Domestication of horses

Przewalski's horse - no longer seen to be a direct
ancestor of domestic breeds. Photo by Chinneeb (CC)
 

A large consortium has just reported on the genome of horses (Equus caballus) from the Siberian permafrost (here). The two specimens were estimated to be 16 and 42 thousand years old. Thus they were from before the start of domestication as known from the archeological evidence.

Horse phylogenetic relationships from Schubert et al. (here)
(c) The Authors

The phylogenetic analysis showed as expected that the ancient specimens (purple) are basal to all living members of the E. caballus species. However, while most genes present in domesticated breeds were found in the ancient genomes, many were missing from the Przewalski horse genome. It is perhaps a distant cousin rather than a direct ancestor of the domesticated horse (see commentary here).

Section through umbilical cord of Przewalski's horse
From the Benirschke web site (here)

So there have been two paths of selection: one through selective breeding (resulting in both desirable and deleterious traits) and the other through natural selection resulting in Przewalski's horse.

 

Placenta and implantation site of Przewalski's horse.
From the Benirschke web site (here)

These conclusions are in line with those made after sequencing the genome of a really old horse from the Middle Pleistocene (see previous post).

What were the gondwanatheres?

Right mandible of Sudamerica ameghinoi a gondwanathere
From Koenigswald W. Acta palaeontologica polonica 1999; 44: 263-300

Gondwanatheria is a clade of mammal-like forms once widely distributed on the southern continents that once were part of Gondwana. Until now they were known only from teeth and jaw fragments such as the one shown above. It therefore was a major breakthrough when a complete skull was found in Cretaceous deposits on Madagascar. It is described in the current issue of Nature (here) as a new genus and species Vintana sertichi.

The most exciting part of the paper is the phylogenetic analysis. Firstly, it reveals a sister group relationship between gondwanatheres (from southern continents) and multituberculates (from the northern continent Laurasia). Secondly, it shows both can be accommodated with another enigmatic group, the haramiyids, in a monophylectic clade Allotheria, i.e. all these fossil species shared a common ancestor.

Finally, Allotheria fits within Mammalia so all these mammal-like species were true mammals. The lineage that led to present day monotremes (duck-billed platypus and echidnas) is basal to Allotheria whereas that of marsupials and placentals came later.

My recent post on Extinct Madagascar concerned more recent mammals, all descendants of individuals that reached the island by rafting. But Madagascar has a more distant past, starting as part of the supercontinent Gondwana. Vintana derives from a lineage that existed on Gondwana before the breakup, evolved in isolation and went extinct, leaving Madagascar without mammals for millions of years.

Origins of the laboratory guinea pig

Newborn guinea pigs (Cavia porcellus)
(c) Per Svendsen

The domestication of guinea pigs dates back hundreds of years. Animals raised for food or the laboratory are of a species (Cavia porcellus) that is not found in the wild. Its closest relatives are the Brazilian guinea pig (C. aperea) and the montane guinea pig (C. tschudii) from western South America including Peru.

Analysis of mitochondrial DNA (here and here) clearly shows that the domestic guinea pig groups with the montane species. Furthermore, analysis of the skeletons of mummified guinea pigs from archaeological sites in Southern Peru and Northern Chile (here) indicates that domestication started in the Andes, the natural habitat of C. tschudii.

Karyotypes of Cavia tschudii male (left) and C. porcellus female (right)
From Walker et al. 2014 (here) (c) Laura I. Walker et al.

A recent paper (here) compared the chromosomes of the wild and domestic species and confirmed that differences arose in the course of this first phase of domestication.

Guinea pigs were imported by European traders in the 16th Century and underwent a second phase of domestication that resulted in the laboratory guinea pig. There was even a further phase of domestication in South America with two lineages of guinea pigs selected for improved meat quality.

Plesiorycteropus was a giant tenrec

Innomate (pelvic bone) of Plesiorycteropus an extinct mammal
from Madagascar (Drawing by Forsyth Major 1908)

The recent fauna of Madagascar included species that were much larger than those found today an example being the gorilla-sized lemur Megaladapis. One of these fossils Plesiorycteropus has defied interpretation. It has been compared to the aardvark and other myrmecophagous (termite-eating) mammals such as pangolins and anteaters.

The most thorough study of the subfossil material, by McPhee (here), defined two species, P.  madagascariensis and P. germainepetterae, and erected a new Order Bibymalagasia to accomodate them. More recently Asher (here) assigned Plesiorycteropus to the superordinal clade Afrotheria.

Phylogenetic analysis based on collagen sequencing has
Plesiorycteropus as sister to the tenrecs from Buckley 2013 (here)

A recent study (here) relied on molecular sequencing of collagen from a fossil Plesiorycteropus and a range of living mammals. The technique, which uses soft-ionization mass spectroscopy, is a promising alternative to sequencing of ancient DNA. The resultant tree confirmed that Plesiorycteropus belonged to Afrotheria but related to tenrecs rather than the aardvark. Therefore it is part of the radiation from a single colonisation event (Sweepstakes Distribution).

Tailless tenrec (Tenrec ecaudatus) the largest Malagasy tenrec
weighs about 1 kg. Photo by Markus Fink (GNU Free Documentation Licence)

Estimated size of Plesiorycteropus was 6-18 kg so it certainly was a giant compared with living Malagasy tenrecs and the giant otter shrew which weigh about 1 kg.

Picturing Madagascar's past

Cover features elephant birds Aepyornis hildebrandti 
and the giant lemur Archaeoindris fontoynontii

Extinct Madagascar by Steven M. Goodman and William L. Jungers has just been published by  The University of Chicago Press (ISBN-13 978-0-226-14397-2). As implied by the subtitle Picturing the Island's Past the text centres around 20 superb colour plates by the Bulgarian artist Velizar Simeonovski each depicting the fauna found at a particular fossil site.

The emphasis is on the larger species of reptiles, birds and mammals that became extinct and the authors explore possible causes ranging from climate change to hunting. This bias means that smaller mammals, such as tenrecs and endemic rodents, are scarcely mentioned except in the synoptic tables.

Aldabra giant tortoises - relatives of the extinct Malagasy species
Muhammad Mahdi Karim (Gnu Free Documentation Licence)

However, I found it fascinating to learn that the extinct giant tortoises (Aldabrachelys spp.) are likely to have been important grazers and that the extant species on the Aldabra Atoll represent a greater biomass per square km than the mammals on the Serengeti grasslands.

Malagasy crowned eagle piercing the shoulder blades of a sloth lemur

The chapter on an extinct raptor, the Malagasy crowned eagle Stephanoaetus mahery, was exciting; by analogy with the extant African species S. coronatus, it likely was a predator of large lemurs including the likewise extinct sloth lemurs (Palaeopropithecus spp.). But the book's plan makes it harder to find a coherent account of, for example, the "Madagascar aardvark" Plesiorycteropus madagascariensis. No reference is made to a study showing that this enigmatic species belongs to the Afrosoricida and thus is related to the tenrecs and golden moles (here).

Apart from the plates, figures are in grey tone. They include historical photos such as Grandidier's 1898-99 expedition. However, even more recent photos lack sharpness and contrast, perhaps due to the quality of paper chosen.

The introductory chapters give useful information on the geology and history of the island including the origins of the Malagasy people from Austronesians and Africans. In general the impact of humans in past centuries may have been overstated. The chapter on elephant birds concludes there is no evidence they were hunted to extinction and some evidence they may have been victims of climate change. The real and frightening aspect is the enormous habitat loss that has occurred in the last 60 years and that is still ongoing.

Reproduction in domestic ruminants

ISBN13: 9781899043637

Every four years there is a conference on reproduction in domestic ruminants. The latest was held this August at Obihiro, which is on Hokkaido, the North Island of Japan. The accompanying book (details here) is a useful collection of reviews covering most aspects of male and female reproductive biology.

The opening chapter Ruminant phylogenetics: a reproductive biological perspective by William J. Silvia is an excellent overview that integrates molecular phylogenetics with morphology including various aspects of placentation.

There are several chapters on placentation including Early placentation and local immune regulation by Kazuhiko Imakawa and colleagues. This deals with transcriptional regulation of IFNT the gene coding for interferon-tau, which is secreted by the trophectoderm at the blastocyst stage and results in maternal regulation of pregnancy. Another topic is syncytins (previous post) in ruminants. In addition, I have contributed a chapter on Evolution of placental structure and function in ruminants.

Previous volumes in this series have appeared under the imprint of the journal Reproduction. Although the current volume conforms to that journal's format, it has been published in book form by Context. As far as I can make out, it is not possible to purchase individual chapters.

Placenta-derived exosomes and the immune response to pregnancy

Placental exosomes at the maternal-fetal interface
Reproduced with permission from Mincheva-Nilsson and Baranov Am J Reprod Immunol 2014
(c) 2014 John Wiley & Sons A/S

Exosomes are tiny vesicles (30-100 nm) released from living cells that facilitate intercellular communication (previous post). Exosomes are assembled by and released from the syncytiotrophoblast of human placenta. They carry molecules that could be of critical importance for suppression of the maternal immune response, which might otherwise cause rejection of the fetal allograft.

A brand new review by Lucia Mincheva-Nilsson and Vladimir Baranov (here) summarizes several mechanisms that might be involved and suggest "the placenta is surrounded by a cloud of exosomes that creates a beneficient and protective mileau for its existence." Among these mechanisms (summarized in the Figure) are reduced NK-cell cytotoxicity (through down regulation of the NKG2D receptor), impaired T-cell signalling, apoptosis of activated lymphocytes and effects mediated by TGF-beta that might include recruitment of regulatory T-cells (previous post).

There is more. The syncytiotrophoblast also releases much larger particles (0.2-2 micrometers) often referred to as STBM (for syncytiotrophoblast-derived microparticles). They are not carefully assembled as are exosomes but resemble a form of cellular debris. Importantly, they are pro-inflammatory with the potential to activate the immune system. Mincheva-Nilsson and Baranov hypothesize that placental exosome production may counterbalance the deleterious effects of STBM. They argue that determination of a normal range for the STBM/exosome ratio should be a research priority as it could lead to development of new diagnostic tools.

The Blakiston line

Thomas Wright Blakiston (1832-91)

Thomas Blakiston spent 23 years in Hakodate, one of the Japanese Treaty Ports opened to foreign trade in 1858. He failed in his original enterprise, to establish a saw mill, but flourished as a merchant. More importantly he made many observations as an ornithologist.

Blakiston was the first to observe that fauna of the northern island of Hokkaido differed from that of Honshu. Thus the Strait of Tsugara formed a zoogeographical barrier of a type similar to the Wallace Line (previous post). It is referred to as the Blakiston Line.

Blakiston's Fish Owl (Bubo blakistoni)

There is a memorial to Thomas Blakiston atop Mount Hakodate. In addition the former British Consulate, now a museum in the historic quarter of Hakodate, commemorates his several contributions. Blakiston's Fish Owl was named in his honour.

A Denisovan signature in modern Tibetans

Tibetan family attending a horse festival (CC) Antoine Taveneaux 

Tibetans are adapted to life at high altitude. Compared to more recent arrivals, notably Han Chinese, they have much lower rates of fetal growth restriction and fewer pregnancy complications (reviewed here).

For non-adapted populations, long-term residence and high altitude can lead to chronic mountain sickness, which is characterized by high levels of haemoglobin. However, the erythropoietic response to low ambient oxygen is blunted in Tibetans. Recent studies have ascribed this to a variant allele of EPAS1, the gene that encodes hypoxia-inducible factor 2alpha (HIF2a) (here).

In the current issue of Nature, Huerta-Sanchez and others confirmed that the gene had a highly unusual haplotype in Tibetans (here). It occurred rarely in Han Chinese and was entirely absent in a larger set of worldwide populations. Interestingly, however, it could be detected in the genome af an ancient hominin population, the Denisovans (see previous post). The conclusion drawn is that the EPAS1 haplotype of Tibetans derives from admixture between modern humans and Denisovans.  

A downside to long gestation periods

Giraffe with calves - John Storr (Wikimedia Commons)

Giraffes (Giraffa camelopardalis) and the forest-dwelling okapi (Okapia johnstoni) are the survivors of a much broader radiation. Recently Clauss and Rössner (here) used the New and Old Worlds (NOW) data base of fossil mammals to examine the prevalence of various types of ruminant over time.

Rise and fall of tragulids 

The most basal group is Tragulidae, represented by present day chevrotains or mouse deer. In the Early Miocene they were the most prevalent ruminants but were subsequently displaced by the pecorans. The principal difference was the evolution in pecorans of an additional forestomach, the omasum, and this seems to have given them the edge over tragulids. 

Both tragulids and pecorans have synepitheliochorial placentation where binucleate trophoblast cells fuse with uterine epithelial cells at the fetal-maternal interface. However, tragulids lack the cotyledons typical of the placenta in pecorans.

Rise and fall of giraffoids

Among pecorans, Giraffidae is basal to both Bovidae (cattle, sheep, antelopes) and Cervidae (deer). Looking at the equivalent fossil clades, Clauss and Rössner found that Giraffoidea were much more  abundant in the later Early to Middle Miocene but then steadily declined to be supplanted by Bovoidea in Africa and by Bovoidea and Cervoidea in Eurasia. Why?

Based on extant species, the most striking difference between giraffids and other pecoran ruminants is their extremely long gestation - in excess of a year. Assuming this also was the case in fossil species, could that explain their decline? Clauss and Rössner argue that they were unable to develop a seasonal breeding pattern. This put them at a disadvantage compared to other pecorans with shorter gestation times such as bovids and cervids.  

Perhaps in support of this narrative, fossil giraffoids occupied a much greater range of ecological niches and many were grazers. The giraffes grew a long neck and survived as browsers in a special niche. The okapi is highly adapted to its restricted forest habitat.

Placentation in the giraffe has recently been described (see previous post).   

Menstruation in elephant shrews

Etendeka Round-eared Elephant Shrew or Sengi Macroscelides
micus. Image credit John P. Dumbacher
 

This post is prompted by the discovery in Namibia of a new species of elephant shrew or sengi, the smallest yet of the 19 species in the Order Macroscelidea. Elephant shrews are so named because of their mobile proboscis.





Midgestation conceptus of the Four-toed Elephant Shrew Petrodomus
tetradactylus. The embryo and fetal membranes are enclosed in the embryo
chamber by the decidua pseudocapsularis. Reproduced from
Oduor-Okelo et al. (here) (c) 2004 with permission from Elsevier

The report (here) mentions two pregnant females carrying one fetus in each horn. This suggests they may resemble other elephant shrews in that implantation of the blastocyst occurs in a preformed embryo chamber as shown above for Petrodumus tetradactylus. There is one such chamber in each horn. 

 

Should a female fail to become pregnant, the chamber is discarded in a process akin to menstruation. In most mammals transformation of the endometrial stroma to decidua occurs only following implantation. Exceptions are the catarrhine primates, including humans; if pregnancy does not ensue the decidua is shed together with blood and fluids (see previous post). In the 1940's, when human menstruation was poorly understood, Professor C. J. van der Horst of the University of Witwatersrand proposed using elephant shrews as a model. His suggestion was not followed as the establishment of a breeding colony of macaques at the Carnegie Institution of Washington provided a better alternative.

 

Placentation in elephant shrews was studied by van der Horst and others and more recently has been described by Dominic Oduor-Okelo (here and here). The placental disc has a labyrinth with a haemochorial structure and a spongy zone. In addition there is a paraplacenta. The allantoic sac is large and divided into four lobes. This last feature is a synapomorphy for the superordinal clade Afrotheria (discussed here).



Placental hormones and syncytins in the blind mole rat

A blind mole rat Spalax ehrenbergi
(Wikimedia Commons)

Mole rats (Spalacidae) occupy a basal position in the superfamily Muroidea. The blind mole rats, Spalax spp., are highly adapted to a subterranean lifestyle. They are resistant to both spontaneous cancer and carcinogens. For all these reasons they are widely studied and now we have a description of the genome of one species S. galili and the placental transcriptome both of that species and of S. carmeli (here).

Placental hormones

Placental-specific genes known from mouse and rat (Muridae) include cathepsins, placental lactogens (derived through duplication of the prolactin gene) and pregnancy-specific glycoproteins (reviewed here). Orthologues of many of these genes were present in Spalax and given the basal position of Spalacidae this indicates they had started to diversify in the last common ancestor of the muroid rodents.

Syncytins

Syncytins are endogenous retroviral envelope proteins thought to be essential for the formation of syncytiotrophoblast (previous post). Two such genes are known from mouse, rat (Muridae) and hamster (Cricetidae). Both are present in the Spalax genome although only Synb was confirmed in the placental transcriptome. This extends the timing of the env gene capture further back in time to an estimated 45 Mya.

Globin genes

Beta globin genes code for the two chains of haemoglobin molecules. One of them HBG is expressed in the embryo of most mammals but in the fetal haemoglobin of higher primates (discussed here). The HBG of Spalax shows evidence of rapid sequence evolution under positive selection. It is not clear to what extent this affects its affinity for oxygen.

Placentation in a marmot: the woodchuck

Woodchuck or groundhog (Marmota monax)
CC Wikimedia Commons

Not much has been written about placentation in squirrels and other sciuromorph rodents - at least in comparison to myomorphs (e.g. mouse, hamster) and hystricomorphs (e.g. guinea pig, capybara). Marmots belong with chipmunks and ground squirrels in the Tribe Marmotini. The most complete description is for the thirteen-lined ground squirrel (Ictidomys tridecemlineatus) (Mossman & Weisfeldt Am J Anat 1939;64:59-109). It was based largely on specimens collected a century ago by Thomas George Lee (background here).

Interhaemal region in the labyrinth of a woodchuck placenta
Marmota monax Courtesy of Dr. Allen C. Enders

The woodchuck has a labyrinthine, haemochorial placenta. In the above section the large channels with maternal red cells are lined by syncytiotrophoblast. A fetal capillary is seen to the right.

Early Development of the placenta in the Colorado chipmunk
Tamias quadrivittatus Courtesy of Dr. Allen C. Enders

There are several ways to make a haemochorial placenta (discussed here). Squirrels go through a transient endotheliochorial phase. The figure is from a chipmunk and shows a maternal capillary in which part of the endothelium has been replaced by syncytiotrophoblast whilst two endothelial cells remain intact (further figures here). In the first instance this creates the equivalent of the spongy zone found in other rodent placentas.

Later the fetal mesoderm grows into the trophoblast bringing with it the fetal capillaries. To start with the outgrowths are fingerlike (villi) as can be seen in a recent publication on the woodchuck (here). Nearer term, however, the labyrinth occupies most of the depth of the placenta. The spongy zone is then very thin and occupied by syncytiotrophoblast with clumps of nuclei as well as mononucleate giant cells (Dr. Allen C. Enders, personal communication).

Syncytins are endogenous retrovirus envelope genes (previous post). Two occur in murid rodents and another in South American hystricomorphs. Now a search of the genome of the thirteen-lined ground squirrel has turned up several candidates and further work in the woodchuck has shown one of them to be a bona fide syncytin. By in situ hybridization the gene was not expressed in the labyrinth but rather in the part of the spongy zone that had yet to be reached by the fetal vessels.

Evolution of Neotropical primates

Geoffroy's spider monkey (Ateles geoffroyi)
Wikimedia Commons

Derek Wildman's Group at Wayne State University have re-examined the evolution of Neotropical primates (here). Using genomic data from 36 species they derive a tree with few surprises but better support than in other recent analyses.

What I found interesting is their attempt to place platyrrhine evolution in a biogeographical context. They suggest that the most recent common ancestor of extant species lived in what today is the Amazon rain forest, Guiana Shield and Northern Andes. Then, however, this was largely an area of lowlands and mountains. In support of their interpretation, known fossil sites are within this region. They further suggest that diversification of platyrrhines occurred with the establishment and development of the Amazon rain forest. 


Placenta of the white fronted capuchin (Cebus albifrons)
From Carter and Mess (here)

The founder of the Neotropical primates arrived in South America during the Oligocene when the continent was completely isolated from other land masses. Personally I favour the view (espoused here) that they came by a transatlantic route. However, Jameson Kiesling et al. suggest they may have come directly from Asia. In support they cite the occurrence of all the early fossils on the west side of the continent and recent evidence that platyrrhines may have emerged in Asia rather than Africa. In either case the means of dispersal was most likely by rafting (see previous post on sweepstakes distribution).




Homo habilis - fiftieth anniversary

Homo habilis the handy man (Wikimedia Commons)

An article in the current issue of Nature (here) reminded me that 50 years have passed since Louis Leakey, Phillip Tobias and John Napier published their controversial paper, "A new species of the genus Homo from Olduvai Gorge" (here). Until then most fossil hominins had been accomodated in the genera Australopithecus and Pithecanthropus. Whether or not the new fossils justified the title of Leakey's paper was disputed then and remains contentious.

As I wrote at the time, "There are two criteria that might be used to define man: his ability to make tools and the size of his brain. Homo habilis scores on the first point but not on the second" (Carter AM. A new ancestor for man. The Humanist 1964; 79: 198-201).

Happy Birthday Jane Goodall

I was reading anthropology while the paper was being written and was taught by both Phillip Tobias and John Napier. I also met Louis Leakey on one of his visits to Cambridge - probably angling for a job - and was introduced to his protégée, the then unknown Jane Goodall (whose 80th birthday is today).

Anna-Riitta Fuchs

Anna-Riitta Fuchs (1926-2014)

Anna-Riitta Fuchs was a reproductive endocrinologist whose great interest was the control of parturition. Much of her work centred on the posterior pituitary hormone oxytocin and its receptors in the myometrium.

I first met Anna-Riitta and her husband Fritz at their laboratory in Copenhagen shortly before they relocated to New York. I was a very green graduate student back then but was received with great warmth as they patiently explained their work on parturition in the rabbit. Those were heady times when a great debate was raging about the most important determinant of birth: was it oxytocin release or the withdrawal of progesterone from the placenta?

Anna-Riitta's many achievements include a D.Sc. from the University of Copenhagen and the Carl G. Hartman Award from the Society for the Study of Reproduction. Anna-Riitta was born 1926 in Helsinki and died last week in New York. A full obituary can be found here.

Endogenous retroviruses expressed by ovine trophoblast

Urial Sheep (Ovis vignei)
Wikimedia Commons

Jaagsiekte sheep retrovirus (JSRV) is a nasty pathogen causing lung tumours in sheep. No fewer than 27 JSRV-related endogenous retroviruses (enJSRVs) occur in domestic breeds. Gene capture is an ongoing process and the distribution of enJSRVs has been exploited to test hypotheses about the domestication of sheep (here). For example, the most common variant (enJSRV-18) is absent in ancestral breeds such as the Urial (above) and Mouflon. Although found in goats, enJSRVs are not present in cattle so are much younger than a syncytin recently described by Cornelis et al. for ruminants (here).

Five enJSRVs are capable of transcription and like syncytins (previous post) they have an env gene. Are they then "nascent syncytins" as suggested by Cornelis et al., or do they already subserve a function in the ovine placenta?

A period of blastocyst elongation precedes implantation in sheep and binucleated trophoblast cells first appear then. enJSRV mRNAs are detectable at this stage and later are expressed in binucleate trophoblast cells as well as in the syncytial plaques formed by fusion of those cells with uterine epithelial cells (reviewed here).

Moreover, when antisense oligonucleotides were used to block enJSRV protein production, differentiation of binucleate cells was inhibited (here). The more i read about endogenous retroviruses the more intrigued I become.

Blood supply to brain and placenta in the capybara

Capybara (Hydrochoeris hydrochaeris)
Wikimedia Commons

The current issue of Science (here) draws attention to recent work on the blood supply to the brain in capybaras. As in other mammals young capybaras have a dual supply from the internal carotid arteries and the basilar artery. At one year of age, however, remodelling of the internal carotid shuts down that source and the basilar artery becomes the sole source of blood to the brain. Research on the underlying mechanisms is being conducted at the Department of Surgery at the Veterinary School in Sao Paulo (here).

The Department is also home to a vibrant research group led by Angelica Miglino with whom it has been my privilege to collaborate on the blood supply to the capybara placenta (here and here).

Placentation in the capybara from Kanashiro et al.
Reprod Biol Endocrinol 2009 (here)

Like other hystricognath rodents, capybaras have a discoid, labyrinthine, haemochorial placenta with an inverted yolk sac that persists to term. An additional feature shared with other hystricognaths is the subplacenta (sub in panel D above). With Claudia Kanashiro we published a detailed study of this structure in the capybara (here). 

It is encouraging to see Science advocate the capybara as a model for stroke. In view of its size - at around 65 kg it is the largest living rodent - it might be useful as a model for fetal physiology. As shown in a previous post on the guinea pig, hystricognaths have precocial young and are in this respect more satisfactory models for gestation than mice and their kin. 

Ten thousand birds

Birkhead, Wimpenny and Montgomerie
Princeton University Press 2014 ISBN 978-0-691-15197-7

Because a bird has no placenta, Eggs is how this world they enter (Simon Drew). Yet it would be remiss of me not to mention this lucidly written and lavishly illustrated narrative of the history and philosophy of ornithology.

The opening chapter, "Yesterday's Birds," is a fascinating account of the progression of ideas on the origin of birds, including the influence of the Danish artist and self taught palaeontologist Gerhard Heilmann, who surmised birds evolved from thecodonts (Pseudosuchia). The alternative view of birds as dinosaurs (BAD), promoted in the 1970's, was slow to take hold. A related story concerns the origin of feathers, which were long thought to be highly modified scales but now are seen as a novel evolutionary development. The chapter brings us up to date with feathered but flightless dinosaurs, including superb fossils from China, the colours of fossil feathers and the different type of keratin that distinguish scales from feathers.

One word of caution: despite the title this is not an overview of the various families of birds although it does contain many paintings and photographs to delight the eye of the amateur ornithologist (a group not recognized by the authors to whom ornithologists are scientists and the rest mere bird watchers).

Trophoblast Research

A new issue of Trophoblast Research has just appeared. Entitled "Models for Molecular Understanding of Placental Development and Associated Disorders," it reports the proceedings of IFPA Meeting 2013 at Whistler, British Columbia.

There are 15 review articles and three comprehensive workshop reports all open access. To view them go to the Placenta web site and scroll down until you find the above image in the left side bar.

Disclosure: I am Editor of Trophoblast Research.

Tempers ran hot over tarsiers

Philippine tarsier (Tarsius syrichta)
Jasper Greek Golangco

A recent post dealt with controversy over the evolution of placentals. This is nothing new. In 1897 debate ranged in the pages of Science about whether tarsiers belonged with lemuroid or anthropoid primates. It was sparked by the work of Hubrecht, who claimed that the embryological development of tarsiers resembled that of higher primates. He pointed to the precocious development of the extraembryonic mesoderm as well as the absence of an allantoic sac and its replacement by the connecting stalk.

Skull of Anaptomorphous

Had he stopped there all might have gone well. But Hubrecht proceeded to give a new interpretation of the primate fossil record, in particular Anaptomorphous homunculus (now placed in Omomyidae). This raised the ire of Charles Earle, curator of fossils at the American Museum of Natural History. He argued on the basis of osteological characters and dentition that tarsiers might represent an intermediate stage between lemuroids and anthropoids but certainly did not belong with the latter (here). In a spirited reply (here), Hubrecht wrote, "It is, indeed, rather hard upon me...to be now pilloried by Mr. Earle as if I had been making that coarse and indiscriminate use of placentary characters in classification against which I have been all the time loudly protesting."

In the next exchange (here), Earle argued for the superiority of palaeontological over embryological methods in determining phylogeny. He rather spoiled the effect by presaging one argument, "On this side of the Atlantic..."

As a footnote it is worth observing that there remain huge gaps in the fossil record of primates and the position of Anaptomorphous is still open to alternative interpretations. Meanwhile Hubrecht's view has triumphed over Earle's with primates split in Strepsirrhini (the lemuroids) and Haplorrhini (tarsiers and anthropoid primates). 

New species of river dolphin

The Araguaian boto (C) Nicole Dutra

The boto, Inia geoffrensis, popularly known as the pink dolphin, is widely distributed in the rivers of the Amazon basin. It is also found in the Araguaia-Tocantins river basin. Since the two basins became disconnected at the Pliocene-Pleistocene boundary, Tomas Hrbek and colleagues (here) asked if this really was the same species. They analysed morphological and molecular data (including mitochondrial genes), concluded that the Araguaian boto was a distinct species and named it Inia araguaiaensis. In addition they proposed that the boto found in the Bolivian sub-basin be raised from subspecies to species status as Inia boliviensis.     

Distribution map of species and subspecies of Inia
From Hrbek et al. PLoS ONE 2014: 9: e83623
(c) Hrbek et al. (Creative Commons)

Some time ago Dr. Vera da Silva, a co-author of the new study, afforded me the opportunity to study placentation in the boto and also the tucuxi (Sotalia fluviatilis), another dolphin found in the Amazon (here).


Placenta of the boto
From da Silva et al. RBE 2007; 5: 26

For more about these creatures including their place in folklore I recommend Journey of the Pink Dolphins: An Amazon Quest by Sy Montgomery.

More debate on the origin of placentals

The first placental mammal
From O'Leary et al. Science 2013; 339: 662-7
Reprinted with permission from AAAS

Controversy over the timing of the mammalian tree (previous post) continues. The latest contribution, by Mario dos Reis et al. (here), boldly states, "O'Leary et al. seek to reignite a controversy over the age of the placental ancestor that otherwise has been settled." The italics are mine. The references that support this statement are a paper by the same authors and one by Meredith et al. No false modesty here.



Alternative calibrations of the same tree
From dos Reis et al. Biol Lett 2014; 10: 20131003
(c) The authors (Creative Commons)

The problem arises because of different approaches to calibration of the molecular clock. The figure shows trees with identical topology but dated with different sets of fossils. In the first three, many extant orders of mammal can trace their origin to the Late Cretaceous. The problem is that all known fossils of placentals date from after the mass extinction event at the Cretaceous-Paleogene boundary. A literal interpretation of the fossil record, on the other hand, has all orders and even placentals themselves postdating the boundary.
It is not easy to choose appropriate fossils for calibration. Dos Reis and colleagues criticise O'Leary et al. for placing too much weight on Protungulatum donnae. They point out that the fossils of the genus may be found in the Cretaceous, yet the authors they cite (here) are unsure whether or not Protungulatum is a placental.

For a sober discussion of the difficulties in fossil calibration I highly recommend a recent paper by Bibi (here) on the evolution of ruminants. En passant Bibi observes, "The problem stems in part from the opacity of paleontological literature to non-specialists."

The O'Leary paper is co-authored by some of the most eminent specialists in fossil mammals. Arraigned gainst them we have some of the most competent molecular phylogeneticists. There seems little chance of compromise to judge from the acrimonious tone in this latest contribution. Surely the reviewers and editor of Biology Letters could asked the authors to damp things down?
     

Was Homo erectus the fourth hominin?

Skull of Homo erectus (Wikimedia Commons)

The current issue of Nature has a comprehensive analysis of the genome of Neanderthals and comparisons with modern humans and Denisovans (here). The supplementary material alone fills 16 Mb but there is an excellent summary (here) entitled "Four makes a party." As it says, "it does seem that Eurasia during the Late Pleistocene was an interesting place to be a hominin, with individuals of at least four quite divergent groups living, meeting and occasionally having sex."

The fourth hominin was alluded to in a previous post and is inferred from analysis of the Denisovan genome (previous post). The current study estimates that this putative hominin's ancestor diverged from other hominins 0.9-1.4 million years ago. This date is compatible with the unknown hominin being Homo erectus a hominin well known from the fossil record.