Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution

As one of the earliest-known mammaliaforms, Haramiyavia clemmenseni from the Rhaetic (Late Triassic) of East Greenland has held an important place in understanding the timing of the earliest radiation of the group. Reanalysis of the type specimen using high-resolution computed tomography (CT) has revealed new details, such as the presence of the dentary condyle of the mammalian jaw hinge and the postdentary trough for mandibular attachment of the middle ear—a transitional condition of the predecessors to crown Mammalia. Our tests of competing phylogenetic hypotheses with these new data show that Late Triassic haramiyids are a separate clade from multituberculate mammals and are excluded from the Mammalia. Consequently, hypotheses of a Late Triassic diversification of the Mammalia that depend on multituberculate affinities of haramiyidans are rejected. Scanning electron microscopy study of tooth-wear facets and kinematic functional simulation of occlusion with virtual 3D models from CT scans confirm that Haramiyavia had a major orthal occlusion with the tallest lingual cusp of the lower molars occluding into the lingual embrasure of the upper molars, followed by a short palinal movement along the cusp rows alternating between upper and lower molars. This movement differs from the minimal orthal but extensive palinal occlusal movement of multituberculate mammals, which previously were regarded as relatives of haramiyidans. The disparity of tooth morphology and the diversity of dental functions of haramiyids and their contemporary mammaliaforms suggest that dietary diversification is a major factor in the earliest mammaliaform evolution.Haramiyidans are among the first mammaliaforms to appear during the Late Triassic in the evolutionary transition from premammalian cynodonts. Their fossils have a cosmopolitan distribution during the Late Triassic to the Jurassic (1–8), tentatively with the youngest record in the Late Cretaceous of India (9). Most of these occurrences are of isolated teeth. For this reason, Haramiyavia clemmenseni (1) holds a special place in mammaliaform phylogeny: It is the best-preserved Late Triassic haramiyid with intact molars, nearly complete mandibles, and also postcranial skeletal elements (Figs. 1 and ​and22 and SI Appendix, Figs. S1–S4) (1). By its stratigraphic provenance from the Tait Bjerg Beds of the Fleming Fjord Formation, East Greenland (Norian-Rhaetic Age) (7), Haramiyavia is also the oldest known haramiyid (5, 7). Haramiyids, morganucodonts, and kuehneotheriids are the three earliest mammaliaform groups that are distinctive from each other in dental morphology and masticatory functions (10–12).Open in a separate windowFig. 1.(A and B) Composite reconstruction of Haramiyavia clemmenseni right mandible in lateral (A) and medial (B) views. Dark red: original bone with intact periosteal surface; brown: broken surface of preserved bone or remnant of bone; light blue: morphologies preserved in mold outlines or clear impression. (C) Morganucodon mandible in medial view.Open in a separate windowFig. 2.Molar features of Haramiyavia. (A) Right M1–M3 in occlusal view (medio-lateral orientation by the zygomatic root and the palate). (B) Occlusal facets of upper molars. (C) Lingual view of M1–M3. (D) Root structures of upper molars (M1 and M2 show three partially divided anterior roots connected by dentine and two posterior roots connected by dentine; M3 has two anterior and two posterior roots connected respectively by dentine). These roots have separate root canals. (E) Buccal view of M1–M3. All roots are bent posteriorly, suggesting that crowns shifted mesially, relative to the roots, during the tooth eruption, also known as mesial drift of teeth (arrowhead), typical of successive eruption of multirooted postcanines. (F) SEM photograph of lower m3 in a posterior occlusal view. (G) Approximate extent of wear facets by orthal occlusion (a1 cusp in embrasure of upper molars) (blue) and palinal movement of b2–b4 cusps sliding across the median furrow of upper molars (green). (H) Lingual view of m3. There are no wear facets on lingual side of cusps a1–a4. (I) Buccal view of m3 showing wear facets on the buccal sides of cusps b1–b4 and on apices.Haramiyids are characterized by their complex molars with longitudinal rows of multiple cusps. The cusp rows occlude alternately between the upper and lower molars. Primarily because of similarities in molar morphology, haramiyids are considered to be related to poorly known theroteinids of the Late Triassic (5, 13) and eleutherodontids of the Middle to Late Jurassic (14–17). Collectively haramiyids and eleutherodontids are referred to as “haramiyidans” (10, 14, 15, 18, 19). Recent discoveries of diverse eleutherodontids or eleutherodontid-related forms with skeletons from the Tiaojishan Formation (Middle to Late Jurassic) of China (18–20) have greatly augmented the fossil record of haramiyidans, ranking them among the most diverse mammaliaform clades of the Late Triassic and Jurassic.Historically, it has been a contentious issue whether haramiyidans (later expanded to include theroteinids and eleutherodontids) are closely related to the more derived multituberculates from the Middle Jurassic to Eocene (13) or represent a stem clade of mammaliaforms excluded from crown mammals (21, 22). The conflicting placement of haramiyidans was attributable in part to the uncertainties in interpreting the isolated teeth of most Late Triassic haramiyids (21, 22). More recent phylogenetic disagreements have resulted from different interpretations of mandibular characters in Haramiyavia (17–20, 23–25), which has not been fully described (figure 2 in ref. 1).Here we present a detailed study of the mandibles and teeth of Haramiyavia from the exhaustive documentation during initial fossil preparation (Fig. 1 and SI Appendix, Figs. S1–S4), from scanning electron microscopy (SEM) images, and from computed tomography (CT) scans and 3D image analyses of the two fossil slabs with mandibles (MCZ7/95A and B), plus a referred specimen of upper molars in a maxilla (MCZ10/G95) (Figs. 2 and ​and3,3, SI Appendix, Figs. S5–S8 and Tables S2 and S3, and Movie S1). These new data are informative for testing alternative mammaliaform phylogenies (Fig. 4 and SI Appendix) and are useful for reconstructing evolutionary patterns of feeding function in the earliest mammaliaforms.Open in a separate windowFig. 3.Molar occlusion of haramiyids. (A) In Haramiyavia the upper and lower molars form an en echelon pattern, a series of parallel and step-like occlusal surfaces in lingual and buccal views (based on 3D scaled models from CT scans of MCZ7/G95 and MCZ10/G95). (B–E) In Haramiyavia are shown the occlusal paths of cusps a1–a4 of the lingual row (B), cusps b2–b4 of the buccal row (shown with the lingual half of the tooth cut away) (C), and tooth orientation and the cut-away plane (D). During the orthal occlusion phase, the tallest lingual cusp a1 occludes into the embrasure of the preceding and the opposing upper molars (B and E), and the tallest buccal cusp b2 occludes into the upper furrow and behind the A1–B1 saddle of the upper molar (C). During the palinal occlusion phase, cusps b1–b4 of the buccal row slide posteriorly in the upper furrow, and in the upper row cusps B5–B1 slide in the lower furrow (lower molars with blue and green shading, superpositioned by flipped upper molar in clear outlines) (E). (F) Extent of wear on molars during the orthal phase (blue) and the palinal movement (green) produced by OFA simulation (Movie S1). (G–I) In Thomasia, reconstruction of upper and lower molar series on the basis of wear surfaces and tooth crown morphology (revised from refs. 2, 3, and 10). (G) The en echelon occlusal surfaces in lingual view. (H) Orthal occlusion (blue) is followed by palinal occlusal movement (green). (I) Occlusal wear facets of molars. Facets worn by orthal occlusion are shown in blue, and facets worn by palinal occlusion are shown in gray hatching. Cusp and facet designations are after refs 3 and 6.Open in a separate windowFig. 4.Hypotheses concerning the phylogenetic relationship of Haramiyavia and timing estimates of the basal diversification of crown mammals. (A) Haramiyavia is a close relative of multituberculates, both nested in the crown Mammalia. This hypothesis (haramiyidan node position 1) was based on a misinterpretation of a previous illustration of a fragment of the mandible (17, 18). (B) Haramiyavia is a stem mammaliaform, as determined by incorporating the features preserved on both mandibles into phylogenetic estimates (haramiyidan node position 2). (C) Placement of Haramiyavia and other haramiyidans among mammaliaforms according to this study. Many mandibular features were treated as unknown by studies favoring a Late Triassic diversification of mammals (18, 23). A more complete sampling of informative features revealed by this study now has overturned the previous placement. Clades: crown Mammalia (node a); Mammaliaformes (node b); haramiyidans (node 1 or 2, alternative positions); Eleutherodontida (node c). The rescored datasets and analyses are presented in SI Appendix.