Every winter, something remarkable happens off the southern coast of Australia. In a confined area of Spencer Gulf known as Black Point, thousands of animals brave the cold, and the rocky reefs, and the pounding surf and tides to obey Nature’s prime directive – they come to breed. The animal in question is the cuttlefish, specifically the giant Australian cuttlefish, Sepia apama, the largest cuttlefish in the world. Cuttlefish are cephalopods, like octopi and squid. To the untrained observer, they look like a cross between those two relatives having roughly the body shape of the octopus, but the arm-and-tentacle arrangement of the squid. Cuttlefish are differentiated from their cousins by the ‘cuttlebone’, an internal shell all of the their own making.

A male giant Australian cuttlefish. Credit: arkive.org

Most cuttlefish breed opportunistically whenever they happen to chance upon a member of the opposite sex during their oceanic travels. But the giant Australian cuttlefish prefers to spawn in massive aggregations of thousands of individuals. Every year, between April and August (the Australian winter), they travel from their feeding grounds to aggregate at a few breeding locations on the Australian coast. And that’s when the trouble starts.

Cuttlefish males outnumber females by 4:1. This is great for the females, they get to be extremely choosy, and ensure their eggs are fertilized by only the highest quality males. But it’s a lousy deal for the guys, and leads to intense competition between the males to impress the females. The big, strong males have it easy. They quickly find a female (or three), and follow them closely, aggressively chasing off any pretenders to the throne. If the female is suitably impressed, she and the male will line-up head-to-head, and wrap their arms around one another. Then the male will transfer his spermatophore (a portable sperm packet) to the female, and she will use it to fertilize her eggs.

Romantic.

But what about the little guys? Male cuttlefish vary widely in size, and only the large, strong males can successfully chase off other males. The smaller, weaker males have to adopt a different strategy. They have to be smart.

Some of the little males are stealthy. They wait until a large male is distracted by competitors, and then swoop in to a woo the momentarily-abandoned female. Others are sneaky. Females lay their eggs in holes underneath rocks on the sea floor. The holes are too small for the large males to enter, but the small males can fit. Small males will hide in the holes and wait for a female to come and scout for egg-laying opportunities, before seducing her while the large male flits about nervously outside, oblivious to the cuckoldry.

Variation in cuttlefish size. Credit: arkive.org

Another group of the little males have adopted disguise as their method of seduction. The skin of cuttlefish is covered in cells called chromatophores. These specialized skin cells, controlled by the brain, allow the cuttlefish to change its skin colour, like a chameleon. Beneath the chromatophores there are two other skin layers, the iridiphores and leucophores, that let cuttlefish’s skin to take on a metallic sheen. Under normal conditions this colour changing ability is used as camouflage and as a type of language – the cuttlefish change the pattern and colour of their skin to communicate with one another. But some groups of males co-opt it for disguise.

The skin patterns of male and female cuttlefish, particularly at the mating aggregations, are distinct. It’s easy to tell a male and a female apart – most of the time. One group of little males, however, change the balance. They alter their skin patterns to mimic females. Only the smallest males do this, but it works to great effect. The real females (perhaps being smarter) see right through the charade, but it fools the large males. They think they’ve hit the jackpot – they only had one female, but then a second one just appeared! And it’s staying close! Sure, it’s a little small, and not too receptive to mating attempts, but that’s okay, two females is better than one.

On left is a female cuttlefish, and on the right is a male mimicking a female. Two large males stand guard. Credit: Fred Bavendam.

Until the large male is looking the other way, and the mimic secretly mates with the real female.

These mating tactics are determined by the size of a male. If he happens to be small one year, he may be sneaky or act as a mimic, but the next year, if he has grown, he may act aggressive. But they’re all viable routes to reproduction. Because the ratio of males to females is 4:1, the females hold most of the power. They’re able to be picky about which male they ultimately decide to mate with, and many of them choose the small, sneaky males – preferring brains over brawn.

This type of behaviour is not uncommon across the animal kingdom. Large, aggressive male dung beetles imprison females deep in burrows and block the entrance with a dung ball. The male then sits just inside the burrow, and fights off any other male until the female is ready to mate. But small, sneaky males bypass the guard post completely by digging a new tunnel into the burrow, before cuckolding the guarding male.

Two morphs of male dung beetle. One fights for females (R), and the other is sneaky (L).

In the common side-blotched lizard, a small lizard native to the Pacific coast of North America, males come in three colours: orange, blue, and yellow. The orange males are ultra-dominant. They secure a large territory, containing multiple females, and chase off rival males. The blue males are smaller and less vigorous, and usually mate monogamously – they hold small territories, capable of supporting only one female. Yellow males are sneaky. Their colouration resembles adult females, and they travel with impunity through the territory of orange males, mating whenever the orange male’s back is turned (and sometimes being forced to demure in the face of advances from over-eager orange males).

Lizard rock-paper-scissors. Credit: Science4All

The three colour morphs operate in a rock-paper-scissors way towards one another. Orange males can steal females from blue males, but are vulnerable to sneaky yellow males. Blue males can lose their mates to orange males, but aren’t fooled by yellow males and will work together with other males to chase away yellows. Yellow males can trick orange males, but are caught-out by blue males. Because of the relationship between the three morphs, every year the rarest morph in the population is likely to have the greatest reproductive success. This ensures a stable equilibrium over time – all three morphs will always be present in the population, because the rarest one is favoured. There’s always hope for the little guy.

Neil Griffin

Literature Cited

Alonzo, SH and B Sinervo. 2001. Mate choice games, context-dependent good genes, and genetic cycles in the side-blotched lizard, Uta stansburiana. Behavioral Ecology and Sociobiology 49: 176-186.

Hall, KC and RT Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Marine Biology 140: 533-545.

Hanlon, RT and JB Messenger. 1987. Adaptive coloration in young cuttlefish (Sepia officinalis L.): The morphology and development of body patterns and their relation to behaviour. Phil. Trans. R. Soc. Lond. 320:437-487.

Hanlon RT, Naud MJ, Shaw PW, and JN Havenhand. 2005. Behavioural ecology: Transient sexual mimicry leads to fertilization. Nature 433, 212