Same-Sex Squid Sex

Hoving HJT, Fernández-Álvarez F, Portner EJ, Gilly WF (2019) Same-sex sexual behaviour in an oceanic ommastrephid squid, Dosidicus gigas (Humboldt squid). Mar Biol 166(3):1–7.

An Evolutionary Paradox

Same-sex sexual behavior, i.e. male-male or female-female mating, has been reported across a wide range of species in the animal kingdom. In fact, just among octopus and squid this behavior has been documented in six different species. The observation of this kind of mating behavior is no longer surprising, but what does still continue to puzzle scientists is the apparent paradox of same-sex mating. The purpose of mating, evolutionarily, is to produce offspring. By definition, same-sex mating cannot produce young. Thus, there is a cost to mating behavior that does not result in offspring because sperm and energy are used without any evident advantages. So why does this behavior exist in so many animals?

Evolution by natural selection implies that all animal behaviors should have some adaptive value that helps the animal. It’s likely that same-sex sexual behavior has evolved separately in different species and that it exists for different reasons in animals with different mating strategies. For most animals, we still don’t know for sure what the different reasons are for animals to exhibit seemingly paradoxical reproductive behavior. In a recent article, researchers documented this evolutionary paradox for the first time in the Humboldt squid (Dosidicus gigas) and they postulated what benefits same-sex sexual behavior might have for this species that outweigh the costs.

A photo of a Humboldt squid captured in Cordell Bank National Marine Sanctuary in 2005 at a depth of about 820 feet (250m). Source: NOAA/CBNMS

Jumbo, Flying, Red Devils

Humboldt squid are a large species found in the open ocean habitat of the Pacific. Individuals often grow up to six feet long and weigh 110 pounds. These huge squid also have the ability to light up with red and white light. Thanks to these bioluminescence skills and their aggressive behaviors, Humboldt squid have earned the nickname red devils. As if that weren’t enough, these squid are one of a few species who have been observed rapidly propelling themselves out of the ocean, where they seem to fly through the air.

It’s pretty difficult to tell Humboldt squid males from females, except for the fact that mature females are usually somewhat bigger than mature males. A small subset of the population of red devils, however, has been found to be small at the time when they become mature and are ready to mate. This group of small squid make it even harder to tell males from females, as both sexes are approximately the same, small size. In investigating same-sex sexual behavior in Humboldt squid, researchers suggested that these small males may be mating with other small individuals, regardless of sex. All of the small, mature individuals, males and females, look nearly identical. So is this, as the scientists ask in their recent paper, a case of “mistaken identity?”

This Humboldt squid was observed in a swarm of individuals and “greenish-gold ink” the squid had emitted. This individual is about 3-6 feet (1-2m) and was seen off northern California. Source: NOAA/MBARI

Small is the new sexy

The researchers found male-male matings had occurred in roughly 20-60% of individuals surveyed across the three years of their study, so this behavior is far from rare. It does seem, however, that this behavior is more common in small males than it is in large males. If size is the primary determinant of same-sex sexual behavior in Humboldt squid, the evolutionary hypothesis points to a tradeoff between the energy expended in mating behavior that doesn’t result in offspring and the energy expended in trying to tell the difference between nearly identical individuals of different sexes. This sort of tradeoff is described by the authors as a non-adaptive trait, meaning that there are no direct benefits, there are simply no significant costs.

But why not mate with large individuals that are more certainly mature females? Why are small Humboldt squid mating with individuals that are the same size as them? More specifically, why are small males trying to mate specifically with small females (and incidentally mating with small males as well in the process)?

It’s possible that males who mate with recently matured females, who are also smaller, are more likely to experience successful fertilization. Female Humboldt squid are able to mate with multiple males and store the sperm in receptacles. But if a male mates with a recently matured female, he may be able to fill her receptacles with his own sperm preventing future males from successfully mating with that female.

 Another possibility involves a darker twist in this story – Humboldt squid are also known cannibals. Larger female Humboldt squid have been known to cannibalize smaller individuals, so by mating with a large, mature female, male squid are also putting themselves at risk of being eaten. Given the choice of being eaten by a large female squid or mating with a small squid of ambiguous sex, the small squid seems to be the way to go. Accidentally mating with a male is a far better outcome than becoming a large female’s next meal. 

Both sexes of Humboldt squid look very similar, they mate for very brief periods, live in groups, and have shown evidence of cannibalism. Because of these characteristics, the species may have evolved to mate indiscriminately with other individuals which are the same size as they are. Thus, small males may be preferentially mating with smaller females and end up mating with other males, a behavior which has very little cost compared with the benefits of many mating events. It’s very likely that same-sex sexual behavior is not a trait that all squid species have, and that the reasons for same-sex sexual behavior’s evolution is different in different species. As we continue to learn more about the mysteries of life in the ocean, we will continue to encounter evolutionary paradoxes and the fascinating ways in which animals have been uniquely molded to best fit their habitat and lifestyle.

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