Did placental oxygen transfer support increased brain metabolism as humans evolved?

Cerebral blood flow in relation to age of fossil skulls
from 12 hominin species.
Reproduced from Seymour et al.  R S Open Science (CC-BY) 

There is much interest in how increased brain size impacted on dimensions of the pelvis, birth weight and placentation as humans evolved (here). Increased brain growth in fetal life would seem to demand a greater placental blood flow to ensure an adequate oxygen supply. This may have led to increased invasiveness (discussed here) and indirectly to the risk of preeclampsia (here). 

But what if there was an increase not only in size but in the metabolic rate of the brain?

In a novel approach, Seymour, Bosiocic and Snelling attempted to assess cerebral blood flow in fossil adult hominins as a surrogate for oxygen supply to and consumption by the brain. As their starting point they measured the diameter of the carotid foramen in skulls of fossil hominins ranging from Australopithecus to archaic Homo sapiens (the carotid foramina carry the principal arteries supplying the brain). As can be seen in the figure, their main finding was that during hominin evolution cerebral blood flow increased disproportionately to brain size. The implication was that there was a progressive increase in the metabolic rate of the brain.

Of course this approach required some major assumptions (see below). But if the metabolic rate of the adult brain did increase successively as humans involved, so perhaps did that of the fetal brain. Here more is at play than the rate of blood flow to the brain. In adults the blood becomes fully saturated in the lungs, but that is not the case in fetal life. The oxygen content of the blood reaching the brain is dependent on placental function (reviewed here).

For Neanderthals there is enough data to conclude that brain size at birth did not differ from that of modern humans (here). But if human fetal brain had a higher metabolic rate than Neanderthal fetal brain, it might still have required a more efficient placenta.

Assumptions: The approach adopted by Seymour et al. relied on rearranging an equation for shear stress to isolate one of its determinants, blood flow rate. To accomplish this, shear stress must first be estimated using a scaling model that relates shear stress to body size. This is the weak point in the analysis, but the authors point to a previous study that verified the approach in primates and marsupials

Horned armadillos and rafting monkeys

A giant caiman (Purussaurus neivensis) and small
litopterns (Megadolodus molariformis)
Illustration Velizar Simeonovski (C) 2016 by Darin A. Croft

I thoroughly recommend this new book on South American fossil mammals of the Caenozoic Era. Intended for a broad readership, it is a times fanciful. The full caption to the above figure reads, "A giant caiman (Purussaurus neivensis) finally strikes in a fury of mud and water after quietly approaching a group of small litopterns (Megadolodus molariformis) drinking at the river."

Indiana University Press ISBN 978-0-253-02084-0

The book is dedicated "to anyone who has ever wondered what a notoungulate looked like," which makes me the target audience. I read extensively about the fossil fauna when writing about the placentation of the extant species (here). The extinct families that lived side by side with marsupials and earlier xenarthrans were so unfamiliar as to seem wraith-like.

The xenungulate Carodnia vieirai from Itaboraí
Illustration Velizar Simeonovski (C) 2016 by Darin A. Croft

Darin A. Croft has worked closely with Velizar Simeonovski to bring extinct taxa to life. "The xenungulate Carodnia vieirai passes under the shadows of the dense vegetation of Itaboraí at high noon" is another example. This is the same artist who illustrated Extinct Madagascar (previous post).

After some introductory chapters the subject matter is arranged according to 15 fossiliferous localities. Conspicuously absent is Lagoa Santa in Brazil where the Danish palaeontologist P. W. Lund worked in the Nineteenth Century (here). His extensive Collection is housed at the Natural History Museum of Copenhagen University.

Insectivores endemic to the Caribbean

Puerto Rican Nesophontes (N. edithae)
Reconstruction by Jennifer Garcia CC BY SA 3.0

The Caribbean is home to two endemic families of insectivores. The Nesophontidae are recently extinct. Their demise is attributed to the introduction of rats by Spanish Explorers though some believe the genus survived into the 20th Century.

To establish their phylogenetic position, scientists recently extracted DNA from a specimen preserved in an ancient owl pellet (here). This was no mean feat as the specimen was 750-years-old and DNA degrades rapidly in the tropics.



Hispaniolan Solenodon (S. paradoxus)
Biodiversity Heritage Library CC BY 2.0

The main finding was that Nesophontes shares a common ancestor with Solenodon. There are two species of this insectivore both listed as threatened by IUCN. A common origin had not been predicted on anatomical grounds not least because Nesophontes and Solenodon have different patterns of tooth occlusion (here). Together these families represent the oldest branch of the insectivores (Order Lipotyphla).

Placenta of Solenodon paradoxus
Wislocki (1940)

Despite its rarity, the placentation of S. paradoxus has been described (here) and we later compared it with that of other insectivores (here). Interesting features are remnants of capsular decidua, elaborately branched yolk sac villi and a sheath that superficially resembles that of crociduran shrews.

Congratulations Andrea Wulf

Andrea Wulf author of prize winning The Invention of Nature

The Invention of Nature: The Adventures of Alexander von Humboldt: The Lost Hero of Science by Andrea Wulf was just awarded the Royal Society Insight Investment Science Book Prize 2016. Previously it won the 2015 Costa Biography Award.


ISBN-13: 978-1848548985

This is a fantastic book. While rooted in the late 18th Century, Andrea Wulf convinces us that Alexander van Humboldt's life and legacy are pertinent today. He started life as a mine inspector and was in his early thirties before realising his dream and travelling in South America where he showed extraordinary stamina and a capacity for accumulating huge amounts of data in all areas of science.

Charles Darwin had a set of Humboldt's books in his cramped cabin on the Beagle and they were heavily annotated. Humboldt met and corresponded with American presidents in post Revolutionary America and influenced the thinking of conservationists such as John Muir. It was his way of thinking about the interrelatedness of the environment that led Ernst Haeckel to coin the very word ecology (from the Greek for household).

Statue of Alexander von Humboldt in front of
Humboldt-Universität in Berlin

Alexander's older brother Wilhelm was a Prussian diplomat and minister of education. He it was who founded the university in Berlin that now bears the family name.

The subtitle The Lost Hero of Science suggests Alexander von Humboldt has been largely forgotten in the English-speaking world. Andrea Wulf's biography puts this to rights. 

Mammal tree of life still not resolved

Lesser hedgehog tenrec (Echinops telfairi)
A member of the superordinal clade Afrotheria
Photo by Wilfried Berns CC BY-SA

My studies of placental evolution were stimulated by the large-scale molecular phylogenetic analyses of mammals that appeared 15 years ago (e.g. here). Especially riveting was the revelation of four superordinal clades, among them Afrotheria. 

An excellent review of the progress made in molecular phylogenetics and phylogenomics in the last 15 years recently appeared under the heading "Mammal madness" (by Foley, Springer and Teeling here). 

Competing hypotheses on the root of the mammalian tree
From Mess and Carter (here) based on Springer (Chapter here)



Some of the uncertainties arising from the earlier work remain. Most striking is the failure unequivocally to root the tree. The three competing hypotheses shown above are still in play. While consensus is tipping in favour of Model A above, retroposon analysis provides similar support for all three.

This is not all. There remains uncertainty about the branch order within Laurasiatheria, which includes bats, carnivores, pangolins and even- and odd-toed ungulates.

Such uncertainties make it difficult to plot the evolution of fetal membranes and placentation. Thus the likelihood that the common ancestor of extant eutherians had an endotheliochorial placenta is greater under Model A than the other two hypotheses (shown here).

Concatenation and coalescence

Analysis of large data sets involves some fancy statistics. Foley et al. give a fair account of the pitfalls in concatenation, used in all the early papers, and coalescence. Coalescent methods require much more computer time and are not applicable to large data sets unless short cuts are taken. So far this has not worked out too well.

An article just appeared in Cladistics (here), which seems to demand a "correction," in reality a retraction, of a paper in PNAS based on a coalescent approach. The authors doth protest too much, methinks. As Foley et al. point out, some pretty weird results appeared in the early days of DNA studies, too.

Morphology and molecules

The attitude of some researchers to morphological data could also be more generous. Attempts to integrate morphology and molecules, such as O'Leary et al. (previous post) do throw up some counterintuitive results. But there are examples where fossils have been useful in bolstering hypotheses based on molecular data - the position of whales is a case in point (previous post). Similarly, Afrotheria is not well supported by morphology, but we have published an apparent synapomorphy in the form of the allantoic sac (here).

Moreover fossil calibrations are the key to solving another conflict, which concerns the timing of ordinal diversification of mammals. Deservedly this is given close attention in Foley et al.'s excellent review. The sort of fossils we are talking about are too old to yield ancient DNA so we have only morphology to go on.

Foley et al. finish on an optimistic note and predict the next 20 years of phylogenetic research "should result in the resolution and dating of the mammal tree of life."

 



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. 

Evolution of altriciality

Kangaroo Joey inside the pouch
Photo by Geoff Shaw, Zoology, Melbourne, Australia CC BY-SA 3.0)

Marsupials and so-called placental mammals share a common ancestor yet pursue very different reproductive strategies. This led Ingmar Werneberg and colleagues to ask what reproduction was like in the common ancestor of marsupials and placentals (here).
They sampled data from the literature and examined specimens in the Hill and Hubrecht Collections at Museum für Naturkunde in Berlin. (In published sources they found examination of photographs and drawings more reliable than verbal descriptions.) There is a huge data set in the Supporting Information.


Altricial and precocial neonates exemplified by the
mouse (above) and guinea pig

It was estimated that the last common ancestor of placental mammals had a gestation of around 4 months and a litter of 3-5 young. The newborn were altricial and had closed eyes and almost naked skin at birth. The precocial lifestyle of hoofed mammals and the guinea pig is a derived feature (previous post). The newborn of marsupials are, of course, highly altricial.

A reconstruction was attempted of the neonate of the therian ancestor. This suggested it was anatomically more like extant placentals than extant marsupials. In contrast, the preweaning period was very long compared to intrauterine gestation and thus infancy in this ancestor was more marsupial-like. The relative timing of eye opening was between that of placental and marsupial mammals. Gestation lasted 31 days in this hypothetical ancestor. It was reduced to 21 days in the marsupial lineage while increasing fourfold in the placental lineage.