arm into her buccal cavity.
This is the first study to provide support for both predictions of the competition-coordination model, supporting the idea that fitness consequences involved in fighting and fornicating might be driving a stable but skewed number of lefty and righty males in a population. It is important to point out, however, that the observed fitness advantages are dynamic and dependent on the frequency of lefties and righties in the population. As right-biased males become more common in a population, they will likely lose their unpredictable advantage during a rumble.
Reference: Schnell A.K., Jozet-Alves C., Hall K.C., Radday L. & Hanlon R.T. (2019) Fighting and mating success in giant Australian cuttlefish is influenced by behavioural lateralization, Proceedings of the Royal Society B, 286: 20182507.