Lagoa Santa skulls still perplex Danes

Peter Wilhelm Lund (1801-1880)
Danish National Library (public domain)

When Peter Lund excavated human remains from Sumidouro Cave he was thoroughly perplexed. Not least because they were jumbled together with the bones of an extinct megafauna. This was in 1840 so well before Darwin had published On the Origin of Species (which cites Lund's work).

The skeletons were shipped to Copenhagen and examined there by several distinguished anthropologists (Lund never returned to Denmark). The consensus that arose was that "Lagoa Santa Man" was unrelated to present-day Native Americans. 

Springer 2017: ISBN 978-3-319-57465-3

Research and debate was renewed in the last century with new excavations in the caves near Lagoa Santa (now a suburb of Belo Horisonte). A key find was Luzia, a skull feared lost in the recent fire at the National Museum in Rio de Janeiro (previous post) (it survived but suffered heat damage). This skull was dated to 11,000 years ago.

Comparisons have been drawn between the features of the Lagoa Santa skulls and those of Australasian peoples such as Andaman Islanders. What can genomics tell us? A first set of clues hinted at an early wave of migrants designated "Population Y" who left a genetic signature that is strongest in some isolated Brazilian communities (see my review of David Reich). 

Skull from Sumidouro Cave excavated by Peter Lund

Now a Dane has ventured into the Lund Collection and extracted ancient DNA from a 10,400 year-old skull. The results appeared in Science last December (here). Eske Willeslev and his group found a clear Australasian genomic signature that was absent in other ancient remains from the Americas. They concluded this signal, "implies that an early group possessing it had disappeared or that a later-arriving group passed through North America without leaving any genetic trace." A conclusion echoed by the lead author, José Victor Moreno-Mayar, who simply said (here), "How did it get there? We have no idea."

It seems the Lagoa Santa remains are just as perplexing to Willerslev as they were to Lund and for a similar reason: they do not neatly fit into the scheme of things.

Postscript

The Willerslev paper is really worth reading. It builds on earlier work to confirm that Native Americans (other than Inuits) derived from a group that split from East Asians and resided in Beringia (Ancient Beringians). As they advanced into the Americas at the end of the Ice Age there was an early split into Northern (NNA) and Southern Native Americans (SNA). The SNA dispersed rapidly south of the remaining ice some 14,000 years ago. In a later phase there was admixture from a population in Mesoamerica that migrated both north and south. Another paper on ancient DNA from the Reich group also found evidence for rapid expansion into South America (here), but did not have Lagoa Santa in the data set.

Why Luzia was important

Cast of the skull known as Luzia as displayed at
National Museum of Natural History Washington DC
Photo by Ryan Somma CC BY-SA 2.0

Luzia was excavated from Lapa Vermelha, Minas Gerais, Brazil and was the oldest human fossil from South America. She was found in strata dated to 11,000 years ago. Whilst casts of the skull exist elsewhere the original was lost (at best severely damaged) in the catastrophic fire that destroyed the National Museum in Rio de Janeiro. 

Luzia Woman belonged to an ancient population formerly known as Lagõa Santa Man or Paleoamerind. The first to excavate such skulls was the Danish Naturalist Peter Lund, who found them as far back as 1840. Based on the classical craniometric criteria used by anthropologists until well into the twentieth century, this population clearly diverged from all others in North and South America.

Lagõa Santa skull excavated 1840 by Peter Wilhelm Lund

There is an interesting correlate in modern genomic data. David Reich and colleagues postulate an ancient Population Y corresponding to a genetic signal borne by the Surui people of the Amazon region (discussed here - see previous post for Reich's book where this is further discussed). The interesting thing about this signal is that it is shared with the faraway Andaman Islanders and natives of New Guinea and Australia.

We already know of two branches to the population that crossed the Bering Strait and peopled North and South America - thanks to work by Eske Willerslev's group (here). Was there a third branch that gave rise to the Paleoamerinds or even a separate and earlier migration?

To piece this together it would have been useful to extract ancient DNA from the Luzia skull. That had not been done prior to the fire. There are other skulls around including those excavated by Peter Lund and now housed in Copenhagen. They may yet yield new pieces to complete the puzzle.

Carnegie Collection of human embryos

Carnegie embryo 8171. Early lacunar stage (Stage 5b)
Courtesy of Dr. Allen C. Enders

An important source for human embryology, including implantation and formation of the placenta, is the Carnegie Collection now housed at the Human Developmental Anatomy Center in Washington D.C. The core of this collection is the carefully dated series of embryos first described by Hertig, Rock and Adams (here).

The Virtual Human Embryo is an online ressource based on the serially sectioned embryos in this collection and includes 3D reconstructions. It covers all 23 Carnegie stages in the first 8 weeks of embryonic development and cannot be too highly recommended.

Carnegie Embryo 7801. Showing extraembryonic coelom (eec)
and secondary yolk sac (sys) (Stage 6)
Courtesy of Dr.Allen C. Enders

Now a group in Amsterdam has used the Carnegie Collection to develop an additional annotated digital atlas of human development (described here). They also utilized material from the Boyd Collection at the Centre for Trophoblast Research in Cambridge.

They make two claims. First that representations in textbooks have become increasingly schematic. This is demonstrably true. Second that the descriptions in standard texts are often based on extrapolation to humans from animal models. It is hard to assess if the latter truly is the case. For example Human Embryology by Hamilton, Boyd and Mossman (previous post) was based on the human embryos in the possession of the three authors. In Germany there was a strong tradition to cover the embryology of all vertebrates, concluding with the human, exemplified by Dietrich Starck's Embryologie.

In physiology, on the other hand, animal data often are presented as if they were human. One example concerns oxygen tensions in various parts of the fetal circulation. Pretty much every textbook of physiology has a large illustration of the fetal circulation with data obtained in sheep by Dawes, Mott and Widdicombe. The figure legends often fail to acknowledge the source or the species or both.

A colugo genome at last

Phylogenetic placement of colugos  (Scandentia) in the lineage of primates
From Mason et al. Sci Adv 2016 (here) CC BY-NC

Used to be that tree shrews (Scandentia) were regarded as the closest relatives to primates as cogently argued by Wilfrid Le Gros Clark. Molecular phylogenetics have brought that into question with some proposing colugos  or "flying lemurs" (Dermoptera) as a better alternative. But there have several competing hypotheses (see Martin). Choosing the right one has been difficult in the absence of a colugo genome.

Now that has been rectified in a comprehensive study by Mason and colleagues (here) who sequenced the genome of a Sunda colugo and compared it with genomes from 21 mammals. The result clearly came out in favour of colugos as the closest relatives to primates, supported by  20 shared indels and 16 shared retrotransposons.

There are many morphological similarities between tree shrews and colugos but the tree constructed by Mason et al. implies these are due to convergent evolution. Within Euarchontoglires they find tree shrews as the sister to Glires (rodents and lagomorphs).

Museomics and hidden biodiversity within colugos

Colugo fetus and placenta at term; ys = yolk sac;
pat = patagonium From Hubrecht 1894 (here)

Current reference works recognize no more than two species of colugo: Sunda Colugo (Galeopterus variegates) and the Phillipine Colugo (Cynocephalus volans). Mason et al. conclude that there may be as many as 6 Sundaic species and 2 Phillipine ones. They reached this conclusion by extracting DNA from museum specimens of known provenance. As an example, the Eastern and western populations on Borneo are highly divergent consistent with topographical features creating barriers to dispersal.

Currently we are re-examining the placenta and fetal membranes of colugos. We too have had to rely on museum specimens such as those collected by A.A.W. Hubrecht.

The importance of museum collections has been highlighted before in this blog. It is nice that scientists other than morphologists have discovered their value and coined the term museomics for studies of DNA from ancient specimens. Those in the current study ranged from 28 to 121 years old. The oldest specimen from the Raffles Museum of Biodiversity Research is contemporaneous with those collected by Hubrecht for his study of the fetal membranes and now housed at Museum für Naturkunde in Berlin. 

Treasure houses under threat

The Field Museum Chicago
by Juanfibarra Wikimedia Commons CC BY 2.5

Museums house vast collections of specimens. For major museums of Natural History, these can be numbered in tens of millions. The specimens of greatest interest to embryologists will be in the wet collection and preserved as a rule in alcohol. Curating these specimens is an expensive business. When Chicago's Field Museum built a new Collections Resource Center the bill ran to $65 million and so stretched the budget that it resulted in cuts to museum staff (here).

Cross section through placental disc of a web-footed tenrec
(Limnogale mergulus) from Enders et al. (here). FMNH 165440

Now museum collections in the US are under further threat as the National Science Foundation has suspended its funding for the maintenance of biological research Collections (here). This is a matter of great concern.

Thanks to the Field Museum were able to describe the placenta from a rare specimen of an aquatic tenrec (above). We also used Field Museum specimens when reviewing the reproductive organs of bats (here).

Gravid uterus of a chimpanzee (Pan troglodytes) from the Hill Collection
currently housed at Museum für Naturkunde Berlin

Some museums house dedicated collections of embryological material. The J. P. Hill Collection is a good example and we have used it for several projects, including the first description of deep trophoblast invasion in a non-human primate (here).

The history of this collection is instructive. After Hill's death in 1954 it was stored in the attic of Dixon Boyd's house in Cambridge. It subsequently found what seemed to be a permanent home at the Hubrecht Laboratory in Utrecht. Together with the Hubrecht Collection it was eventually kept in a purpose built facility of a new building. With a change of director this space was seen as more suitable for -70 freezers and the future of the collection remained uncertain until it was removed to Berlin. The director subsequently became President of the Royal Netherlands Academy of Arts and Sciences!