In the early 1890s a Philadelphia naturalist named Henry A. Pilsbry set out to create a guide to the land mollusks of North America. An Iowa farm boy turned New York City proofreader turned malacologist, Pilsbry was still in his 30s but already the foremost authority in America on chitons, barnacles, and terrestrial gastropods. One obituary calls his Guide to the Study of Helices, published when he was 32, “the most brilliantly original, iconoclastic book that has ever been written about land snails.” Pilsbry would go on to describe more than 5,800 species in his career.
Among the collections he set out to work on in 1896 were a few dozen large banana slugs from Oakland. Pilsbry noticed that unlike the familiar banana slug Ariolimax columbianus—the oldest known banana slug species, which had been collected by the United States Exploring Expedition in the Pacific Northwest and first described in 1851—none of these banana slugs had penises.
That’s a significant omission in a creature known to have one of the largest phallus-to-body-size ratios on the planet. When unfurled, a banana slug’s male genitalia can stretch the full body length of a six-inch slug. What’s more, like all terrestrial snails and slugs, banana slugs are hermaphroditic. They’re all supposed to have all the parts. Pilsbry decided that he had discovered not just a new species, but a new genus of California slugs. He and collaborator E.G. Vanatta called it Aphallarion. (You know your Latin; you can figure out why.)
Twenty years later a Stanford biologist named Harold Heath was leading a dissection course for undergraduates. He liked to work with local banana slugs, which were large, easy to collect, and biologically interesting. Over a few months Heath and his students noticed that most of the slugs had penises, but about 5 percent didn’t. It was curious, Heath thought, that according to Pilsbry’s work both Ariolimax and Aphallarion lived side by side on what was soon to become the ninth hole of the Stanford golf course.
Some closely related species have a geographic barrier that separates them and explains why they have diverged through the process of evolution into separate species. But here the two slug genera were, looking identical, living on the same fairway, fulfilling the same apparent role. It was an ecological and evolutionary mystery, and Heath and his students determined to get to the bottom of it. On a foggy, drizzly morning they gathered on the Stanford campus near the edge of San Francisquito Creek. Two large slugs were out and mating. We will let Professor Heath take over here, from his 1916 monologue “The Conjugation of Ariolimax Californicus”:
Prior to the act of conjugation each individual viciously bites the side of its mate … then violently retracts the head which gradually is protruded before the next onslaught. The intensity of this first phase gradually lessens as the bodies become curved about each other … The penis of one individual only is then inserted, and after a period of several hours the two animals commence to draw apart. In both of the observed cases, when the penis had become exposed to the extent of about half an inch, one of the animals turned its head and commenced to gnaw upon the walls of the organ. … The other animal (subsequent dissection in one case showed it to be the possessor of the intromittent organ concerned) now took part in the process, and within a very few minutes the penis was entirely severed.
Heath’s banana slug sex discovery was a reasonably famous incident in field biology history. “This spread like wildfire among biologists,” says Janet Leonard, a research associate at the Institute of Marine Sciences at UC Santa Cruz. “Everybody knows about this.”
(I have now asked friends, co-workers, and dinner guests, did you know banana slugs…? Anyway, not everybody knows about this.)
Pilsbry withdrew the Aphallarion genus. In his 1948 work Land Mollusca of North America, he quoted liberally from Heath’s monologue to explain the differences between the various Ariolimax species of North America. The identification key, naturally, focuses on genital structure. “The genitalia are the key character in any of the land snails,” Leonard says.
But as it happens, slug reproductive parts turn out to be the key character in a transfixing evolutionary mystery. During the time Pilsbury completed his field guide in the 1940s through to the 2000s, the number of California banana slug species or subspecies stood at five. The original, Ariolimax columbianus, lived from Juneau, Alaska, to Monterey. A subspecies, Ariolimax columbianus straminius, lived in California’s southern counties, from Monterey down to Ventura and the Channel Islands. Ariolimax californicus lived in a narrow range on the Peninsula from Santa Clara to San Mateo counties. A subspecies, A. californicus brachyphallus, lived on the northern part of the Peninsula, in San Francisco around Mount Sutro and the Presidio, and on the Monterey Peninsula. The UC Santa Cruz mascot Ariolimax dolichophallus lived in Santa Cruz County and the western edge of Santa Clara County.
One of the things Leonard and UC Santa Cruz emeritus biology professor John Pearse were able to do in the early 2000s was revise the taxonomy based on genetic testing. They found that Ariolimax columbianus was actually two distinct species, a northern version that lived from Humboldt County to Alaska and a southern clade, Ariolimax buttoni, which lived from Humboldt down to the North and East Bay, with an isolated population in the Presidio. Pearse says they also identified two remnant species on mountaintops: an undescribed species living on Palomar Mountain in San Diego County, and an undescribed species from Fremont Peak in San Benito County. And then the weirdest thing of all—they found what definitely seems like a slug with a different kind of genital structure living on Alcatraz. Probably it’s a new species. By going through the collections of the Academy of Sciences in San Francisco, they found the same slug had been collected on Southeast Farallon Island—although, Pearse says, it is “almost certainly not there now.”
Long Latin short, we seem to live in an absolute hotbed of banana slug evolution, with potentially nine different species or subspecies of Ariolimax to be found in the Golden State. What’s going on?
Leonard, who studies sexual selection in hermaphrodites, and Pearse, an evolutionary ecologist, decided to investigate banana slug speciation. They focused on two species. Ariolimax californicus, the Peninsula banana slug, and Ariolimax dolichophallus, the Santa Cruz and Monterey banana slug, don’t overlap geographically. The line separating them seems to be drawn at Rancho del Oso in Big Basin Redwoods State Park. The two slug species have different genital structures and extremely different mating behaviors.
Yet in tests of mitochondrial DNA run by colleagues of Leonard and Pearse, the two species’ genetics turned out to be identical. Leonard and Pearse, it seems, had stumbled into slug species so newly split that their mitochondrial genetic code hasn’t had time to catch up to their divergent behavior.
Why? Leonard thinks it has something to do with the pressure of sexual selection—the idea that some evolutionary change is driven by the preferences of potential mates. “At some point,” she says, “you have an isolating event, and in one species two populations become isolated. The individuals that are particularly successful in getting mates have different characteristics in terms of their reproductive anatomy and reproductive behavior from those that are successful in the other population. That may be true in this case—it’s hard to imagine there’s some adaptive value to having a stronger vaginal musculature north of Rancho del Oso than south of Rancho del Oso.”
That’s the next big question. What could be an isolating event for two banana slug species on the Peninsula? Leonard says … it’s complicated. They’ve looked for clues in the geologic history of the Peninsula. Perhaps, Leonard says, the slug populations were separated about 15,000 years ago by rising sand dunes following rising sea levels. Ben Lomond, in the Santa Cruz Mountains, and San Bruno Mountain, on the northern part of the Peninsula, both have peaks of igneous rock. Perhaps on those two peaks, islands isolated by an uncrossable sand desert, the ancestors of the two slug species first grew apart.
Leonard and Pearse are pursuing their slug investigations along with many other things, and funding is scarce. What’s more, a key collaborator on the genetic part of the equation switched roles and isn’t available to continue the work. “Everybody thinks that because they’re a university mascot there must be funding for this, unless you work for the university in which case you know better,” Leonard says.
It is also a challenge to get past the necessity of discussing slug penises and marathon reciprocal copulations. Leonard says she generally introduces the whole chewing issue at the end of talks, to avoid losing the audience. Yet what Leonard and Pearse describe is, in its own way, thrilling. Island-dwelling rare slugs. New species born before our very eyes. Historical mysteries of geology, of separation and rejoining. Answers to tricky questions of evolution, sexual preference, and the origins of species. A commonplace creature known to every schoolchild whose backstory only an adult mind can appreciate, like a Disney movie aside aimed solely at delighting the parents in the theater. “It’s a beautiful system,” Leonard says. “They’re just a fascinating group from an evolutionary standpoint.”