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Three new Jurassic euharamiyidan species reinforce early divergence of mammals

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Abstract

The phylogeny of Allotheria, including Multituberculata and Haramiyida, remains unsolved and has generated contentious views on the origin and earliest evolution of mammals. Here we report three new species of a new clade, Euharamiyida, based on six well-preserved fossils from the Jurassic period of China. These fossils reveal many craniodental and postcranial features of euharamiyidans and clarify several ambiguous structures that are currently the topic of debate. Our phylogenetic analyses recognize Euharamiyida as the sister group of Multituberculata, and place Allotheria within the Mammalia. The phylogeny suggests that allotherian mammals evolved from a Late Triassic (approximately 208 million years ago) Haramiyavia-like ancestor and diversified into euharamiyidans and multituberculates with a cosmopolitan distribution, implying homologous acquisition of many craniodental and postcranial features in the two groups. Our findings also favour a Late Triassic origin of mammals in Laurasia and two independent detachment events of the middle ear bones during mammalian evolution.

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Figure 1: The holotypes of three euharamiyidan species.
Figure 2: Teeth, skull and mandibles of euharamiyidans.
Figure 3: Skeletal features of euharamiyidans.
Figure 4: Phylogeny of mammals with focus on Allotheria.

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Acknowledgements

We thank H.-J. Li and Z.-J. Gao for using the specimens housed at the Jizantang Paleontological Museum; Z.-Y. Sun and D.-Y. Sun for using the specimen housed at the Museum of Wuyishan Mountain; J.-C. Lü for assistance in specimen collecting; S.-H. Xie for specimen preparation; M. A. Klingler and F.-X. Wu for specimen drawing and photography; W.-D. Zhang for SEM imaging; Z.-H. Zhou, X. Xu, F.-C. Zhang and X.-L. Wang for discussion on stratigraphy and faunal compositions; and A. Weil and G. W. Rougier for instructive comments. The study was supported by the National Basic Research Program of China (973 program, 2012CB821906), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB03020501), the National Science Foundation of China (41128002) and the Hundred Talents Programs of the Chinese Academy of Sciences.

Author information

Affiliations

Authors

Contributions

S.B., J.M. and Y.W. designed the study, performed the comparative and analytical work and wrote the paper. J.G. and X.S. collected data and contributed to the writing and discussion.

Corresponding authors

Correspondence to Yuanqing Wang or Jin Meng.

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Competing interests

The authors declare no competing financial interests.

Additional information

The Life Science Identifiers (LSIDs) for this publication have been deposited at http://zoobank.org/ and include: urn:lsid:zoobank.org:pub:766EBC08-EF77-41E5-AC59-9F69E9F59BAA (for this publication), urn:lsid:zoobank.org:act:32B0742D-2DD3-47F9-A35B-E1FB284E9EA5 (Shenshou), urn:lsid:zoobank.org:act:BA8BF69D-0F21-4DE7-9EA5-BA6082973940 (Shenshou lui), urn:lsid:zoobank.org:act:4C10F9F1-A920-450B-8E5F-C88F3BD0920C (Xianshou), urn:lsid:zoobank.org:act:3DB1D738-70E9-4966-93FE-3FE5269F9C91 (Xianshou linglong), urn:lsid:zoobank.org:act:1F7EEE49-5E88-4941-AE8B-B2C7C31F9788 (Xianshou songae).

Extended data figures and tables

Extended Data Figure 1 The holotypes of three euharamiyidan species.

a, Holotype specimen (LDNHMF2001) and line drawing of Shenshou lui. b, Holotype specimen (IVPP V16707A) and line drawing of Xianshou linglong. c, Holotype specimen (BMNHC-PM003253) and line drawing of Xianshou songae. as, astragalus; c, cervical vertebrate; ca, caudal vertebrate; cc, costal cartilage; cm, calcaneum; ct, capitate; cu, cuboid; en, entocuneiform; fr, frontal; hm, hamate; ic, interclavicle; ip, intermediate phalanges; l, lumbar vertebrae; lc, left clavicle; lfe, left femur; lfi, left fibula; lh, left humerus; li, left ilium; lis, left ischium; lm, left mandible; lra, left radius; lsc, left scapular; lpb, left pubis; lti, left tibia; lu, lunate; lul, left ulna; m, maxilla; mb, manubrium; mc, metacarpal; mt, metatarsal; n, nasal; pa, parietal; pi, pisiform; pm, premaxilla; pp, proximal phalanges; r, rib; rc, right clavicle; rfe, right femur; rfi, right fibula; rh, right humerus; ri, right ilium; ris, right ischium; rm, right mandible; rra, right radius; rsc, right scapular; rti, right tibia; ru, right ulna; s, sacral vertebrae; sm, septomaxilla; sp, scaphoid; sq, squamosal; stb, sternebra; t, thoracic vertebrae; td, trapezoid; tm, trapezium; tp, terminal phalanges; tq, triquetrum; tr, thoracic ribs; ts, tarsal spur.

Extended Data Figure 2 Close-up views of craniodental structure of Shenshou lui (LDNHMF2001).

a, The skull and mandibles of Shenshou lui (LDNHMF2001). ap, angular process; m, maxilla; maf, masseteric fossa; n, nasal; pal, palatine; pm, premaxilla; ptf, pterygoid fossa; sm, septomaxilla; sq, squamosal. b, The lingual surface of the mandible of Shenshou lui (LDNHMF2001). The close-up view shows the vestige of the coronoid bone at the ventrodistal side of the ultimate lower molar and the wear facets on the lingual sides of the lingual cusps of M1,2. c, The rostrum of the skull of Shenshou lui (LDNHMF2001). The figure is a close-up view of the rostrum region in a. It shows the relationship of the alveoli for P3,4 with the molars and the wear facets on the medial side of left I2. d, Photographs and stippling drawings of the dentition of Shenshou lui (LDNHMF2001). The dentitions were coated with ammonium chloride to enhance contrast. The holotype of Shenshou is an old individual, judging from the deeper wear on its teeth. The mesial end of the upper molar basin and the distal end of the lower molar basin appear to be open, not closed by ridge or cusps, but this may be partly due to the tooth wear.

Extended Data Figure 3 Paratypes 1 and 2 of Shenshou lui.

a, Dorsal view of the skeleton of Shenshou lui (paratype 1, WGMV-001). b, The split skeleton of Shenshou lui (paratype 2, JZT-CK005A, B).

Extended Data Figure 4 Paratype 3 and skulls of paratypes 1 and 2 of Shenshou lui.

a, Dorsal view of the skeleton of Shenshou lui (paratype 3, JZT-D061). b, Ventral view of the skull of Shenshou lui (paratype 1, WGMV-001). Note the bulging promontorium of the petrosal, the inflected angular process and small right P3. c, Lateral view of the skull and mandible of Shenshou lui (paratype 2, JZT-CK005).

Extended Data Figure 5 Holotype and close-up views of craniodental features of Xianshou linglong (IVPP V16707B).

a, Counterpart of the holotype specimen of Xianshou linglong (IVPP V16707B). ca, caudal vertebrate; ip, intermediate phalanges; lfi, left fibular; lh, left humerus; lra, left radius; lti, left tibia; lu, left ulna; mt, metatarsal; pp, proximal phalanges; r, rib; rfe, right femur; rfi, right fibular; tp, terminal phalanges. b, c, Skull (two sides) and mandibles of Xianshou linglong (IVPP V16707A). b, the skull (ventral view) and left mandible (medial view) and right mandible (labial view). c, the skull (dorsal view) and left mandible (later view); ap, angular process; fr, frontal; glf, glenoid fossa; hy, hyoid; ima, internal acoustic meatus; m, maxilla; mac, mandibular condyle; maf, mandibular foramen; mtf, masseteric fossa; n, nasal; pa, parietal; pm, premaxilla; sm, symphysis of mandible (left); vpt, ventral ridge of pterygoid fossa; za, zygomatic arch. d, Photographs and stippling drawings of the dentition of Xianshou linglong (IVPP V16707). P3 is broken; its crown was left in the matrix so that its outline can be reconstructed in the drawing. The lingual side of P4 and labial side of M1which are exposed or broken are line-hatched. The dentitions were coated with ammonium chloride to enhance contrast. e, Incisors of Xianshou linglong (IVPP V16707A).

Extended Data Figure 6 Close-up views of craniodental features of Xianshou songae (BMNHC-PM003253).

a, Photographs and stippling drawing of the dentition of Xianshou songae (BMNHC-PM003253). The distolingual corner of M2 is not exposed, indicated by hatched lines. P4 and M1are also shown flipped horizontally and the lingual sides of P4 and M1 are not exposed, indicated by hatched lines. The dentition was coated with ammonium chloride to enhance contrast. b, The skull and mandibles of Xianshou songae (BMNHC-PM003253). Note that the right upper and lower dentition are preserved in occlusion, showing that lingual cusp A1 of M1 bites into the valley of upper M2. amf, anterior border of the masseteric fossa; mac, mandibular condyle; maf, mandibular foramen; ptf, pterygoid fossa. c, Teeth in situ of Xianshou songae (BMNHC-PM003253).

Extended Data Figure 7 Wear facets and skeletal features of euharamiyidans.

a, Left lower dentition of Shenshou lui (LDNHMF2001) in lingual view. The image shows the wear facets on lingual sides of the lingual cusps. b, Left P4–M2 of Shenshou lui (LDNHMF2001), coated with ammonium chloride to enhance contrast, in roughly occlusal view. c, Wear facets in the basins of the P3,4 and on the buccal sides of P3–M1. These wear facets indicate that A1 of P4 must have occluded into the P3,4 basins or moved from P3 to P4 basins. The wear facets also indicate that the lingual cusp rows of the lower molars bite into the central valley of the upper molars so that the lingual and buccal sides of the lingual lower cusps and the lingual side of the lower buccal cusps bear wear facets. Similarly, the buccal sides of the buccal cusps of upper molars have wear facets. d, Vertebral column in Shenshou lui. L, lumbard; ltp, lumbar transverse process; T, thoracic. e, The distal end of the humerus in Shenshou lui. f, The anterior section of the rib cage in Shenshou lui. g, the right scapula of Shenshou lui.

Extended Data Figure 8 Euharamiyidan manus and pes, and their ternary plots.

a, The manus of Shenshou lui (LDNHMF2001). b, The pes of Shenshou lui (JZT-D061). as, astragalus; cm, calcaneum; ct, capitate; cu, cuboid; en, entocuneiform; ip, intermediate phalanges; mc, metacarpal; mt, metatarsal; pi, pisiform; pp, proximal phalanges; sp, scaphoid; td, trapezoid; tm, trapezium; tp, terminal phalanges; tq, triquetrum; ts, tarsal spur. c, Ternary diagrams showing intrinsic manual and pedal ray III proportions. Ternary plots showing relative metapodial, proximal and intermediate phalangeal lengths for the third digit ray of the hand and foot. The lengths of the third metapodial, proximal phalanx and intermediate phalanx are shown on their respective axes as a percentage of the combined length of the three segments. Compared to both fossil and extant taxa, euharamiyidans have the intrinsic manual and pedal ray proportions typical of arboreal species in which the proximal and intermediate phalanges are long relative to the metapodials. Ar, Arboroharamiya jenkinsi; Eo, Eomaia scansoria; Je, Jeholodens jenkinsi; Ma, Maotherium sinensis; Sb, Sinobaatar lingyuanensis; Sd, Sinodelphys szalayi; Sh, Shenshou; Xl, Xianshou linglong; Xs, Xianshou songae.

Extended Data Figure 9 The strict consensus tree of 198 equally most parsimonious trees.

Tree length = 2,509; consistency index (CI) = 0.3304; homoplasy index (HI) = 0.6696; retention index (RI) = 0.7901. The simplified version of this consensus tree is presented in Fig. 4. Note that Tinodon was placed as the sister taxon of Allotheria in this cladogram, which is inconsistent with the taxonomic position of the genus33. This tree topology and that in Extended Data Fig. 10b show the phylogenetic instability of Tinodon, as in other studies11,16,17,40, that may be attributed to a significant amount of missing data. However, the current phylogenetic position of Tinodon may reflect the possibility that the allotherian tooth pattern, as represented by Haramiyavia, was derived by developing an extra cusp row from a triconodont-like tooth pattern or even from a tooth pattern with an initially reversed triangular cusp arrangement, as discussed in the main text. Better material is needed to secure the phylogenetic position of Tinodon and to test our hypothesis. See Supplementary Information, section H, for methods as well as tree 1 and related data.

Extended Data Figure 10 Strict consensus trees with Megaconus and without both Megaconus and Hadrocodium.

a, The strict consensus tree of 133 equally most parsimonious trees (including Megaconus). Tree length = 2,528; CI = 0.3283; HI = 0.6717; RI = 0.7910. Note that Megaconus is separated from allotherians and placed outside the crown mammals. This suggests that the placement of Megaconus in allotherians40 needs to be tested when new material becomes available. See Supplementary Information, section E, for discussion. b, The strict consensus tree of 101 equally most parsimonious trees without Megaconus and Hadrocodium. Tree length = 2,448; CI = 0.3386; HI = 0.6614; RI = 0.7952. See Supplementary Information, section G, for discussion. Note that Tinodon is clustered with other ‘symmetrodonts’ plus the clade leading to therians, and that eutriconodonts are split into two groups. See Supplementary Information, sections E and G, for discussion.

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Bi, S., Wang, Y., Guan, J. et al. Three new Jurassic euharamiyidan species reinforce early divergence of mammals. Nature 514, 579–584 (2014). https://doi.org/10.1038/nature13718

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