New genomic estimate misses monotreme-marsupial split by 43 million years

Summary for those in a hurry:
Fossils provide hard evidence. Deep time gene studies provide estimates and false positives too often to trust them.

Zhou et al. 2021 report:
“Our phylogenomic reconstruction shows that monotremes diverged from therians around 187 million years ago, and the two monotremes diverged around 55 million years ago. This estimate provides a date for the monotreme–therian split that is earlier than previous estimates (about 21 million years ago, but agrees with recent analyses of few genes and fossil evidence.”

Let’s stop putting our faith in estimates derived from genomic deep time studies that have proven themselves to be wrong too many times. Here, the Zhou et al. estimate is at least 43 million years too late (Fig. 2) based on Brasilitherium (Fig. 3) fossils and the tree topology recovered by the LRT (Fig. 1).

Figure 1. Subset of the LRT focusing on Metatheria (marsupials) including Paedotherium and Adalatherium.

By contrast with Zhou et al. 
Morganucodon (Late Triassic, 205mya, Fig. 4) is a basal marsupial in the large reptile tree (LRT, 1790+ taxa; subset Fig. 1) based on phenomic (= trait) analysis that includes fossil taxa. Genomic tests are infamous for false positives when dealing with deep time taxa.

Figure 2. Select basal cynodonts and mammals set chronologically. The divergence times for placentals (Eutheria), marsupials (Metatheria) and monotremes (Mammalia) are estimated here.

Brasilitherium,
(Figs. 3, 4) from the Early Norian, Late Triassic, 225mya, is a derived monotreme in the LRT. That means it lived AFTER the monotreme-therian split which must have occurred at least 230mya.

Figure 3. Brasilodon compared to Kuehneotherium, Akidolestes and Ornithorhynchus, the living platypus.

As everyone knows
the platypus and echidna are highly derived monotremes. Megazostrodon (Fig. 4) is the last common ancestor (LCA) of all monotremes and all mammals. Megazostrodon was a Late Jurassic late survivor of that earlier (Middle Triassic?) radiation.

Figure 4. Basal mammals and their proximal ancestors. Here taxa below Megazostrodon are mammals. Those above are not. Hadrocodium is uniquely reduced, but this occurs within the Mammalia.  The dual jaw joint was tentatively present in Pachygenelus.

According to the LRT,
there was no gradual ascent of monotremes leading to marsupials. Rather the monotreme-marsupial split occurred at the origin of mammals and monotremes. How this affects the genes for lactation discussed in the Zhou et al. paper is beyond the scope of this blogpost.

The purpose here
is to emphasize the importance of a broad, proper and valid phylogenetic context before proceeding to the narrow focus of your interests. 42 co-authors using cutting edge genomic techniques hobbled their otherwise excellent and in-depth report by skipping step number one.

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References
Zhou Z et al. (41 co-authors) 2021. Platypus and echidna genomes reveal mammalian biology and evolution. Nature https://doi.org/10.1038/s41586-020-03039-0

 

Priacodon: How to tell a crown mammal from a mammal mimic

Jäger et al. 2020 discuss ‘molar’ occlusion
in a tiny taxon, Priacodon fruitaensis (LACM 120451, Fig. 1), they said was a crown mammal (a clade with living relatives). Priacodon is principally represented by a mandible with teeth and a maxilla with teeth. Triconodont ‘molar’ cusps are three in number and aligned like a row of three knives distinct from basal cynodonts and basal mammals.

Figure 1. Priacodon µCT scans from Jäger et al. 2020. Colors and restoration added. This looks like a mammal jaw. The LRT nests it with mammal mimics. That’s an odd sort of canine with more than one cusp.

The authors wrote: 
“Triconodontids are a clade of the eutriconodontans which is a clade of early crown mammals with a fossil record from the Late Jurassic through the Late Cretaceous.”

So this clade had plenty of time to develop their unique teeth and convergent jaw joints alongside crown mammals (= monotremes + marsupials + placentals).

By contrast 
the large reptile tree (LRT, 1786+ taxa, subset Fig. 4) nested Priacodon and kin like Sinocodon (Fig. 2), within a clade of mammal mimics arising from the cynodont,  Pachygenelus, and preceding the Last Common Ancestor of all living mammals, Megazostrodon (Fig. 5). That LCA status makes Megazostrodon the most primitive of crown mammals. Any taxa preceding Megazostrodon are excluded from crown mammals. A valid cladogram is needed to place taxa within a crown clade or outside it. Jäger et al. did not provide a cladogram.

Wang et al. 2001 provided a traditional cladogram of mammals and pre-mammals. That was invalidated in 2016 by the addition of taxa to the LRT.

The single replacement of milk teeth with adult teeth
also marks Megazostrodon as a mammal because toothless hatchlings are initially feeding on their mother’s mammary glands, but that’s beside the point. That’s a trait, not a phylogenetic nesting  node.

Figure 2. Sinoconodon growth series including jaws and teeth, here colorized from Zhang et al. 1992. Note the lack of tiny post-dentary bones in this mammal-mimic.

Unfortunately,
this is a continuing problem in mammal paleontology going back before Repenomamus (Fig. 3), an Early Cretaceous mammal-mimic, typically considered the largest mammal in the Cretaceous. According to Wikipedia, “Repenomamus is a genus of triconodonts, a group of early mammals with no modern relatives.” According to the LRT, they have no living relatives because they are pre-mammals or mammal-mimic cynodonts.

Tiny post-dentary bones
This is a classic case of “Pulling a Larry Martin” because both Repenomamus and Priacodon have a certain trait shared with mammals by convergence. They lack the small post-dentary bones thought to be lost only in mammals. As a result they also have a dentary-squamosal jaw joint. The authors put all their money on this single trait and did not recognize the possibility of convergence. They didn’t provide a phylogenetic analysis that included all pertinent taxa.

In counterpoint, 
Megazostrodon (Fig. 5) retains tiny post-dentary bones. These ultimately migrate to help form the middle ear bones of higher mammals.

A few years ago
I had a chat with co-author R Cifelli in Oklahoma with regard to the nesting of multituberculates in Glires in the LRT. Multis redevelop tiny post-dentary bones by reversal according to the LRT, which tests a suite of 235 traits from head to tail. Cifelli wasn’t ready to consider non-traditional solutions based on an expanded taxon list and the possibility of a reversal.

Figure 3. Repenomamus reconstructed using DGS methods. The manus and feet are loose figments at present. Despite its predatory nature, note the reduction in canines, a clade trait.

Relatives of Sinoconodon replace their teeth multiple times,
(Fig. 2) as in cynodonts and reptiles in general. But even if they had single tooth replacement, their nesting on the LRT apart from crown mammals indicates they are not crown mammals, but mammal-mimics. Like Repenomamus (Fig. 3) and Priacodon (Fig. 1), Sinoconodon also lacked tiny post-dentary bones and had a dentary-squamosal jaw joint.

In their conclusion, the Jäger et al. note:
“Triconodontidae exhibit a molar series that is unique among mammals and is not directly comparable to any extant counterpart.” That’s because triconodonts are not related to extant counterparts, aka: crown mammals. These esteemed authors “Pulled a Larry Martin” by putting a few traits ahead of a suite of hundreds of traits in a phylogenetic analysis.

Convergence runs rampant in the LRT.
The LRT weeds out convergence. That’s why you need to run your own analysis and expand your own taxon list. Don’t rely on a few traditional traits.

Figure 4. Subset of the LRT from 2019 focusing on the Therapsida. Red taxa were tested separately due to too few characters known for a permanent place in the LRT.

Whatever Jäger et al. discovered
by closely examining the occlusal pattern in Priacodon, their study was hobbled by their invalid assignment of Priacodon to the clade crown Mammalia. Despite years in this profession, they had no idea that triconodonts were mammal mimics. To avoid problems like this, get a wide-angle view before setting up your microscopic views.

Figure 5. Megazostrodon skull in several views. Drawings from Gow 1986. Colors applied here.

Taxon exclusion continues to be the number one problem in paleontology,
as you can see dozens of times if you click here: keyword: taxon+exclusion.

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References
Jäger KRK, Cifelli RC and Martin T 2020. Molar occlusion and jaw roll in early
crown mammals. Scientific Reports (2020) 10:22378 https://doi.org/10.1038/s41598-020-79159-4
Wang Y-Q, Hu Y-M, Meng J and Li C-K 2001. An ossified Meckel’s cartilage in two Cretaceous mammals and origin of the mammalian middle ear. Science 294:357–361.

wiki/Crown_group
wiki/Repenomamus
wiki/Priacodon

The most basal mammal in the LRT: Megazostrodon

I thought for many years
that Megazostrodon was known from only a fragment of skull, lacking both the anterior and posterior parts.

Then somehow this paper popped up on the Internet
Gow 1986 illustrated the skull of Megazostrodon (Fig. 1; BPI/1/4983; Crompton & Jenkins, 1968; Latest Triassic; 200 mya). Even without this skull data the large reptile tree (LRT, 1293 taxa) nested Megazostrodon at the base of the Mammalia. There is little  argument among paleontologists that this taxon is a close sister to the last common ancestor of all living mammals.

Often wrongly associated
with Morganucodon, the two are phylogenetically separated from one another by tiny Hadrocodium in the LRT. In Megazostrodon the zygomatic arch is straight (without the ascending arch). The skull lacks a sagittal crest.  As in modern marsupials, carnivores, primates and tree shrews the teeth have a standard incisor, canine, premolar and molar appearance. The permanent molars occlude precisely. Uniquely (as far as I know), the dentary has a coronoid boss and a coronoid process.

Figure 1. Megazostrodon skull in several views. Drawings from Gow 1986. Colors applied here. The upper molars are worn down.

The large reptile tree
(Fig. 2) presents a simple, validated topology of mammals and their ancestors based on hundreds of traits, very few of them dental. It differs in nearly every regard from the Close et al. 2015 study, which employs many dental taxa.

Figure 3. Subset of the LRT focusing on the Kynodontia and Mammalia. Non-eutherian taxa in red were tested in the LRT but not included because they reduce resolution. Eutherian taxa in red include a basal pangolin and derived xenarthran, clades that extend beyond the bottom of this graphic. The pink clade proximal to mammals was considered mammalian by Lautenschlager et al. due to a convergent mammalian-type jaw joint.

The first time I reconstructed Megazostrodon
(Fig. 4) the skull looked legit, and was approved by cynodont expert Jim Hopson, but it had some problems. I’m glad to finally get better data on this, that resolves scoring problems around this node.

Figure 4. Megazostrodon, an a Jurassic mammal, along with Hadrocodium, a Jurassic tiny mammal. The Megazostrodon skull shown here is not correct.

On a side note:
Wikipedia reports,“Tinodon (Marsh 1887; YMP11843) is an extinct genus of Late Jurassic mammal from the Morrison Formation. It is of uncertain affinities, being most recently recovered as closer to therians than eutriconodonts but less so than allotherians.” 

Figure 5. Tinodon is best represented by an incomplete mandible with affinities to basal mammals and basal metatherians. Image from Morphobank.

 

Too few characters are present here
to add it to the large reptile tree, but if I have restored the missing parts correctly, then it is close to the base of the Mammalia and Theria near Megazostrodon.

References
Close RA, Friedman M. Lloyd GT and Benson RBJ 2015. Evidence for a mid-Jurassic adaptive radiation in mammals. Current Biology. 25 (16): 2137–2142. doi:10.1016/j.cub.2015.06.047. PMID 26190074.
Crompton AW and Jenkins FA Jr 1968. Molar occlusion in late Triassic mammals, Biological Review, 43 1968:427-458.
Gow CE 1986. A new skull of Megazostrodon ( Mammalia, Triconodonta) from the Elliot Formation (Lower Jurassic) of Southern Africa. Palaeontologia Africana 26(2):13–22.
Marsh OC 1887. American Jurassic mammals. The American Journal of Science, series 3 33(196):327-348

wiki/Megazostrodon

 

The origin of feathers and hair (part 2: hair)

Yesterday we looked at reptile skin and scales, alpha and beta-keratins and examined the fossil record of scales, naked skin and pterosaur extra dermal membranes. Today we’ll take on mammal hair.

Pre-mammals
Mammals, like Megazostrodon, evolved in the Jurassic from synapsid reptiles, like Archaeothyris, that first appeared in the Late Pennsylvanian.

Dhouailly 2009 reports: “The synapsid lineage, which separated from the amniote taxa in the Pennsylvanian about 310 million years ago, may have evolved a glandular rather than a scaled integument, with a thin alpha-keratinized layer adorned with alpha-keratinized bumps. Those bumps may have even presented some cysteine-rich alpha-keratins, precursors of the hair-type keratins. In addition, the first synapsids may have developed both a lipid barrier outside the epidermis, similar to current amphibians living in xeric habitats, and some lipid complex with the alpha-keratins of the stratum corneum as in current mammals as a means to strengthen the barrier against water loss of the integument.”

So reptilian scales were never part of the mammal legacy — just naked glandular skin.

Mammals
A dense coat of fur is found in all basal extant mammals, even those that lay eggs. Thus the origin of hair is to be found in the common ancestor of all living mammals, perhaps among therapsid-grade synapsids (Thrinaxodon – Chiniquodon), or, more conservatively, perhaps right at the origin of early Jurassic mammals.

Dhouailly 2009 reports: “No intermediate form has ever been found between scales and hairs, resulting in only a few proposals of how mammalian hairs may have evolved from scales. These proposals were based on the development of sensory bristles in the hinge scale region of reptiles.”  Unfortunately basal reptiles and therapsids did not have scales (see below).

The traditional cynodont whisker hypothsis
Foramina (tiny holes) on the faces of basal gorgonopsians, therocephalians and cynodonts have been interpreted as providing passages for nerves and blood vessels supplying movable skin (subcutaneous muscles) and sensory vibrissae (whiskers). This would represent the first appearance of hair only to be followed by more and more hair spreading around the body. This essentially duplicates the new hypothesis on feather origin by Persons and Currie (2015, see that discussion tomorrow).

Unfortunately for this hypothesis,
the basal lizard, Tupinambis has similar rostral foramina, yet it lacks sensory vibrissae (Bennett and Ruben 1986).

An alternate mammal hair genesis hypothesis
Given that pelycosaurs and Estemmenosuchus were naked and had no hair, the origin of mammal-type hair must have occurred closer to mammals. On their way to evolving into mammals, taxa like Pachygenelus and Megazostrodon became progressively smaller in a rather common process known as phylogenetic miniaturization (the opposite of Cope’s Rule).

Due to their increased surface/volume ratio, smaller animals find it more difficult to internally thermoregulate because their insides are closer to their outsides. Having insulating fur when tiny would be helpful. That’s the traditional hypothesis for mammal hair genesis in tiny taxa, like Megazostrodon. Unfortunately the insulation hypothesis gives no reason for the first appearance of tiny sprigs of precursor hair, not yet plentiful enough to trap air (for insulation). Nor does it take into account that the smallest of all basal mammals, their newborns, are hairless.

Dhouailly 2009 reports: “Hairs [may have] evolved from sebaceous glands, with the hairshaft serving as a wick to draw the product of the gland to the skin surface, strengthening the barrier against water loss.”

Figure 2. An automobile driver can sense the presence of a curb on approach when a “curb feeler” is in place. This saves wear and tear on tires. Similarly individual hairs would touch the inside of burrows before the skin comes into contact.

The curb-feeler hypothesis
As others have noted, individual hairs provide tactile feedback. Those are especially useful to nocturnal and burrowing animals.

Naked mole rats provide a good analogy. Like therapsids, naked mole rats burrow, adjust their internal temperature to ambient temperatures, AND they have only a few whisker-like hairs that crisscross the body to form a sensitive array that helps them navigate in the dark. We know that certain small cynodonts were  also burrowers. That’s where we find them. We don’t know if they had whisker-like hairs that crisscrossed their body. Only the bones are preserved.

In this way,
individual hairs would have been like curb-feelers (Fig. 2), small wires that make a noise whenever a 1950s era automobile approaches a curb. Thus provided, basal mammals could have avoided multiple abrasions while running through their tunnels using their own curb feelers.

Nevertheless,
if that’s how hair started, once provided with the ability to grow hair, simply growing more hair would have provided incremental opportunities to spend more and more time outside of the burrow. Hair insulated mammals not only from ambient temperature, but from the environment at large, including the approach of winged insects like flies and mosquitoes. Note that those insects that finally developed the ability to burrow past the hair barrier, fleas, lost their wings in order to do so.

Navigation skills
learned in dark tunnels could be readily transferred to leaf litter in the open air at night (all the while avoiding the predatory gaze of hungry Jurassic dinosaurs).

Figure 2. Opossum tail showing false scales. A couple of ‘curb feelers’ appear on the proximal tail.

The “scaly tail” of mammals,
like the opossum (Fig. 2), is actually, a criss-cross series of epidermal folds interspersed with hairs, not homologous with the scale of any other animal (Dhouailly 2009).

Figure 3. Naked mouse babies surround the furry mother mouse. The babies may be recapitulating evolution as they are naked and unable to maintain their own body temperature without a little help from mom.

The surprising origin of mammary glands
Dhouailly 2009 reports: “The mammary gland apparently derives from an ancestral sweat or sebaceous gland that was associated with hair follicles, an association which is retained in living monotremes, and transiently in living marsupials. The original function of the mammary gland precursor may not have been feeding the young, but as a means to provide moisture to the eggs.”

Tomorrow: dinosaur feathers.

References
Bennett AF and Ruben JA 1986. The metabolic thermoregulartory status of therapsids. In The Ecology and Biology of Mammal-like reptiles (Hottom, Roth and Roth eds) 207-218. Smithsonian Institution Press, Washington DC
Chudinov PK 1970. Skin covering of therapsids [in Russian] In: Data on the evolution of terrestrial vertebrates (Flerov ed.) pp.45-50 Moscow: Nauka.
Dhouailly D 2009. A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of Anatomy 214:587-606.
Persons WC4 and Currie PF 2015. Bristles before down: A new perspective on the functional origin of feathers.Evolution (advance online publication) DOI: 10.1111/evo.12634