Nude Revelations: A few surprises in nudibranch behavior by MENNO SCHILTHUIZEN

I once watched an Irish mollusk researcher, in a fit of slug chauvinism, try to convince an audience of biologists that slugs are superior lab rats. “Behaviorally speaking, a slug is basically a rat,” he told them. “Cover a rat in slime, amputate its legs, pull its genitalia up behind its right ear, and film it in slow motion, and you’ve got a slug!” Where their genitalia and sexual behavior are concerned, slugs indeed are a gold mine for research, with even richer seams than Rattus norvegicus. Malacologists, mollusk aficionados, are slowly beginning to dish out the slug sex smorgasbord that lies hidden under rocks and stones, both on land and in the sea. The slugs offer tremendous surprises about how genital evolution works in simultaneous hermaphrodites. Sea slugs are perhaps best known for their wonderful psychedelic colors, especially in one particularly prominent and species-rich group, the so-called nudibranchs. Nudibranchs — “nudis” to friends — are named after the gills (branchia) that many species carry uncovered (“nude”) on their backs. One of the more modestly colored nudis is Aeolidiella glauca, a species that inhabits the cold shallow-water eelgrass beds along the shores of Northern and Western Europe. (Although A. glauca is not found in the Bird’s Head Seascape, other members of the genus Aeolidiella are found throughout Indonesia.) They prey on small sea anemones, and they carry frills along their flanks in which they store the stinging anemones’ venomous nettle cells, appropriating them for their own defense. But that’s neither here nor there. I mention A. glauca because it is one of the few nudibranchs — out of the more than 3,000 species that are known — that have had their sexual behavior properly studied. We can credit our current knowledge of A. glauca to marine biologist Anna Karlsson, now a senior marine environmental analyst for the Swedish government, and zoologist Martin Haase of the University of Greifswald in Germany. Back in the late 1990s, Haase explains as I chat with him in the office he shares with his wife, ornithologist Angela Schmitz-Ornés, his boss ran into Karlsson, then a PhD student at Uppsala University, at a conference and invited her to join forces with Haase. She was a novice investigator of reproductive biology in this common marine nudi, he a skilled anatomist of mollusks willing to try his hand at something new. Together they embarked on a series of discoveries that had their jaws dropping. And dropping. “Everything the church forbids is present in this species!” Haase exclaims.

A. glauca sex goes like this. When a randy individual runs into a potential partner, it starts tailgating it. Sooner or later, the object of its love will turn around and face its suitor. Within a minute, this face-to- face phase then merges into “sidling” — the pair sliding past each other’s right-hand flank, where the genital openings are. If necessary, the more eager of the two will nibble at the other’s genital opening. First anchoring themselves together using flaps around their genital openings, the slugs then both produce their huge penises. Haase and Karlsson were surprised to discover that the slugs don’t insert these into each other as most other sea slugs do — the organs are too large for that. Instead, they each release a sausage-shaped spermatophore from the penis, which they carefully place on each other’s back. Then they lift their penises and tap down on the spermatophore several times, as if to hammer it firmly in place. Usually both slugs accomplish all this in perfect synchrony. This phase of sperm transfer lasts only a minute or two, after which the two slither their separate ways. The real magic starts only once the mate has left. Within a few minutes, a slug with a spermatophore on its back will crane its head around over its right ‘shoulder’ to reach and then eat part of the spermatophore, which increases the distance between the genital opening and the spermatophore. Then it waits. Some three hours later, a thin file of sperm is seen to begin to break free from the spermatophore and to start marching over the slug’s skin toward its genital opening. The sperm being tiny, it takes several hours for them to reach their destination, despite the fact that the column takes shortcuts by swerving between the nettle-cell-containing lobes on the slug’s back. The slug is not a passive bystander to the sperm parade on its back. It seems to monitor the progress closely, and when it decides that enough sperm have entered its genital opening it will interrupt the flow by sucking up the sperm from its back. “You can really watch that!” Haase says. Then, its stomach full of hapless sperm, it will begin laying eggs, using the sperm that it did not eat up to fertilize them. Haase goes on: “I even watched two animals that interrupted the sperm with their mouths, then started to lay a batch of eggs, and when that was finished resumed sperm uptake from the thread that was still traveling across their back.”

More recently, in 2012, details in another nudi, the Indo-Pacific species Chromodoris reticulata, revealed other distinctive traits. (C. reticulata is commonly encountered throughout the Bird’s Head Seascape.) Japanese researchers discovered that, though this species copulates in a more conventional way (penis in vagina), after mating the penis drops off, only to be replaced by a spare length of penis that the animal keeps coiled up inside its body. The coil is long enough for three matings before the whole system needs to be regrown. Nobody understands yet why such a throwaway penis evolved, but since sperm were found snagged by the barbs at the end of the penis, it may be a way to remove and then discard sperm from previous mates. Sea slug sex is sure to come up with even more surprises. The genitals of hermaphrodites are every bit as weird as those of “regular” animals. In fact, they are often even weirder and more exaggerated. Although every amorous slug (and many a snail) is wired the same way as its mate, this does not lead to mundane sex. Quite the contrary: since each prefers the male role, they have evolved a whole battery of tricks to bring out, as it were, the feminine side of their partner, to persuade the other to be the one that accepts more sperm. The outcome of this struggle shows what sexual selection can do to the evolution of a species.

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By Menno Schilthuizen

MENNO SCHILTHUIZEN is an ecologist and evolutionary biologist based at Naturalis BiodiversityCenter in Leiden, the Netherlands. This article is adapted from his new book, Nature’s Nether Regions: What the Sex Lives of Bugs, Birds, and Beasts Tell Us About Evolution, Biodiversity, and Ourselves
©2014 Menno Schilthuizen, by arrangement with Viking, a member of Penguin Group (USA) LLC, a Penguin Random House company.

To read more click here, Menno’s blogs .  Follow him on Twitter @schilthuizen

This article originally appeared in the July/August 2014 edition of Natural History magazine. Reprinted with permission of the author.