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A Jurassic eutherian mammal and divergence of marsupials and placentals

August 2011
Nature 476(7361):442-5

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University of Chicago

Placentals are the most abundant mammals that have diversified into every niche for vertebrates and dominated the world's terrestrial biotas in the Cenozoic. A critical event in mammalian history is the divergence of eutherians, the clade inclusive of all living placentals, from the metatherian-marsupial clade. Here we report the discovery of a new eutherian of 160 Myr from the Jurassic of China, which extends the first appearance of the eutherian-placental clade by about 35 Myr from the previous record, reducing and resolving a discrepancy between the previous fossil record and the molecular estimate for the placental-marsupial divergence. This mammal has scansorial forelimb features, and provides the ancestral condition for dental and other anatomical features of eutherians.

Dental and mandibular features of Juramaia sinensis (BMNH PM1343B). a–d, Right upper M2 in mesial, occlusal, labial and distal views (composite restoration from both the right and the left sides). e, Stereo photographs of right premolars and molars. f, Stereo photographs of left premolars and molars. g, Right P3–M3 in occlusal view. h, Left upper dentition restoration in labial view. i, Left lower dentition (restoration) and mandible. Grey-shaded areas represent reconstruction from incomplete bone or tooth structure or mould outline in matrix. Abbreviations: ag, angular process; cod, coronoid process of dentary; dc; dentary condyle; M, m, upper and lower molars; mf, mental foramen; P, p, upper and lower premolars; dP3, deciduous P3 in situ. Terminology of tribosphenic molar follows 1.1 of ref. 1.

…

Time-calibrated phylogeny of the eutherian Juramaia among other boreosphenidan mammals, and comparative morphology of some key molar features. a, Basal eutherian and metatherian phylogeny from parsimony analysis of data set of ref. 24 (446 characters of 103 cynodont–mammaliaform clades; based on the strict consensus of 172 equally parsimonious trees (each with treelength 2,243; consistency index 0.373, retention index 0.803) from 1,000 PAUP heuristic runs, without any topology constraints and with all multi-state characters unordered, multi-state taxa interpreted as polymorphism). Placement of Juramaia in eutherians is significantly different (*P<0.050) from suboptimal hypotheses of Juramaia as either a boreosphenidan or a metatherian by Templeton tests. This topology is corroborated by a separate analysis on a different and complementary data set by refs 4, 5 (389 informative characters of 71 eutherian taxa and outgroups), by the strict consensus of 41 equally parsimonious trees, from 1,000 heuristic runs, without topology constraints and 33 multi-state characters ordered, multi-state taxa as polymorphism. Placement of Juramaia among basal eutherians is consistent with topologies from constrained search under molecular scaffolding of extant taxa in the main data set of ref. 24 and the complementary data set of refs 4, 5 (details in Supplementary Information). b, The increased en-echelon postvallum shearing of upper molars in the earliest eutherians17, in contrast to metatherians18 that lack a strongly developed postvallum shearing by metacingulum, except for the Late Cretaceous Pediomys1. Nodes (1) Cladotheria, (2) Boreosphenida1, 2, (3) crown Theria, (4) Eutheria (including Placentalia), and (5) Metatheria (including Marsupialia).

…

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LETTER doi:10.1038/nature10291

A Jurassic eutherian mammal and divergence of

marsupials and placentals

Zhe-Xi Luo

, Chong-Xi Yuan

, Qing-Jin Meng

& Qiang Ji

Placentals are the most abundant mammals that have diversified

into every niche for vertebrates and dominated the world’s terrestrial

biotas in the Cenozoic. A critical event in mammalian history is the

divergence of eutherians, the clade inclusive of all living placentals,

from the metatherian–marsupial clade

1–8

.Herewereportthe

discovery of a new eutherian of 160Myr from the Jurassic of

China, which extends the first appearance of the eutherian–placental

clade by about 35Myr from the previous record, reducing and

resolving a discrepancy between the previous fossil record and the

molecular estimate for the placental–marsupial divergence

9–13

.This

mammal has scansorial forelimb features, and provides the ancestral

condition for dental and other anatomical features of eutherians.

Class Mammalia

Clade Boreosphenida

Infraclass Eutheria

Order and family incertae sedis

Juramaia sinensis

gen. et sp. nov.

Etymology. Jura, Jurassic; maia, mother, in reference to placental

affinities; sinensis, of China. The binomial refers to ‘Jurassic mother

from China’.

Holotype. Beijing Museum of Natural History (BMNH) PM1143

(Fig. 1) is preserved with full dentition, incomplete skull, anterior part

of postcranial skeleton and residual soft tissues, such as hairs.

Locality and age. The Daxigou site of Jianchang County of Liaoning

Province in the Middle–Late Jurassic Tiaojishan formation. The forma-

tion was datedby the SHRIMP U–Pb methodon zircon at 164–165 Myr

in the neighbouring Ningcheng area

and its stratigraphic equivalent

dated by the

Ar/

Ar method on sanidines at 160.760.4 Myr in the

Beipiao area

(Supplementary Information).

Diagnosis. I

–C

–P

–M

–C

–P

–M

(Fig. 2), with identical for-

mula as the eutherian Eomaia

and typical count of five premolars

and three molars for Cretaceous eutherians

. Molars tribosphenic,

with derived eutherian features of distinctive paraconule, incipient

metaconule (M2 only), long preprotocrista past the paracone and long

postprotocrista past the metacone. The postmetacrista and the

extended postprotocrista of an upper molar form two separate ranks

of shearing crests that pass the prevallid crest (paracristid) of the

succeeding lower molar (Fig. 3). The preparacrista and the preproto-

crista form two ranks of shearing crests that pass the postvallid crest

(protocristid) of the preceding lower molar. This kind of stepwise or

en-echelon shearing is much better developed in Juramaia than in

most metatherians

. Distinct from metatherians in lacking the vertical

keel of the paraconid and the hypoconulid shelf

18,19

and in lacking the

close approximation of the hypoconulid and the entoconid as in

Sinodelphys

or the twinning of these cusps in other metatherians

Differs from metatherians (except Sinodelphys) in lacking the inflected

mandibular angle and flat ventral surface ofthe angle. Juramaia sinensis

is similar to many eutherians in having the posterior mental foramen of

the mandible below the p4–p5 junction, by contrast to metatherians

that have the posterior mental foramen below m1. Juramaia sinensis is

similar to several Cretaceous eutherians in retaining a deciduous dP3 in

the middle of the right premolar series

but differs from metatherians

wherein replacement only occurs at the ultimate premolar position

6,20

Juramaia sinensis differs from all australosphenidans in lacking the

continuous mesial cingulid and the wrapping cingulid, and from most

australosphenidan and pseudotribosphenidan mammals in lacking the

postdentary trough on the mandible

14,21–24

. Among the earliest-known

eutherians, Juramaia sinensis differs from Eomaia in having a two-

rooted upper canine

, and from Acristatherium in having different

numbers of upper and lower incisors, a larger M3 and absence of

Carnegie Museum of Natural History, Pittsburgh, Pennsylvania 15213, USA.

Chinese Academy of Geological Sciences, Beijing 100037, China.

Beijing Museum of Natural History, Beijing 100050, China.

P3–dP3

M1–3

cv2

ManusJu

M1–3

P3–dP3

I1–5

cod

cl ac cos

cv7 hh ph

tv1

enf ecc

ra mc

r13

10 mm10 mm

5 mm 3 mm

Scaphoid

Hamate

cv1

tv13

Figure 1

Holotype specimen of

Juramaia sinensis

, Beijing Museum of

Natural History (BMNH) PM1343B. a,b, Specimen photograph and

morphological identification. c, Restoration of the partly preserved skeleton

and skull. d, Restoration of hand (ventral view; alignment of incomplete and

scattered carpals is conjectural). Abbreviations: ac, acromion (scapula); ag,

angular process (dentary); C, c, upper or lower canine; ca, carpals; cl, clavicle;

cod, coronoid (dentary); cos, coracoid process (scapula); cv1–7, cervical

vertebrae 1–7; dc, dentary condyle; ecc, ectepicondyle; enf, entepicondylar

foramen; hh, humeral head; ht, humeral trochlea; I1–5, upper incisors 1–5; Ju,

jugal; M, m, upper or lower molar; manus, hand; mc1–5, metacarpals 1–5; oc,

occipital condyles; ol, olecranon process; P1–5, upper premolars 1–5; ph,

phalanges; r1–13; thoracic ribs 1–13; ra, radius; sn, semilunar notch (ulna); sp.,

scapular spine; tv1–13, thoracic vertebrae 1–13; ul, ulna.

442 | NATURE | VOL 476 | 25 AUGUST 2011

diastemata between the anterior upper premolars

. It differs from

Prokennalestes,Murtoilestes and Acristatherium in having a much

lower protocone and longer postprotocrista

1,25,26

,fromallknown

Early Cretaceous eutherians in a deeper ectoflexus on P5–M2, and from

Montanalestes in having larger lower premolars 3 and 4. See

Supplementary Information for full differential diagnosis and summary

of morphological distinction from other Mesozoic mammal groups.

Our study has firmly placed Juramaia among the basal-most

eutherians, the Mesozoic relatives to the Cenozoic placental mammals

(Fig. 3), by phylogenetic analyses of two independent morphological

data sets (Supplementary Information). Juramaia is more closely

related to extant placentals than all metatherians of the Cretaceous

including Sinodelphys and Deltatheridium. In the first parsimony ana-

lysis of a comprehensive data set of all Mesozoic mammaliaform

clades

,Juramaia and Montanalestes form an unresolved polytomy

with the Eomaia–Prokennalestes clade and other eutherians (Fig. 3,

left). Placement of Juramaia with eutherians is corroborated by ana-

lysis of a second and complementary data set of the largest sampling of

Cretaceous eutherians

4,5

;Juramaia is placed in a more crown-ward

position than the Early Cretaceous eutherian Acristatherium

(Sup-

plementary Information). Our analysis by the mammaliaform data set

reaffirms that the autralosphenidan mammals

are not eutherians

;

they represent a separate lineage of Mesozoic mammalian diversity,

and are stem taxa to monotremes

1,14

, as corroborated by most of the

recent independent studies

4,12,22–24

Juramaia, at an age of 160 Myr (refs 15, 16), establishes a much older

geological time for the split of the metatherian–marsupial and the

eutherian–placental lineages than previously shown by the fossil

record. The previously earliest eutherian record is Eomaia and the

metatherian record is Sinodelphys, both about 125 Myr (refs 3, 7).

The next oldest eutherian with a direct geochronological dating is

Acristatherium at 123 Myr (ref. 5). Juramaia extends the first appear-

ance of eutherians from these previous records by about 35 Myr.

Because Juramaia is unambiguously placed on the placental side of

the marsupial–placental divergence, the marsupial–placental diver-

gence must have occurred before Juramaia. Therefore this new fossil

serves to re-set the minimal age at 160Myr for the basal-most diver-

sification of marsupials and placentals, the two clades that collectively

make up 99.9% of all living mammals and are very important in

terrestrial ecosystems, especially after the Cretaceous/Tertiary extinc-

tion of non-avian dinosaurs.

Timing of the divergence of marsupials and placentals is critical for

calibrating the rates of evolution in therian mammals, especially for

molecular evolutionary studies and comparative genomics

2,10,13

Previously, some molecular time estimates for marsupial and placental

divergence postulated significantly older windows for this divergence

than the then-oldest fossil records

3,7

. However, these and other pre-

vious molecular estimates differed widely. Several were compatible

with relatively young placental intraordinal divergences (for example,

ref. 10), and just about all showed wide error margins (reviewed by

Stylocone

Ectoexus

Post-

Metacrista

cusp (C)

Pre-parastyle

Paracone

Preprotocrista

1 mm

Paraconule

(mesial)

Lateral (labial)

Protocone

Protoconal

swelling Protocone

Pre-

parastyle

P3 P5

tallest

dP3

p2 p4

3 mm

cod

P4P3

Paracone

M1 M2 M3

Post-

protocrista

Metacone

2 mm

Parastyle

Figure 2

Dental and mandibular features of

Juramaia sinensis

(BMNH

PM1343B). a–d, Right upper M2 in mesial, occlusal, labial and distal views

(composite restoration from both the right and the left sides). e, Stereo

photographs of right premolars and molars. f, Stereo photographs of left

premolars and molars. g, Right P3–M3 in occlusal view. h, Left upper dentition

restoration in labial view. i, Left lower dentition (restoration) and mandible.

Grey-shaded areas represent reconstruction from incomplete bone or tooth

structure or mould outline in matrix. Abbreviations: ag, angular process; cod,

coronoid process of dentary; dc; dentary condyle; M, m, upper and lower

molars; mf, mental foramen; P, p, upper and lower premolars; dP3, deciduous

P3 in situ. Terminology of tribosphenic molar follows Fig. 11.1 of ref. 1.

LETTER RESEARCH

25 AUGUST 2011 | VOL 476 | NATURE | 443

ref. 13). Regarding the marsupial–placental split, recent molecular rate

studies provided estimates of 147.7 65.5 Myr (ref. 11), or 160 Myr

(median) with a 95% highest posterior distribution of 143–178 Myr

(ref. 12), or a window of 193–186 Myr (ref. 9). This new eutherian fossil

age is now similar to the age of placentals at 160 Myr with 95%

posterior distribution from 143 to 178 Myr by the latest molecular

estimate

. The age of Juramaia has now set the minimal divergence

time by the fossilto coincide with the range ofmolecular time estimates,

serving as a corroboration of thenewest fossil record with themolecular

clock of evolution. The 160-Myr-old Juramaia also has important

implications for mammalian evolution as a whole. Eutherian mammals

are nested in the more inclusive Mesozoic boreosphenidan clade (Fig.3,

node 1), for which the previously earliest record had been entirely Early

Cretaceous

1,27

. The eutherian Juramaia requires that the ghost-lineages

of boreosphenid and cladotherian mammals would also extend to the

Middle Jurassic. Therefore the magnitude of the mammalian faunal

turnover from the Early to Middle Jurassic is greater than previously

known, and the Early–Middle Jurassic is a critical transition for the

appearance of more of the derived mammalian clades

1,2

Phylogenetically, Juramaia sinensis is one of the basal-most eutherians

and it is currently the earliest-known eutherian (Fig. 3); therefore,

this fossil provides crucial inferences on the ancestral features of all

eutherians. Juramaia weighed about 15–17 g, and was an insectivore

based on tooth morphology. Its long preprotocrista (Fig. 2c, d) and

postprotocrista (Fig. 3e) enhance the en-echelon shearing in which

more than one crest of the upper molar, arranged in stepwise pattern,

shears past the surfaces of the trigonid of the lower molar. This is

especially prominent on the posterior face of the upper molar (post-

vallum) (Fig. 3e–i), an important derived character of eutherians com-

pared with other tribosphenic mammals

(Fig. 3).

The forelimb and shoulder girdle of Juramaiashow several eutherian

apomorphies and lack such metatherian features as the supra-scapular

notch and the expanded ectepicondylar shelf on the humerus for the

supinator muscle

7,28,29

. Its manual phalanges suggest a scansorial

adaptation (Fig. 1d). Proximal phalanges of three digits show protuber-

ances of the annular ligament of the digital flexor muscle tendon,

suggesting a gripping capability of the hand, common in scansorial

extant mammals

3,7

. In the third manual digit, the proximal phalanx is

2.77 mm long, the intermediate phalanx is 2.39mm and the metacarpal

is 4.26 mm. The phalangeal index ((proximal 1intermediate pha-

langes)/metacarpal 3100) (ref. 30) is 121 for Juramaia.Mostextant

mammals with this index value are arboreal. The proximal phalangeal

index (proximal/intermediate phalanges 3100) is 65 for Juramaia.

Extant placental carnivorans, primates and dermopterans with this

value also tend to be arborealists, but rodents with this value are all

terrestrial

. Compared with fossil mammals of the Early Cretaceous

Yixian formation, phalangeal indices of Juramaia are between Eomaia

scansoria, a scansorial mammal, and the eutriconodont Jeholodens

jenkinsi, which is interpreted to be terrestrial

. In its habitat preference,

Juramaia should be similar to the eutherian Eomaia scansoria,tothe

Maastrichtian

Late

Monotremataformes

Kielantherium

Peramus

Juramaia (160 Myr)

Dryolestes

Montanalestes

Prokennalestes

Murtoilestes

Eomaia (125 Myr)

Sinodelphys (125 Myr)

Holoclemensia

Deltatheridium

Atokatheriidum

Australosphenidans

Cretaceous

EarlyLateMiddle

JurassicTriassic

Early

Campanian

Santonian

Coniacian

Turonian

Cenomanian

Albian

Aptian

Barremian

125

145.5

161.2

175.6

199.6

Myr

Theriamorpha

Theriiformes

Trechnotheria

Hauterivian

Valanginian

Berriasian

Tithonian

Kimmeridgian

Oxfordian

Callovian

Bathonian

Bajocian

Aalenian

Toarcian

Pliensbachian

Sinemurian

Hettangian

99.6

65.5

Myr

Cenozoic

monotremes

Cenozoic

placentals

Late

Cretaceous

eutherians

Late

Cretaceous

metatherians

Cenozoic

marsupials 1 cm 2 mm

2 mm

A Didelphis

B Alphadon

C Deltatheridium

D Kielantherium

E Juramaia

F Murtoilestes

G Kennalestes

H Gypsonictops

I Protungulatum

Figure 3

Time-calibrated phylogeny of the eutherian

Juramaia

among

other boreosphenidan mammals, and comparative morphologyof some key

molar features. a, Basal eutherianand metatherian phylogeny from parsimony

analysis of data set of ref. 24 (446 characters of 103 cynodont–mammaliaform

clades; based on the strict consensus of 172 equally parsimonious trees (each

with treelength 2,243; consistency index 0.373, retention index 0.803) from

1,000 PAUP heuristic runs, without any topology constraints and with all

multi-state characters unordered, multi-state taxa interpreted as

polymorphism). Placement of Juramaia in eutherians is significantly different

(*P,0.050) from suboptimal hypotheses of Juramaia as either a

boreosphenidan or a metatherian by Templeton tests. This topology is

corroborated by a separate analysis on a different and complementary data set

by refs 4, 5 (389 informative characters of 71 eutherian taxa and outgroups), by

the strict consensus of 41 equally parsimonious trees, from 1,000 heuristic runs,

without topology constraints and 33 multi-state characters ordered, multi-state

taxa as polymorphism. Placement of Juramaia among basal eutherians is

consistent with topologies from constrained search under molecular

scaffolding of extant taxa in the main data set of ref. 24 and the complementary

data set of refs 4, 5 (details in Supplementary Information). b, The increaseden-

echelon postvallum shearing of upper molars in the earliest eutherians

,in

contrast to metatherians

that lack a strongly developed postvallum shearing

by metacingulum, except for the Late Cretaceous Pediomys

. Nodes (1)

Cladotheria, (2) Boreosphenida

1,2

, (3) crown Theria, (4) Eutheria (including

Placentalia), and (5) Metatheria (including Marsupialia).

RESEARCH LETTER

444 | NATURE | VOL 476 | 25 AUGUST 2011

Cretaceous and Early Cenozoic metatherians

7,28

and to living scansorial

or arboreal didelphids

. The scansorial habits are also corroborated by

the forelimb features, which are indicative of that habitat preference in

extant mammals, such as the hypertrophied acromion and the acute

posterior angle of the scapula

The earliest-known eutherians Juramaia and Eomaia and the earliest

metatherian Sinodelphys are scansorial mammals, and differ from con-

temporary Mesozoic mammals, most which are terrestrial

1,2

.Thissug-

gests that the phylogenetic split of eutherians and metatherians and

their earliest evolution are accompanied by major ecomorphological

diversification, notably scansorial adaptation, which made it possible

for therians to exploit arboreal niches.

Received 26 December 2010; accepted 10 June 2011.

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www.nature.com/nature.

AcknowledgementsWe thank A. R. Tabrum for his meticulous preparationof the fossil,

Y.-Q. Zhang for casting, and M. A. Klingler for assistancewith graphics. During thiswork,

we benefited from discussion with Y.-Q. Liu on field geology and dating, and with

R. J. Asher, K. C. Beard,R. L. Cifelli, M. R. Dawson, T. Martinand J. R. Wible for discussion

on mammal phylogeny. J. Wible and M. Dawson helped to improve the manuscript.

Supportwas given to Z.-X.L. from theNational Science Foundation(USA), to C.-X.Y.from

the National Natural Science Foundation-China and the Chinese Academy of

Geological Sciences, and to Q.J. from the 973 Project of the Ministry of Science and

Technology of China and funding from the Chinese Academy of Geological Sciences.

Author Contributions Z.-X.L. and Q.J. designed the research plan. All authors

participated in morphological studies. Z.-X.L. and C.-X.Y. performed phylogenetic

analyses. Z.-X.L. wrote the paper with discussion from all authors.

Author Information Reprints and permissions information is available at

www.nature.com/reprints. The authors declare no competing financial interests.

Readers are welcome to comment on the online version of this article at

www.nature.com/nature. Correspondence and requests for materials should be

addressed to Z.-X.L. (luoz@carnegiemnh.org).

LETTER RESEARCH

25 AUGUST 2011 | VOL 476 | NATURE | 445

Cathelicidin antimicrobial peptides mediate immune protection in marsupial neonates

Article

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Apr 2025

Marsupial neonates are born with immature immune systems, making them vulnerable to pathogens. While neonates receive maternal protection, they can also independently combat pathogens, although the mechanisms remain unknown. Using the sugar glider (Petaurus breviceps) as a model, we investigated immunological defense strategies of marsupial neonates. Cathelicidins-a family of antimicrobial peptides expanded in the genomes of marsupials-are highly expressed in developing neutrophils. Sugar glider cathelicidins reside in two genomic clusters, and their coordinated expression is achieved by enhancer sharing within clusters and long-range physical interactions between clusters. Functionally, cathelicidins modulate immune responses and have potent antibacterial effects, sufficient to provide protection in a mouse model of sepsis. Evolutionarily, cathelicidins have a complex history, with marsupials and monotremes uniquely retaining both clusters among tetrapods. Thus, cathelicidins are critical mediators of marsupial immunity, and their evolution may reflect the life history-specific immunological needs of these animals.

Down to earth: therian mammals became more terrestrial towards the end of the Cretaceous

Article

Apr 2025
Palaeontology

The end Cretaceous extinctions had a profound effect on mammalian diversity, especially on metatherians (marsupials and their extinct relatives). Could mammalian substrate preference have influenced differential survival patterns? The plant fossil record shows changing angiosperm leaf anatomy during the last ten million years of the Cretaceous that would have resulted in a greater richness of terrestrial understory habitats, and work by other researchers implies that terrestrial (vs arboreal) substrate preference promoted increased survival over the Cretaceous–Palaeogene boundary for both mammals and birds. Here we use fragmentary postcranial remains of Late Cretaceous mammals and show that, at least in the Western Interior of North America, therian mammals were becoming more terrestrial in their locomotor mode towards the end of the Cretaceous.

Phylogeny and Molecular Characterisation of PRNP in Red-Tailed Phascogale (Phascogale calura)

Article

Full-text available

Feb 2025
BSRCCS

Background/Objectives: The normal cellular prion protein (PrPC) is a cell-surface glycoprotein, mainly localised in neurons of the central nervous system (CNS). The human PRNP gene encodes 253 amino acid residues of precursor PrPC. Several studies that investigated the role of PRNP and PrPC in placental mammals, such as humans and mice, failed to reveal its exact function. Methods: In this study, we sequenced and characterised the PRNP gene and PrPC of the marsupial, P. calura, as a strategy to gain molecular insights into its structure and physicochemical properties. Placentals are separated from marsupials by approximately 125 million years of independent evolution. Results: Standard Western blotting analysis of PrPC phascogale displayed the typical un-, mono-, and di-glycosylated bands recognized in placentals. Furthermore, we showed that phascogale PRNP gene has two exons, similar to all the marsupials and placentals of the PRNP genes studied. Of note, the phascogale PRNP gene contained distinctive repeats in the PrPC tail region comparable to the closely related Tasmanian devil (Sarcophilus harrisii) and more distantly related to the grey short-tailed opossum (Monodelphis domestica), common wombat (Vombatus ursinus), and Tammar wallaby (Macropus eugenii); however, its specific composition and numbers were different from placentals. Of importance, comparisons of the phascogale’s PrPC physicochemical properties with other monotremes, marsupials, and placentals confirmed the Monotremata–Marsupialia–Placentalia evolutionary distance. We found that the protein instability index, a method used to predict the stability of a protein in vivo (Stable: <40; Instable >40), showed that the PrPC of all marsupials tested, including phascogale, were highly stable compared with the birds, reptiles, amphibians, and fish that were shown to be highly unstable. However, the instability index predicted that all placental species, including human (Homo sapiens), mouse (Mus musculus), bank vole (Myodes glareolus), rhinoceros (Rhinocerotidae), dog (Canis lupus familiaris), flying fox (Pteropus vampyrus), whale (Physeter catodon), cattle (Bos taurus), and sheep (Ovis aries), were either slightly unstable or nearly unstable. Further, our analysis revealed that despite their predicted high PrPC stability, P. calura exhibited substantial N-terminal disorder (53.76%), while species with highly unstable PrPCs based on their instability index, such as Danio rerio, Oryzias latipes, and Astyanax mexicanus, displayed even higher levels of N-terminal disorder (up to 75.84%). These findings highlight a discrepancy between overall predicted stability and N-terminal disorder, suggesting a potential compensatory role of disorder in modulating prion protein stability and function. Conclusions: These results suggest that the high stability of marsupial prion proteins indicates a vital role in maintaining protein homeostasis; however more work is warranted to further depict the exact function.

Candidate SNP markers of changes in the expression levels of the human SCN9A gene as a hub gene for pain generation, perception, response and anesthesia

Article

Full-text available

Dec 2024

In this work, we for the first time performed a comprehensive bioinformatics analysis of 568 human genes that, according to the NCBI Gene database as on September 15, 2024, were associated with pain generation, perception and anesthesia. The SCN9A gene encoding the sodium voltage-gated channel α subunit 9 and expressed in sensory neurons for transferring signals to the central nervous system about tissue damage was the only one involved in all the processes of interest at once as a hub gene. First, with our tool called OrthoWeb, we estimated the phylostratigraphic age indices (PAIs) for each of the genes, that is, identified the taxon of the most recent common ancestor of the organisms for which that gene has been sequenced. The mean PAI for all genes under study, including SCN9A as a hub gene for pain generation, perception, response and anesthesia, was '4'. On the evolutionary scale by the Kyoto Encyclopedia of Genes and Genomes (KEGG), the ancestor is the phylum Chordata, some of the most ancient of which evolved the central and the peripheral nervous system. Next, with our tool called ANDSystem, we found that phosphorylation of ion channels is a centerpiece in pain generation, perception, response and anesthesia, on which the efficiency of signal transduction from the peripheral to the central system depends. This conclusion was consistent with literature data on a key role an efficient signal transduction from the peripheral to the central system from the peripheral to the central system for adjusting the human circadian rhythm through detection of a change from the dark of night to the light of day and for identification of the direction of the source of sound by auditory brainstem nuclei, for generating the response to cold stress and for physical coordination. 21 candidate SNP marker of significant SCN9A over-and underexpression. Finally, the ratio of SCN9A upregulating to downregulating SNPs was compared to that for all known human genes estimated by the 1000 Genomes Project Consortium. It was found that SCN9A as a hub gene for pain generation, perception, pain response and anesthesia is acted on by natural selection against its downregulation, to keep the nervous system highly informed on the status of the organism and the environment.

Paleoinspired Vision: From Exploring Colour Vision Evolution to Inspiring Camera Design

Preprint

Dec 2024

The evolution of colour vision is captivating, as it reveals the adaptive strategies of extinct species while simultaneously inspiring innovations in modern imaging technology. In this study, we present a simplified model of visual transduction in the retina, introducing a novel opsin layer. We quantify evolutionary pressures by measuring machine vision recognition accuracy on colour images shaped by specific opsins. Building on this, we develop an evolutionary conservation optimisation algorithm to reconstruct the spectral sensitivity of opsins, enabling mutation-driven adaptations to to more effectively spot fruits or predators. This model condenses millions of years of evolution within seconds on GPU, providing an experimental framework to test long-standing hypotheses in evolutionary biology , such as vision of early mammals, primate trichromacy from gene duplication, retention of colour blindness, blue-shift of fish rod and multiple rod opsins with bioluminescence. Moreover, the model enables speculative explorations of hypothetical species, such as organisms with eyes adapted to the conditions on Mars. Our findings suggest a minimalist yet effective approach to task-specific camera filter design, optimising the spectral response function to meet application-driven demands. The code will be made publicly available upon acceptance.

Feature selectivity and invariance in marsupial primary visual cortex

Article

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Dec 2024
J PHYSIOL-LONDON

A fundamental question in sensory neuroscience revolves around how neurons represent complex visual stimuli. In mammalian primary visual cortex (V1), neurons decode intricate visual features to identify objects, with most being selective for edge orientation, but with half of those also developing invariance to edge position within their receptive fields. Position invariance allows cells to continue to code an edge even when it moves around. Combining feature selectivity and invariance is integral to successful object recognition. Considering the marsupial–eutherian divergence 160 million years ago, we explored whether feature selectivity and invariance was similar in marsupials and eutherians. We recovered the spatial filters and non‐linear processing characteristics of the receptive fields of neurons in wallaby V1 and compared them with previous results from cat cortex. We stimulated the neurons in V1 with white Gaussian noise and analysed responses using the non‐linear input model. Wallabies exhibit the same high percentage of orientation selective neurons as cats. However, in wallabies we observed a notably higher prevalence of neurons with three or more filters compared to cats. We show that having three or more filters substantially increases phase invariance in the V1s of both species, but that wallaby V1 accentuates this feature, suggesting that the species condenses more processing into the earliest cortical stage. These findings suggest that evolution has led to more than one solution to the problem of creating complex visual processing strategies. image Key points Previous studies have shown that the primary visual cortex (V1) in mammals is essential for processing complex visual stimuli, with neurons displaying selectivity for edge orientation and position. This research explores whether the visual processing mechanisms in marsupials, such as wallabies, are similar to those in eutherian mammals (e.g. cats). The study found that wallabies have a higher prevalence of neurons with multiple spatial filters in V1, indicating more complex visual processing. Using a non‐linear input model, we demonstrated that neurons with three or more filters increase phase invariance. These findings suggest that marsupials and eutherian mammals have evolved similar strategies for visual processing, but marsupials have condensed more capacity to build phase invariance into the first step in the cortical pathway.

Bioactive components in the marsupial pouch and milk

Article

Full-text available

Nov 2024
NUTR RES REV

Marsupials give birth to immunologically naïve young after a relatively short gestation period compared to eutherians. Consequently, the joey significantly relies on maternal protection, which is the focus of the present review. The milk and the pouch environment are essential contributors to maternal protection for the healthy development of joeys. In this review, we discuss bioactive components found in the marsupial pouch and milk that form cornerstones of maternal protection. These bioactive components include immune cells, immunoglobulins, the s100 family of calcium-binding proteins, lysozymes, whey proteins, antimicrobial peptides and other immune proteins. Furthermore, we investigated the possibility of the presence of plurifunctional components in milk and pouches that are potentially bioactive. These compounds include caseins, vitamins and minerals, oligosaccharides, lipids, and microRNAs. Where applicable, this review addresses variability in bioactive components during different phases of lactation, designed to fulfil the immunological needs of the growing pouch young. Yet there are numerous additional research opportunities to pursue, including uncovering novel bioactive components, investigating their mode of action, dynamics, stability, and ability to penetrate the gut epithelium ensuring systemic actions.

A Broad Genome Survey Reveals Widespread Presence of Secretoglobin Genes in Squamate and Archosaur Reptiles that Flowered into Diversity in Mammals

Article

Full-text available

Feb 2025

Secretoglobins (SCGBs) are a superfamily of small, dimeric, cytokine-like proteins found originally in the reproductive tracts and airways of mammals. Most SCGB research has focused on respiratory diseases in humans and laboratory animal models but knowledge of their biological functions is sparse. We report here a broad survey of Scgbs, the genes that encode SCGBs, in animal genomes. We tested the view that they are uniquely mammalian in origin and distribution, hoping that understanding their distribution would shed light on their evolutionary history and perhaps point to putative biological functions. Rather than being uniquely mammalian, we found many different SCGBs in turtles, crocodilians, lizards, and birds, suggesting they existed in the Carboniferous Period (∼320 MYA) when the sauropsids evolved in the amniote lineage. We identified no SCGBs in amphibians or fishes, suggesting that this characteristic originated in an amniote ancestor. Amniotes include sauropsid and synapsid lineages, and three subfamilies of SCGBs (SCGB2A, SCGB3A, and SCGB1C) are found in both sauropsid and synapsid lineages. Uteroglobin (SCGB1A), the first identified SCGB protein, is uniquely mammalian, having appeared in monotremes. The SCGB subfamilies including androgen-binding proteins (SCGB1B and SCGB2B) are first seen in metatherians. This complex distribution suggests that there is an as-yet-undiscovered basic function of SCGBs shared by all amniotes.

Low mutation rate but high male-bias in the germline of a short-lived opossum

Preprint

Dec 2024

Age and sex have been found to be important determinants of the mutation rate per generation in mammals, but the mechanisms underlying these factors are still unclear. One approach to distinguishing between alternative mechanisms is to study species that reproduce at very young ages, as competing hypotheses make different predictions about patterns of mutation in these organisms. Here, we study the germline mutation rate in the gray short-tailed opossum, Monodelphis domestica, a laboratory model species that becomes reproductively mature at less than six months of age. Whole-genome sequencing of 22 trios reveals the lowest mutation rate per generation found in mammals thus far (0.26 × 10-8 per base pair per generation at an average parental age of 313 days), which is expected given their early reproduction. We also examine the mutation spectrum and find fewer mutations at CpG sites in opossums than in humans, consistent with the lower CpG content in the opossum genome. We observe that two-thirds of mutations are inherited from the male parent in opossums, slightly lower than the degree of male bias observed in organisms that reproduce at much older ages. Nevertheless, the very young age at reproduction in opossums suggests that ongoing spermatogonial divisions in males after puberty are not the primary driver of the observed male mutation bias. These findings contribute to a growing body of evidence that the differences between male and female germline mutation may arise from mechanisms other than cell division post-puberty. Article Summary This study investigates the germline mutation rate in the gray short-tailed opossum, a marsupial with early reproductive maturity. By sequencing 22 families, we report the lowest mutation rate recorded in mammals but a typical male mutation bias. These findings add to growing evidence that challenges the traditional view that continuing cell division is the primary driver of male-biased mutations. Instead, the study suggests that alternative mechanisms, such as differences in DNA repair, may influence sex-specific mutation rates.

Candidate SNP Markers Significantly Altering the Affinity of the TATA-Binding Protein for the Promoters of Human Genes Associated with Primary Open-Angle Glaucoma

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Nov 2024
INT J MOL SCI

Primary open-angle glaucoma (POAG) is the most common form of glaucoma. This condition leads to optic nerve degeneration and eventually to blindness. Tobacco smoking, alcohol consumption, fast-food diets, obesity, heavy weight lifting, high-intensity physical exercises, and many other bad habits are lifestyle-related risk factors for POAG. By contrast, moderate-intensity aerobic exercise and the Mediterranean diet can alleviate POAG. In this work, we for the first time estimated the phylostratigraphic age indices (PAIs) of all 153 POAG-related human genes in the NCBI Gene Database. This allowed us to separate them into two groups: POAG-related genes that appeared before and after the phylum Chordata, that is, ophthalmologically speaking, before and after the camera-type eye evolved. Next, in the POAG-related genes’ promoters, we in silico predicted all 3835 candidate SNP markers that significantly change the TATA-binding protein (TBP) affinity for these promoters and, through this molecular mechanism, the expression levels of these genes. Finally, we verified our results against five independent web services—PANTHER, DAVID, STRING, MetaScape, and GeneMANIA—as well as the ClinVar database. It was concluded that POAG is likely to be a symptom of the human self-domestication syndrome, a downside of being civilized.

The delayed rise of present-day mammals

Article

Full-text available

Mar 2007

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals. Molecular data and the fossil record can give conflicting views of the evolutionary past. For instance, empirical palaeontological evidence by itself tends to favour the 'explosive model' of diversification for extant placental mammals 1 , in which the orders with living representatives both originated and rapidly diversified soon after the Cretaceous/Tertiary (K/T) mass extinction event that eliminated non-avian dinosaurs and many other, mostly marine 2 , taxa 65.5 million years (Myr) ago 1,3,4. By contrast, molecular data consistently push most origins of the same orders back into the Late Cretaceous period 5-9 , leading to alternative scenarios in which placental line-ages persist at low diversity for some period of time after their initial origins ('phylogenetic fuses'; see ref. 10) before undergoing evolutionary explosions 1,11. Principal among these scenarios is the 'long-fuse model' 1 , which postulates an extended lag between the Cretaceous origins of the orders and the first split among their living representatives (crown groups) immediately after the K/T boundary 8. Some older molecular studies advocate a 'short-fuse model' of diversification 1 , where even the basal crown-group divergences within some of the larger placental orders occur well within the Cretaceous period 5-7. A partial molecular phylogeny emphasizing divergences among placental orders suggested that over 20 lineages with extant descendants (henceforth, 'extant lineages') survived the K/T boundary 8. However, the total number of extant lineages that pre-date the extinction event and whether or not they radiated immediately after it remain unknown. The fossil record alone does not provide direct answers to these questions. It does reveal a strong pulse of diversification in stem eutherians immediately after the K/T boundary 4,12 , but few of the known Palaeocene taxa can be placed securely within the crown groups of extant orders comprising Placentalia 4. The latter only rise to prominence in fossils known from the Early Eocene epoch onwards (,50 Myr ago) after a major faunal reorganization 4,13,14. The geographical patchiness of the record complicates interpretations of this near-absence of Palaeocene crown-group fossils 14-16 : were these clades radiating throughout the Palaeocene epoch in parts of the world where the fossil record is less well known; had they not yet originated; or did they have very long fuses, remaining at low diversity until the major turnover at the start of the Eocene epoch? The pattern of diversification rates through time, to which little attention has been paid so far, might hold the key to answering these questions. If the Cretaceous fauna inhibited mammalian diversification , as is commonly assumed 1 , and all mammalian lineages were able to radiate after their extinction, then there should be a significant increase in the net per-lineage rate of extant mammalian diversification , r (the difference between the per-lineage speciation and extinction rates), immediately after the K/T mass extinction. This hypothesis, along with the explosive, long-and short-fuse models, can be tested using densely sampled phylogenies of extant species, which contain information about the history of their diversification rates 17-20. Using modern supertree algorithms 21,22 , we construct the first virtually complete species-level phylogeny of extant mammals from over 2,500 partial estimates, and estimate divergence times (with confidence intervals) throughout it using a 66-gene alignment in conjunction with 30 cladistically robust fossil calibration points. Our analyses of the supertree indicate that the principal splits underlying the diversification of the extant lineages occurred (1) from 100-85 Myr ago with the origins of the extant orders, and (2) in or after the Early Eocene (agreeing with the upturn in their diversity known from the fossil record 4,13,14), but not immediately after the K/T boundary, where diversification rates are unchanged. Our findings-that more extant placental lineages survived the K/T boundary than previously recognized and that fewer arose immediately after it than previously suspected-extend the phylogenetic fuses of many extant orders and indicate that the end-Cretaceous mass extinction event had, at best, a minor role in driving the diversification of the present-day mam-malian lineages. A supertree with divergence times for extant mammals The supertree contains 4,510 of the 4,554 extant species recorded in ref. 23, making it 99.0% complete at the species level (Fig. 1; see also

Early Cretaceous mammals from Flat Rocks, Victoria, Australia

Article

Full-text available

Jan 1999

Ji-EtAl(2002)Eomaia

Data

Full-text available

Oct 2013

Earliest Evolution of Multituberculate Mammals Revealed by a New Jurassic Fossil

Article

Full-text available

Aug 2013
SCIENCE

Early Multi Multituberculate mammals (multis) first arose in the Jurassic and became extinct in the Oligocene, a span of over 100 million years, which makes them the longest-living order of mammals known. This highly diverse and abundant group filled many niches occupied by today's similarly diverse rodents. Multis are known for their complex dentition and unique locomotor adaptations, which facilitated their divergence into a suite of ecosystems. Yuan et al. (p. 779 ) describe a new basal multi from a nearly complete skeleton that shows that the underpinnings of these adaptations arose early in the evolution of the order, setting the stage for the major diversification and radiation of the group that came during the Cretaceous and Paleogene.

A Swimming Mammaliaform from the Middle Jurassic and Ecomorphological Diversification of Early Mammals

Article

Full-text available

Feb 2006
SCIENCE

A docodontan mammaliaform from the Middle Jurassic of China possesses swimming and burrowing skeletal adaptations and some dental features for aquatic feeding. It is the most primitive taxon in the mammalian lineage known to have fur and has a broad, flattened, partly scaly tail analogous to that of modern beavers. We infer that docodontans were semiaquatic, convergent to the modern platypus and many Cenozoic placentals. This fossil demonstrates that some mammaliaforms, or proximal relatives to modern mammals, developed diverse locomotory and feeding adaptations and were ecomorphologically different from the majority of generalized small terrestrial Mesozoic mammalian insectivores.

Fossil evidence for the origin of the marsupial pattern of tooth replacement

Article

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Feb 1996
NATURE

EXTANT marsupials are distinctive in their pattern of dental development1, in that only one tooth is replaced postnatally in each jaw. Interpretation of this pattern for marsupials ancestrally is disputed2-5, partly because ontogenetic data in fossils have been unobtainable. Here we present an ultra-high-resolution X-ray computed tomography (CT) study of the tiny fossil Alphadon, which represents the first evidence of dental development and replacement in a Mesozoic marsupial. In the known pattern of tooth replacement and development, Alphadon is identical to living marsupials, a derived similarity suggesting that this pattern is ancestral to Marsupialia, and that it was established by the Late Cretaceous, at least. This pattern has been correlated with some specialized aspects of marsupial lactation1,6. Hence the presence of a marsupial pattern of tooth replacement in Alphadon provides indirect evidence that at least some specialized features of marsupial reproductive processes arose during the Mesozoic.

High-precision 40Ar/ 39Ar age constraints on the basal Lanqi Formation and its implications for the origin of angiosperm plants

Article

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Mar 2009
EARTH PLANET SC LETT

Abundant Mesozoic terrestrial fossils were discovered in the Haifanggou Formation and the overlying Lanqi Formation in northeastern China. The recent discovery of Schmeissneria sinensis from the Haifanggou Formation provides evidence that the origin of angiosperms could be much earlier than previously believed. 92 taxa of plant fossils from the Lanqi Formation provide unique opportunities to understand the floral evolution and its diversification in the Mesozoic. Here we present robust high-precision 40Ar/39Ar data of 160.7±0.4 Ma and 158.7±0.6 Ma for two tuffs from the lowest part of the Lanqi Formation near the main outcrop of floral fossils in Beipiao City, Liaoning, China. Our age results indicate the whole Lanqi Formation was deposited in the Late Jurassic; consequently, the underlying Haifanggou Formation and Schmeissneria sinensis are at least Middle Jurassic in age. Besides its importance for floral evolution, our high-precision age results for the basal Lanqi Formation indicate the paleoenvironment in the north margin of the North China Craton was dry and hot in the Late Jurassic. Moreover, the new age data for the basal Lanqi Formation suggest that the unearthed fossils from the Haifanggou Formation and Lanqi Formation should be equivalent to the Daohugou Biota in Inner Mongolia, China.

Calibrating And Constraining Molecular Clocks

Chapter

Apr 2009

For well over 200 years, natural scientists have used fossils with varying degrees of confidence to date the evolution of life. The field has advanced dramatically in the last few years, and it would be useful now to review some of the key issues and to suggest an outline of a modus operandi for the future. In explaining the role of fossils in establishing timescales, it is useful to review the historical sequence in which key observations were made. Much of this early history predates the 1960s concept of the molecular clock; but the way in which fossils should be used today depends crucially on those earlier geological and paleontological observations. In presenting these observations in a logical sequence, we highlight what can and cannot be done with fossils, and link this to the relative strengths and weaknesses of molecular data. The value of carrying out this survey now is that it is not framed in the old and rather worn narrative of a “conflict” between fossils and molecules (e.g., 1, 2). It is no longer a question of which is better than the other, or how far one can go with one or the other source of data. It is evident that both fossils and molecules have great strengths, but in recognizing the weaknesses of each source of data, a realistic plan for collaboration between paleontologists and molecular biologists can be proposed (3, 4).

Mammals from the Age of Dinosaurs: Origin, Evolution, and Structure

Book

Nov 2004

UPb zircon age for the Daohugou Biota at Ningcheng of Inner Mongolia and comments on related issues

Article

Nov 2006

SHRIMP U-Pb zircon dating was carried out for the Daohugou Biota near Ningcheng of Inner Mongolia and for lavas overlying or underlying salamander-bearing strata at Reshuitang in Lingyuan of West Liaoning. The results suggest that the Daohugou Biota occurred at an interval from 168 Ma to 164–152 Ma. Both the Daohugou Biota and the salamander-bearing fossil assemblage are the same biota and thus developed from 168 to 152 Ma, i.e. from late Middle Jurassic to the early Late Jurassic. The Daohugou Biota-bearing rocks, resting on the Jiulongshan Formation in disconformity and being overlain in unconformity by Late Jurassic Tuchengzi Formation and Early Cretaceous rocks containing the Jehol Biota, are mainly composed of volcanic-sedimentary rocks in a normal sequence. It is recommended that the Daohugou Biota and the related stratigraphy should be correlated with the Tiaojishan Formation (Lanqi Formation in West Liaoning) or its synchronous rocks. It is suggested that the Daohugou Biota and the Jehol Biota would be neither taken into one biota nor considered as the earliest elements of the Jehol Biota. The Daohugou Biota and the related rocks and the Yixian Formation were respectively formed in different periods of volcanic-sedimentary tectonics.

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