Three million years of unwanted guests

Well, I guess they've got a plot for the pilot of that caveman show:

Humans caught pubic lice, aka "the crabs," from gorillas roughly three million years ago, scientists now report.
Rather than close encounters of the intimate kind, researchers explained humans most likely got the lice, which most commonly live in pubic hair, from sleeping in gorilla nests or eating the apes.

"Sleeping in gorilla nests." Yep, that's the ticket.

The quote is from a LiveScience article by Charles Q. Choi. The article talks a lot about "monkey business" but really spends more time on the hominid-eating-gorilla scenario:

"Unfortunately, even today among modern humans there's a bush meat trade where gorillas are killed for their meat," he said. "If archaic humans were butchering or scavenging those animals 3.3 million years ago, it would be a simple thing to transfer those lice from prey to predator."

UPDATE (3/7/2006): Carl Zimmer's post is great (he's all about the parasites) and mirrors some of what I wrote below. He also includes probably the best snarky quote: "Is this evidence of a Pliocene love that dare not speak its name?"

To telegraph my conclusion a bit, I still think the flawed assumption is that the hominid-gorilla interaction occurred when the hominid and gorilla Pthirus diverged. The interaction works a lot better later, assuming within-gorilla parasite variation. Since there is a lot of within-human variation in the other louse genus, Pediculus, the idea of a couple million years of delay between louse genetic divergence and lateral transfer is not at all unlikely, even without invoking ancient gorilla speciations.

Thoughts

I downloaded the research paper in BMC Biology by Reed and colleagues. Here's the 'Conclusions' section of the abstract:

Reconciliation analysis determines that there are two alternative explanations that account for the current distribution of anthropoid primate lice. The more parsimonious of the two solutions suggests that a Pthirus species switched from gorillas to humans. This analysis assumes that the divergence between Pediculus and Pthirus was contemporaneous with the split (i.e., a node of cospeciation) between gorillas and the lineage leading to chimpanzees and humans. Divergence date estimates, however, show that the nodes in the host and parasite trees are not contemporaneous. Rather, the shared coevolutionary history of the anthropoid primates and their lice contains a mixture of evolutionary events including cospeciation, parasite duplication, parasite extinction, and host switching. Based on these data, the coevolutionary history of primates and their lice has been anything but parsimonious.

There is actually a much more interesting story here than is indicated in either press account or abstract. The genera Pediculus and Pthirus were thought to have diverged at the time that gorillas diverged from the chimpanzee-human clade. This would explain why gorillas have Pthirus and chimpanzees Pediculus. The fact that humans have both ... well, that remained unexplained. The purpose of the study was to test whether humans retained the two genera ancestrally, or if instead they picked one up later.

What they found is that the two genera didn't diverge at the gorilla-chuman split, but instead way earlier. Their estimate for the Pediculus-Pthirus divergence is 13 million years. Thirteen million is as much as twice the age of the human-gorilla common ancestor. This estimate is probably biased toward the recent side, since it is calibrated against a divergence between hominoid and baboon lice assumed at 22.5 million years ago -- probably more recent than the true hominoid-baboon divergence.

The paper considers it likely that the human-gorilla-chimpanzee common ancestor lineage maintained this pair of lice species for the intervening time period, with one genus being lost in each of the two (gorilla and chuman) descendant clades. This ancestral lineage would be similar to humans in that respect -- host to two distinct parasite lineages, both of which stemmed from a single ancestor species.

But much later than the chimpanzee-human divergence, humans apparently picked up the gorilla lice somehow. The paper doesn't belabor this point or attempt to explain it, beyond this:

Evidence suggests that Pthirus pubis has been associated with humans for several million years, and likely arrived on humans via a host switch from gorillas. Despite the fact that human pubic lice are primarily transmitted via sexual contact, such contact is not required to explain the host switch. Parasites often switch from a given species to a predator of that species [17], and are sometimes found to switch to unrelated hosts in communally used areas, such as roosting or nesting sites [18]. The host switch in question could have resulted from any form of contact between archaic humans and gorillas including, but not limited to, feeding on or living among gorillas. Regardless of how the transfer occurred, suitable habitat had to be available on the new human host for the host switch to be successful. For example, it is possible that the switch of Pthirus from gorillas to humans coincides with a change in available niche space in humans, such as the loss of body hair. Further study, however, is required to test such a hypothesis (Reed et al. 2007:7).

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Hominids were certainly not hunting gorillas 3.3 million years ago. At least, not the hominids we know about. That date is a bit older than Lucy; it's 700,000 years older than the earliest evidence of flaked stone and 800,000 earlier than the earliest evidence of antelope butchery. Hominids weren't hunting gorillas because they weren't hunting any large mammal species then.

What's worse, gorillas and hominids weren't sympatric 3.3 million years ago. At least, not the gorillas and hominids we know about. Unless gorillas ranged into open woodland, and in particular the East African coastal forest, or hominids ranged into the central or west African rain forest, they never came into contact with each other at all.

If anything, we might expect that gorillas and chimpanzees would have been likely to come into contact and exchange parasites. They are currently sympatric, they eat the same foods, and they even build similar sorts of nests. It's like they share the same locker room. But they didn't have this parasite exchange.

It's all very strange. First we have this long period of divergence of the two great ape louse genera (orangutans don't have their own louse species). Then we have a divergence of the human and chimpanzee Pediculus species just exactly when it should have happened. And then there is this lateral transfer of lice from gorillas to humans 3 million years ago - when hominids and gorillas weren't apparently sympatric and had no credible mechanism for lice exchange.

Here's my hypothesis: cryptic African hominoids. The apparent craziness all comes from the assumption that the only species that existed are the ones we know about. For Africa 3 million years ago, that means two or three hominid species, one gorilla lineage and one chimpanzee lineage. We don't have any fossils that old for the apes; we can only infer their existence from the fact that they exist now.

Let's consider what we know. We know that 3 million years ago there weren't any chimpanzee or gorilla relatives in the Rift Valley, and plausibly (but not definitely) not in South Africa or the Sahel.

We don't know how extensively hominids ranged into the west African or central African forests, particularly from the north and southeast. We don't know how extensively gorillas and/or chimpanzees may have ranged outside the core forested areas where they have historically existed. In the absence of Homo, the competition between these apes and hominids at the forest boundaries may have been a close game.

We don't know how many species of ancient chimpanzees and gorillas there may have been. The present subspecific variation of chimpanzees seems to reflect recent colonization of the eastern range from central Africa, and some substantial population interchange between central and western ranges. Gorilla subspecies now seem to have emerged within the same time frame, with a possible colonization from their western range into their eastern range within the past million years.

Bonobos are only ca. 850,000 years old (Won and Hey 2005). To summarize, the current eastern chimpanzees weren't in East Africa half a million years ago, and the bonobos weren't south of the Congo a million years ago, and eastern gorillas weren't there a million years ago either.

Who was? It seems to me that the best candidates would be ancient species of gorillas and chimpanzees that no longer exist. A second-best (and maybe more interesting) candidate is some variety of hominid. A third-best (and even more interesting) candidate is an ancient ape lineage dating from before the G-C-H divergence.

Three million years ago, any one of those possibilities is credible. Here's my favorite: two gorilla species (or subspecies) became isolated enough for louse divergence 3.3 million years ago, and continued to coexist. Sometime after 2 million years ago, Homo encountered one of these species and picked up its lice. That gorilla lineage later became extinct, perhaps by range expansion from Homo.

Oh, and the long divergence time between the two lice genera? I like a long divergence and later lateral transfer from some pre-H-C-G Miocene ape lineage. There were likely several in Africa to choose from. Maybe it was Sahelanthropus...

References:

Reed DL, Light JE, Allen JM, Kirchman JJ. 2007. Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol 5:7. doi:10.1186/1741-7007-5-7

Won Y-J, Hey J. 2005. Divergence population genetics of chimpanzees. Mol Biol Evol 22:297-307. <a href="http://"