An ancient endogenous retrovirus

Classes of ERVs Wikimedia Commons

Endogenous retroviruses (ERVs) are genes of retroviral origin that have been incorporated into the genome. They include the syncytins expressed in the placentas of various mammals. Six are known so far and each represents a separate capture of a retroviral gene (see previous post). 

Now an ERV has been described that occurs in representatives of all four superordinal clades of placental mammal (here). In this case the gene is orthologous and thus represents a single integration event that must have predated the divergence of placental mammals in the Cretaceous (for possible dates see my recent post).

This work was published in a special issue of Phil Trans R Soc B on the theme "Paleovirology: insights from the genomic fossil record." Although sequence substitutions occur over time, an ERV is essentially a "fossil" record of a virus as it existed at the time of incorporation into the host genome. Thus the study of ERVs in various organisms (not just mammals) can provide insight into the long term history of viruses and virus-host interactions (see overview here).

In a historical overview of the field (here) Robin A. Weiss notes, "The advantage to the host of ERV protein expression is most dramatic in the evolution of the mammalian placenta." Incidentally, if you find the whole concept hard to swallow you are in good company as the early history of the field so clearly shows.

The Mammalian Ovary

Mossman and Duke 1973

It is now 40 years since publication of Harland Mossman's "other" book (previous post). It differs in many respects from the better known volume on fetal membranes. In particular it is richly illustrated with photomicrographs. Most of the specimens were in the collections of its authors. The Harland W. Mossman Collection is conserved at the University of Wisconsin Zoological Museum and there is a searchable data base (here).

Kenneth L. Duke was an alumnus of Brigham Young University at Provo, Utah. On retiring from Duke University he sent his collection there. Mercifully it has remained intact although it has not been catalogued. Much of the material will be from Duke's yearly field trips to The Great Basin but there is also material from South East Asia. There are placentas from some species including the Philippine colugo.

Comparative Morphology of the Mammalian Ovary takes as a starting point the red squirrel (Tamiasciurus hudsonicus) before dealing with a number of topics across the full range of mammals. For individual taxa the synoptic tables at the back of the book are unsurpassed as a source. The footnotes to these tables indicate where they rely on Duke's Collection now at BYU.

Disclosure: I am adjunct curator of The Harland W. Mossman Collection.    

Alternative views on the origin of placentals

The first placental mammal

From O'Leary et al. Science 2013; 339: 662-7

Reprinted with permission from AAAS

Hot on the heels of the controversy about crown mammals comes a dust up over crown placentals. This time in Science and in response to an important paper by O'Leary et al. that combined morphological and molecular data (see previous post). One conclusion in that paper (here) was that ordinal diversification of placentals occurred after the Cretaceous-Paleogene boundary (Explosive Model, cf. Wednesday's post).

This has elicited a response from an eminent group of molecular phylogeneticists (Springer et al. here). Their best estimate of the origin of placentals (here) posits a common ancestor 100 Mya with most orders arising in the Cretaceous (Long Fuse Model). They contend that that molecular phylogenies are more reliable than phenome-based (morphological) phylogenies even when they imply ghost lineages (i.e. with no fossil record).

In their rebuttal, O'Leary et al. (here) note that molecular phylogenetics has failed to resolve the basal split in Placentalia (see here) or to establish a sister taxon for primates. Thousands of nonplacental Cretaceous fossils are known so why are placentals absent? 

A seemingly weightier point made by Springer et al. is that ordinal diversification over a short time span in the early Paleocene implies high substitution rates. Maybe so respond O'Leary et al. Let's redo our tree but impose average substitution rates as a limitation. The result is to extend the origin of orders past the K-Pg boundary but only by some 6 My. That puts the common ancestor at 70 Mya which is still 30 My later than the molecular estimate.

New fossils support alternative views of mammalian evolution

Alternative interpretations of early mammalian history

Reproduced with permission by Macmillan Publisher Ltd.

from Cifelli and Davis (here) copyright 2013

Crown Mammalia are the extant monotremes, marsupials and placentals together with all extinct species with which they share a common ancestor. It is widely accepted that they include the multituberculates that became extinct in the Oligocene.

Two well preserved Jurassic fossils from another group of mammaliforms, the haramiyids, are described in the current issue of Nature. In one paper (here) the fossil form (Arboroharamiya jenkinsi) is found to group with the multituberculates and thus within Crown Mammalia. Since the haramyids have a deep fossil record this pushes the common ancestor of crown mammals back into the Late Triassic.

The second analysis (here) of a different fossil (Megaconus mammaliaformis) places haramiyids outside crown placentals, which thus can retain a Jurassic origin.

An accompanying commentary (here) notes that a Triassic origin is in accordance with the "long fuse" hypothesis of mammalian evolution whereas a Jurassic origin better corresponds to the "explosive" hypothesis. These authors tend to favour the conclusion based on Megaconus as it is a more complete fossil and the counterparts of the middle ear bones remain attached to the mandible, differing in this respect from extant mammals and multituberculates.

Placentation in colugos

Colugo fetus near term from Hubrecht (1919)

Colugos (once known as flying lemurs) are of interest because of their close relationship to primates. Dermoptera (colugos), Scandentia (tree shrews) and Primates group together as Euarchonta.

Dilated maternal blood spaces in a colugo placenta

Hill Collection micrograph courtesy of Allen C. Enders

Their placentation is of interest because it seems to be intermediate between a labyrinthine and villous form. Starck referred to it as a Zwischenform and Wislocki compared it to the trabecular placenta of Neotropical primates. This not withstanding, we still lack a complete description of the term placenta. Mossman (previous post) could not reconcile his own observations with unpublished drawings by Luckett and urged further study. 

Hubrecht (previous post) accumulated 182 uteri of the Sunda colugo (Galeopterus variegatus). His thorough description of early fetal development, published posthumously (Verhandelingen der Koninklijke Akademie van Wetenschappen 1919), stopped at the establishment of the definitive placenta. J. P. Hill collected specimens of the Sunda colugo and the Philippine colugo (Cynocephalus volans) but did not describe them. Nor did Amoroso (previous post) who apparently borrowed most of Hill's slides. The time is ripe for a thorough study of colugo placentation.