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MARGINALIA

A Worm's View of Human Evolution

Pat Shipman

I was surprised recently to discover how much a few worms have to say about human evolution. There are many different ways of knowing in science, many different pathways to uncovering evidence, and some of them only the most ingenious among us would imagine. So it is with a project recently described in the Proceedings of the Royal Society of London that focuses on the anatomy, phylogeny and genetic variability of various species of tapeworms to uncover new facts about the habits of hominids, our human ancestors.

Figure 1. A taeniid tapewormClick to Enlarge Image

Eric Hoberg of the U.S. Department of Agriculture, Nancy Alkire of the University of Colorado, and Alan Queiroz and Arlene Jones, both of the Natural History Museum in London, realized that the tight adaptational relationship between a particular species of tapeworm and its host means that tapeworms can reveal a great deal about the animals in whose guts they live. Human beings are vulnerable to infestation by any of three species of taeniid tapeworms: Taenia saginata, T. asiatica and T. solium. All three are host-specific, meaning they can't survive as adults outside a human gut. Since tapeworms must be ingested to pass from individual to individual or from species to species, the research team realized that the genetic and host differences among tapeworm species can be used to understand something about the changing dietary habits of a host species.

Tapeworms have their own charm and at the very least must be considered to have found a clever way to make a living. They co-opt the work of their host species, who unwittingly provide food and housing to the parasites at various stages in their lives. The beauty of the system is that the host species actually infects itself as it goes about its daily tasks; the tapeworm need do nothing except be at the right place at the right time. The complicated life cycle of a tapeworm is magnificently adapted to its parasitic existence. For taeniids, this always involves taking advantage of a predator-prey relationship, in which a carnivore harbors the adult tapeworm and an herbivore hosts the infective larvae. With the exception of the three taeniid tapeworms that are specific to humans, adult tapeworms in this study commonly live in the intestines of carnivores such as lions, hyenas or African wild dogs. When the adult worms mature, they shed eggs, which pass out of the host's body in its feces. The eggs are then ingested by an intermediate host, which is often a particular species of herbivore, such as a domestic cow, some antelope or a pig (domestic or wild). In the body of the intermediate host, the tapeworm eggs develop into larvae that live in the host's flesh. The larvae then pass into the definitive host when it eats the infected intermediate host, either raw or inadequately cooked. Once in the definitive host's gut, the tapeworm larvae mature into adults and shed eggs, completing the cycle.

When did hominids first become definitive hosts for tapeworms? If we knew the answer to this question, we'd know when our ancestors began to eat animal flesh regularly enough for the human-specific tapeworms to evolve. If we knew which species were the intermediate hosts of tapeworms that are closely related to the human-specific tapeworms, we'd have a good idea of which prey species our ancestors ate. Finally, if we knew which other definitive hosts carry the tapeworm species most closely related to ours, we might learn something of the style of eating and obtaining meat practiced by our ancestors.

As a paleoanthropologist who spent decades trying to track the lifestyle and origins of meat-eating, hunting and scavenging among early hominids, I regret that I never conceived of such an interesting and sound approach to these questions. Fortunately Hoberg and his colleagues did. Among parasitologists and others who appreciate the humble tapeworm, the conventional wisdom has been that humans were first exposed to tapeworms that lived in domestic animals, either in companion carnivores such as dogs or in food animals such as cattle and swine. It is important to realize that a domestic animal is distinctly different from a tame individual of a wild species. A dog or a sheep is a domestic animal; a wolf or a mountain goat is not, even when it is brought up from birth by humans. A tame animal does not pass that tameness onto its offspring; taming is not a heritable, genetic change, and there is no simple way to discover when a hominid first tamed another species. In contrast, domestication is genetic and fundamental and changes the lives of those involved. Species become domesticated because humans control their reproduction and survival over generations. By picking and choosing which animals live and reproduce and which are eaten before they reproduce, people act as powerful selective agents. The process of domestication is actually a manipulation of the genetic makeup of a formerly wild species by humans, with the result that the evolved domesticate has desirable genetic attributes such as docility, high meat yield, abundant milk, thick wool or the like. Too, there are often bony changes in domesticated species that permit them to be recognized in the fossil record.

Who Infected Whom?

It is easy to imagine that a domestic animal, say a pig or a cow, living with humans and regularly eaten by humans, will pass along an array of larval tapeworms. Repeated exposure of humans to tapeworms previously found in another carnivore species through a shared food source could provide the opportunity for that tapeworm to evolve into a new, human-specific species. If the domestication hypothesis is true, then tapeworms specific to humans will be closely related to those that circulate among our canine companions or to those of food animals, such as cattle or pigs, or other domestic species. What's more, the hypothesis predicts that the genetic divergence between the domestic animals' tapeworms and our own should have occurred at about the time of domestication—about 10,000 years ago, according to the archaeological record. Since 10,000 years is a mere blink of an eye in evolutionary terms, if humans "caught" tapeworms from domestic animals only once, then all human-specific tapeworms should be very similar genetically.

For Hoberg and his colleagues, the key question was, Are the differences among human tapeworms consistent with a mere 10,000 years of evolution since their divergence? To find out, Hoberg and his team determined the phylogenetic relationships among all known species of Taenia. Then they examined the genetic sequence divergence between the two most closely related of the human taeniid tapeworms: T. saginata and T. asiatica. Rather than look at the entire mitochondrial DNA (mtDNA) sequence of each worm, they focused on the genes that encode cytochrome c oxidase, an essential catalyst in the end stage of metabolic respiration. Since mtDNA is passed maternally, without recombination, every change in mtDNA between mother and offspring represents a mutation. The standard metaphor is that each mutation represents a "tick" of the molecular clock. Because not all molecules tick (mutate) at the same rate, the clock has to be calibrated using data from pairs of species with well-known divergence dates: in this case, chimps and humans, rats and mice, and two species of snapping shrimp. Using this now-standard procedure for estimating divergence dates between T. saginata and T. asiatica, Hoberg got a startling answer: These two sister species of tapeworm diverged from each other not 10,000 years ago, but between 780,000 and 1.71 million years ago. Their ancestor most likely already lived in humans. Clearly, this lineage could not have been acquired because of the domestication of pigs and cattle by modern humans.

The researchers' alternative hypothesis was that the origin of human-specific tapeworms was triggered by a dietary shift from a primarily plant-based diet to one with much more animal flesh, which occurred among early (prehuman) hominids. The estimated divergence dates suggest that the hominid in question was most probably Homo habilis or H. ergaster. (The latter is sometimes considered merely an early African variant of H. erectus.) Where did these early hominids get their tapeworms from? And what role did domestic animals play in this story of worms and hominids? Revealing clues came from the analysis of T. solium, the third human-specific tapeworm, for it is closely related to tapeworms such T. hyaenae, T. crocutae, T. gonyamai and T. madoquae. These last four tapeworms respectively have the following definitive hosts, in order: brown hyenas, spotted hyenas and African hunting dogs; brown and spotted hyenas; lions and cheetahs; and jackals. The fossil record shows that each of these carnivores co-existed with early Homo in Africa for many millennia. These findings suggest that early African hominids got their food and ate in ways roughly similar to these carnivores. But these carnivores were by no stretch of the imagination domestic animals from which hominids "caught" tapeworms; they were instead fierce competitors for the same animal resources.

Personally, I find this a singularly gratifying result, since I was among the first to argue that early Homo hunted and scavenged animal carcasses. My evidence was archaeological—the presence of stone tools, cutmarks and hominid-induced breakage patterns on the fossil bones at hominid sites. Now quite different evidence from taeniid tapeworms provides a strong confirmation of the hypothesis that our hominid ancestors were adept facultative carnivores. The intermediate hosts of these tapeworms tell another important tale. African antelopes are the most common intermediate hosts. Other such hosts include the large buffalo, Syncerus caffer (which is not the domesticated water buffalo), wildebeest, waterbuck, impala, kob and quite small-bodied duikers. Three significant points emerge from these analyses. First, the definitive and the intermediate hosts are all African species. Second, the predators incorporate a wide range of hunting styles. They include classic ambush predators and those that specialize in swift, long-distance pursuit, solitary hunters and group predators, frequent scavengers and habitual hunters. Had all of the carnivores been, for example, swift group predators such as African hunting dogs, this might have suggested that hominids obtained their animal food through a similar strategy, but this idea cannot be sustained. Third, the intermediate hosts exhibit a wide range of habitat preferences, among them wet, marshy areas or dry savannahs; closed forest habitats, open bushland or very open grasslands. Apparently, hominids did not restrict themselves to preying on species of a single habitat. Instead, the pattern is one of diversity, both in the style of obtaining animal food and in the ecological locality in which that food was acquired.

Interestingly, the human-specific T. solium and T. asiatica have intermediate hosts that are not antelopes. The intermediate hosts of T. solium are humans, other primates, hares or rabbits, hyraxes, members of the dog family, and wild or domestic pigs. The intermediate hosts of T. asiatica are the domestic pig and cattle. This observation brings us back to a paradox posed above: If our ancestors weren't initially exposed to tapeworms from their domestic stock, why do human-specific tapeworms have intermediate hosts among domestic animals? Hoberg and colleagues suggest a complex scenario. From their data, they judge that the human lineage acquired taeniid tapeworms in sub-Saharan Africa, quite plausibly coinciding with the onset of regular scavenging and hunting in early Homo between 780,000 and 1.71 million years ago. The eggs of the ancestral taeniids passed from true carnivores to their varied prey, and then from those prey as larvae back to carnivores or on to predatory hominids. In time, the larvae of those carnivore-specific tapeworms evolved into human-specific tapeworms. Hoberg and his colleagues believe there were two independent exposures of hominids to the taeniid tapeworms; one lineage led to T. solium, and the other lineage evolved into T. asiatica and T. saginata. T. asiatica and T. saginata may have diverged when some hominids migrated out of Africa into Eurasia. From currently known fossil evidence, this expansion of hominid territory took place about 1.7 million years ago, when Homo ergaster colonized Eurasia. Moving into a new continent meant Homo encountered new prey species and new carnivore competitors. Many millennia after this great migration out of Africa, archaic Homo evolved into modern Homo sapiens, who still later domesticated animals, perhaps in at least two separate episodes. It now seems that conventional wisdom must be turned on its head. Humans did not "catch" tapeworms from their "dirty" domestic animals, but instead infected the domestic animals with their own tapeworms.

This imaginative and thought-provoking study has given us valuable insights into the human past. The transition from a largely plant-based diet to one incorporating significant amounts of meat was an ancient and profound one. Although the more animal-based diet had advantages—it has been linked to the increasing relative size of the brain in early Homo and to that species' enormous expansion of geographic range—one of the real costs of that change in lifestyle was the acquisition of tapeworms that sapped the energy of hominids. Until now, we have read this history as a hero story in which the clever human lineage triumphantly conquers the world. From the worm's-eye view, this is instead the triumph of the tapeworm, who not only spreads all over the world but persuades another to bear the cost of that expansion.

© Pat Shipman

 

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