Eocene

I've been giving the background to the question, "Were there Cretaceous anthropoids?" ("The problem in a nutshell", "What is an anthropoid?")

One of my sources has been the 2004 book by K. Christopher Beard, The Hunt for the Dawn Monkey: Unearthing the Origins of Monkeys, Apes, and Humans. I'm not going to do a full review of the book. It has much of value in it, especially as a description of Beard's major find, Eosimias, and the way that it revised our understanding of anthropoid origins. I'll relate the current understanding of Eosimias (or at least, mine) in the next installment.

In Beard's telling, a central issue in the pre-Eosimias scientific framework was the identification of some omomyids as early tarsiers.

By the early 1990's, most paleoprimatologists accepted tarsiers as the sister group of the anthropoids. The Tarsier-Anthropoid clade identified by this hypothesis is called the haplorhine clade. The haplorhines, as their name implies, are linked by soft tissue characters of the nose, but also some aspects of the face, eyes, bony structure of the ears, and other characters. This used to be an area of much greater controversy before molecular data gained the resolution it has today. Now, we have lots and lots of genetic material from tarsiers and other prosimians, and it is clear that tarsiers are closer to anthropoids than other prosimians.

That doesn't necessarily settle the issues with fossils that share some tarsier features. We don't have their genes, and so we have only morphology to test the hypothesis that they are in fact tarsier relatives. This is important, because if we knew that a fossil represented an ancient tarsier relative, then we could conclude that tarsiers had in fact diverged from anthropoids by that time. And if we know that the anthropoids had diverged from tarsiers, then we know that some stem anthropoid must have existed by the time of that tarsier fossil.

This is exactly what Beard had suggested of a fossil omomyid called Shoshonius, from the Eocene of Wyoming.

[Shoshonius] allows us to predict that the anthropoid lineage extends back in time at least fifty million years, even if no anthropoid fossils come close to being that old. Paleontologists refer to such missing segments of the fossil record as "ghost lineages." We are forced to admit their existence because of the shape of the evolutionary tree, along with the age and position of key fossils that adorn it. Thus, if Shoshonius lies on the same major branch of the family tree that includes tarsiers, and if anthropoids lie on a separate but adjacent branch, the continuity of evolutionary descent requires us to deduce that the anthropoid lineage is at least as old as Shoshonius. To argue otherwise is to deny the geometry of the evolutionary tree (for example, by claiming that Shoshonius is in the wrong place) or to advocate the spontaneous generation of anthropoids (Beard 2004:165).

I like the straightforward starkness of Beard's description. Deny that anthropoids are 50 million years old, and you may as well believe they originated by spontaneous generation! I wouldn't go so far; the traits in question may have evolved convergently in some omomyids and in tarsiers -- in other words, it might not be such a stretch to think that Shoshonius is in the "wrong place". But you get the idea. Once you find a member of a crown group in the fossil record, the crown ancestor must be older than that fossil. If you don't have fossils of the other lineages in the crown group, that means these are all ghost lineages.

One might object that ghost lineages are unparsimonious. It would seem like a cladogram that necessitates long ghost lineages should pay some kind of penalty compared to alternatives that don't require organisms to persist for millions of years without leaving any fossil trace.

But the unpleasant truth is that for every well-documented series of fossils that shows a lineage evolving over millions of years, there are many others for which the fossils are few and far between. Paleontologists have devoted a disproportionate effort finding and describing primate fossil remains but there are still geographic areas in which we know that primates must have existed for millions of years, for which we have no fossil remains. This passage from a paper by Robert Martin, Christophe Soligo and Simon Tavaré describes the gaps in the fossil record of lemurs and callitrichids, which together account for a substantial fraction of primate diversity today.

As there is no convincing fossil evidence for the LCA of euprimates, some increment must obviously be added to the age of the earliest known undoubted fossil representative. With a relatively poor fossil record, the required increment is likely to be large [Martin, 1986, 1990]. The earliest known fossil euprimates are dated at about 55 Ma, but there are undeniable major gaps in the record. Madagascar lemurs (including the recently extinct subfossil species) account for around a quarter of modern primate species, yet not a single fossil relative has so far been found on the island. With the sole exception of Oligocene Bugtilemur in Pakistan, tentatively linked to modern dwarf lemurs in the family Cheirogaleidae [Marivaux et al., 2001; but see Seiffert, 2007], the fossil record of Madagascar lemurs remains totally undocumented. If Bugtilemur is a cheirogaleid, there is a ghost lineage of at least 30 Ma between this fossil and modern cheirogaleids on Madagascar, and older ghost lineages leading to the other extant families of lemurs. If Bugtilemur is not a cheirogaleid but simply an early strepsirrhine, all modern lemurs have a ghost lineage of at least 37 Ma, as fossil members of their sister group (lorisiforms) are now known to date back that far [Martin, 2003; Seiffert et al., 2003, 2005]. Another example of major gaps in the record is provided by the New World monkeys. No convincing relative of marmosets and tamarins (Callitrichidae) has yet been reported, although almost 34% of New World monkeys and more than 11% of extant primates are callitrichids. Undoubted fossil relatives of cebid monkeys indicate that the ghost lineage leading to modern callitrichids extends over at least 20 Ma [McFadden, 1990; Flynn et al., 1995]. It is also noteworthy that there is a gap of several million years in the Oligocene epoch in the primate fossil record as a whole, between the early Oligocene of the Fayum in Egypt and Taqah in Oman, and the late Oligocene deposits of Lothidok, Kenya, and Salla, Bolivia (fig. 1).

Were there no lemurs on Madagascar until 20,000 years ago? Were there no primates in the world during the middle Oligocene? They just had the bad luck of not being fossilized in locations where we currently have a record.

We will eventually find fossil evidence of some of these lineages. Surely we'll find more middle Oligocene sites with primates. Anthropoids must have been diverse by that time, but it seems that much of their Old World diversity became extinct, with the crown catarrhines diverging only by the Late Oligocene. Only the survival of the platyrrhines in the New World, and the Late Oligocene/Early Miocene persistence of groups like propliopithecids inform us about the earlier radiation.

The point is, there are gaps that we know. Is it such a stretch to think that there may be gaps we don't know about? If the tarsiers are found to go back very early, then some stem anthropoid must have existed also.

Next: The (old) new story of anthropoid origins.

References:

Martin RD, Soligo C, Tavaré S. 2007. Primate origins: implications of a Cretaceous ancestry. Folia Primatol 78:277-296. doi:10.1159/000105145

The evolution of early primates is a field that has developed rapidly in the last fifteen years. Many of the central issues were reviewed earlier this year by Blythe Williams, Richard Kay and E. Christopher Kirk ("New perspectives on anthropoid origins"). I want to touch on some issues, in a series of posts that may seem like a bit of a grab-bag.

I got started with a fairly simple question -- the one from the title -- were there anthropoid primates in the Cretaceous? Since this has expanded into a series, I think I'd better lead with the answer: We really don't know.

From the fossil perspective, fifteen years ago you'd have thought I was crazy to even ask the question. It was common knowledge that the living orders of mammals diversified after the extinction of the dinosaurs 65 million years ago. Even today, there are no widely-accepted anthropoid fossils earlier than the Middle Eocene. A few specimens argued to represent anthropoids are earlier, one as early as the Late Paleocene. But that's it. No positive evidence of earlier primate diversification, nothing that even looks like a primate before the Paleocene. Many paleontologists concerned with primate origins have assumed that the common ancestors of today's primates lived in the Late Paleocene, and that the primates had diverged from their closest relatives -- tree shrews, colugos, or bats -- sometime after the end of the Cretaceous.

Opposed to this traditional view, molecular comparisons of living primates and other mammals have suggested an earlier diversification of primates, as early as 90 million years ago. For example -- and I'll review many others during the course of the series -- Steiper and Young (2006) estimated the ages of primate divergences from long sequences homologous to an area around the CFTR gene on human chromosome 7. Like most studies, they assumed some "calibration points" with dates based on fossil evidence. One of these was the human-chimpanzee divergence (7 million years, based on Sahelanthropus), the other was the macaque-baboon divergence (8 million years). Steiper and Young did not have a tarsier sequence, so they reported the estimated strepsirrhine/anthropoid divergence -- necessarily older than the first anthropoids, since tarsiers are the sister group of the anthropoid clade. Their estimate: between 88.2 and 110.2 million years ago. In addition to these "old" estimates, they reported a range of "young" estimates based on lower calibration times, only 60.8 to 75 million years ago. That's a mere 20 to 30 million years older than the oldest uncontroversial anthropoids.

Primates are only one skirmish point of a much larger battle about the timing of diversification of mammal orders. DNA comparisons have consistently sketched out a long pre-Tertiary history for placental mammals. Many paleontologists favor a hybrid view, in which some superordinal groups of mammals -- like Afrotheria or Archonta -- existed in the Late Cretaceous, while the modern orders themselves got started after the extinction of the dinosaurs. That's a softer view of mammal diversification than the traditional idea of a rapid origination of all these groups after the K-T boundary. Even the hybrid hypothesis hides an apparent problem: It means that the K-T impactor must have spared dozens of distinct lineages of mammals, even as it wiped out every kind of dinosaur, large marine reptile, and 75% of the rest of species.

For a brief review of this issue as applied to mammals generally, I can suggest a 2009 article by Jennifer Evans, "The disputed rise of mammals." She reports on the largest molecular phylogeny yet constructed for mammals, called the "supertree," and its apparent conflict with the fossil record:

Although the supertree dated the origin of mammals at 93 million years ago and showed 43 placental lineages surviving the K/T boundary, Wible's analysis of more than 400 morphological characters in Cretaceous fossils across 69 taxa placed the oldest placentals at 63 million years ago. "There was no evidence in the fossil record that any of Cretaceous forms previously identified [by molecular biologists] as placentals were in fact placentals," says Wible.

Although fossils were used to date divergence points on the supertree, they could only date back to around 55-65 million years ago, where paleontologists have fossil evidence of modern mammals. "Until there's [fossil evidence of] a Cretaceous primate that everyone agrees upon there will be conflict between molecular and paleontological evidence," says Ross MacPhee, from the American Museum of Natural History.

Primates take center stage as one of the best-documented early mammalian lineages. Some expect to find anthropoids as early as 90 million years ago, yet the oldest well-established anthropoids are only around 45 million years old.

You might think that the solution is simple. For example, we might posit a different mutation rate on early branches of the primate phylogeny. Or we might simply give up on proposed Miocene hominins like Ardipithecus. Move those calibration points, and you totally eliminate the conflict between molecular and fossil information. But there's uncertainty on the fossil side as well. We expect the known fossils to underestimate the ages of branches on the primate phylogeny -- missing information can do nothing else. Some scientists have suggested that the known primate record is fully consistent with a Cretaceous origin and diversification, given what we know about which lineages of living primates are missing from the fossil record.

So understanding this problem will require some examination of both the fossil record and molecular evidence. Today this molecular side can be expanded to whole-genome comparisons of various kinds, and the data have expanded faster than anybody's analysis of them. That makes it a great topic -- there's work to do here, for those who understand the connections between the fossil and genetic records.

Next: "What is an anthropoid?"

References:

Evans J. 2009. The disputed rise of mammals. The Scientist 23:47. Online.

Steiper ME, Young NM. 2006. Primate molecular divergence dates. Mol Phylogenet Evol 41:384-394. doi:10.1016/j.ympev.2006.05.021

Williams BA, Kay RF, Kirk EC. 2010. New perspectives on anthropoid origins. Proc Nat Acad Sci USA 107:4797-4804. doi:10.1073/pnas.0908320107