LETTER doi:10.1038/nature10880 Adaptive radiation of multituberculate mammals before the extinction of dinosaurs Gregory P. Wilson1, Alistair R. Evans2, Ian J. Corfe3, Peter D. Smits1,2, Mikael Fortelius3,4 & Jukka Jernvall3 TheCretaceous–Paleogene mass extinction approximately 66 million the ecological rise of angiosperms8 and suggests that the resources years ago is conventionally thought to have been a turning point in that were available to multituberculates were relatively unaffected mammalian evolution1,2. Prior to that event and for the first two- by the Cretaceous–Paleogene mass extinction. Taken together, our thirds of their evolutionary history, mammals were mostly confined results indicate that mammals were able to take advantage of new to roles as generalized, small-bodied, nocturnal insectivores3, ecological opportunities in the Mesozoic and that at least some of presumably under selection pressures from dinosaurs4. Release these opportunities persisted through the Cretaceous–Paleogene from these pressures, by extinction of non-avian dinosaurs at the mass extinction. Similar broad-scale ecomorphological inventories Cretaceous–Paleogene boundary, triggered ecological diversification of other radiations may help to constrain the possible causes of mass of mammals1,2. Although recent individual fossil discoveries have extinctions9,10. shown that some mammalian lineages diversified ecologically during Multituberculate mammals were a taxonomically rich3,11 and the Mesozoic era5, comprehensive ecological analyses of mammalian numerically abundant12 clade that had originated by the Middle groups crossing the Cretaceous–Paleogene boundary are lacking. Jurassic epoch (approximately 165 million years (Myr) ago) and went Such analyses are needed because diversification analyses of living extinct in the late Eocene (approximately 35 Myr ago)3,11. They were taxa6,7 allow only indirect inferencesof past ecosystems. Here weshow nearly globally distributed13 and had a distinctive dentition consisting that in arguably the most evolutionarily successful clade of Mesozoic of procumbent incisors, blade-like premolars, molars with longitudinal mammals, the Multituberculata, an adaptive radiation began at least rows of cusps (Fig. 1) and a predominantly posteriorly directed (palinal) 20 million years before the extinction of non-avian dinosaurs and chewing motion14,15. continued across the Cretaceous–Paleogene boundary. Disparity in Palaeontologists have agreed for a long time that the success of dental complexity, which relates to the range of diets, rose sharply in multituberculate mammals was at least partly related to their highly step with generic richness and disparity in body size. Moreover, derived dentition. Despite this, there is little consensus on the inter- maximum dental complexity and body size demonstrate an adaptive pretations of their feeding ecology, perhaps owing to the limitations of shift towards increased herbivory. This dietary expansion tracked previous approaches. For example, toothwear analysis is time intensive a Buccal Occlusal OPC p4 m2 m1 p3 p2 p1 Ctenacodon (155–148 Myr ago) OPC 84.375 b p4 m2 m1 Ptilodus (65–56 Myr ago) OPC 106.75 c m2 m1 p4 Cimolomys (84–66 Myr ago) OPC 202.125 d m2 m1 p4 1 mm + Taeniolabis (65–64 Myr ago) OPC 347.625 − Height Orientation Figure 1 | Cretaceous cimolomyid Cimolomys gracilis (c), Paleocene taeniolabidid Dental and dietary diversity in multituberculate mammals. a–d, Three- Taeniolabis taoensis (d). Surface orientation map of each three-dimensional dimensional buccal–occlusal and occlusal reconstructions of multituberculate reconstruction (colour wheel indicates orientation) for OPC measurements lower-right cheek tooth rows for GIS analysis: Late Jurassic plagiaulacid (shown by the number of coloured patches). Clumps that are smaller than three Ctenacodon serratus (a), Paleocene ptilodontoid Ptilodus kummae (b), Late grid points (black) are ignored. p, premolar; m, molar. Scale bars, 1 mm. 1Department of Biology, University of Washington, Seattle, Washington 98195-1800, USA. 2School of Biological Sciences, Monash University, Victoria 3800, Australia. 3Developmental Biology Program, Institute of Biotechnology, University of Helsinki, PO Box 56, FIN-00014, Helsinki, Finland. 4Department of Geosciences and Geography, University of Helsinki, PO Box 64, FIN-00014, Helsinki, Finland. 22 MARCH 2012 | VOL 483 | NATURE | 457 ©2012 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER and requires high-quality preservation15, and multituberculates lack when comparing morphologically and phylogenetically divergent taxa. living descendants and this hampers comparative studies. Inter- Orientation patch count (OPC), a measure of dental complexity, was pretations of multituberculate feeding ecology therefore vary widely; calculated as the number of discrete surfaces on the cheek tooth row they have been proposed to be broad herbivores, frugivores, granivores, distinguished by differences in orientation (for example, north, root- and bark-eaters, egg-eaters, insectivores, carnivores and southwest; Fig. 1). Extant rodents, carnivorans and bats demonstrate omnivores15–17. a robust correlation between OPC and feeding ecology; OPC increases To obtain a robust and comprehensive view of multituberculate across the dietary spectrum from carnivores toomnivores to herbivores, ecomorphological diversity through time, we quantified dental com- despite many differences in specific tooth components, body size plexity in 41 genera using geographic information systems (GIS) and chewing mechanics among these taxa18,19. For a given clade, the analyses18 of three-dimensional crown surfaces of lower cheek teeth standard deviation of OPC is an effective proxy for the dietary diver- (Fig. 1; Supplementary Table 1). These analyses do not require cusp sification and divergence in feeding function: higher standard devi- and facet homologies to be established, which can be a challenging task ation means greater dental disparity and a broader range of diets. OPC thus offers promise as a powerful tool for quantifying overall tooth K–Pg shape and inferring diet in extinct taxa, such as multituberculates, that 80100120140160180 60 40 have highly derived dentitions with uncertain homology with living a mammals and imprecise functional analogy. 350 60 Among the earliest multituberculates, the ‘Plagiaulacida’ are a Dental-complexity disparity 300 paraphyletic assemblage of taxa with up to four simple blade-like 50 premolars and two multi-cusped molars (Fig. 1a). OPC analyses of 250 ‘plagiaulacids’ from the Late Jurassic through to the Early Cretaceous 40 (s.d.) 200 Herbivore epoch (from 156–100 Myr ago) show low and tightly constrained PD Omni 30 dental complexity (Fig. 2a; OPC, 84–125). Their OPC values corre- 150 Mean dental spond to carnivory and the low end of animal-dominated omnivory complexity (OPC) AD Omni 100 20 among extant mammals (for example, eating both insects and fruits). Carnivore Multituberculates in the early Late Cretaceous (100–84 Myr ago), 50 10 which include mostly basal members of the suborder Cimolodonta, Hypercarn 0 0 had a slightly higher mean OPC than did the ‘plagiaulacids’ but b retained the low standard deviation of OPC (Fig. 2a), indicating low 25 morphological disparity. A distinct break occurred 84–66 Myr ago, in the latest Cretaceous, when the mean OPC rose and peaked within the 20 Campanian (mean OPC, 145) and maximum OPC and disparity sharply increased as well (Fig. 2a; OPC, 70–230). Of the 17 taxa for 15 this interval, 5 have OPC values that are greater than 160 and 2 have OPC values that are greater than 200, corresponding to values for 10 plant-dominated omnivory and herbivory among extant mammals, (no. of genera) respectively (Fig. 2a). Taxonomic richness Taxonomic 5 Finally, in the early Paleocene (66–62 Myr ago) multituberculates maintained high OPC (mean OPC, 138) and disparity peaked (Fig. 2a; OPC, 70–348). The early Paleocene Taeniolabis from North 0 c 100 America (Fig. 1d) had the highest OPC among multituberculates (OPC, 348), which exceeded OPC values of extant herbivorous rodents and 2.5 carnivorans18. Of the 16 other early Paleocene taxa, 4 have OPC values 10 Body size disparity greater than 160 and 1 has an OPC value greater than 200 (Fig. 2a). 2.0 Mean OPC and disparity of OPC declined during the remainder of the 1 (s.d.) Paleocene and in the early Eocene (62–49 Myr ago). Ectypodus, the 1.5 only known genus from the middle to late Eocene (49–35 Myr ago), has 0.1 a low OPC (109), corresponding to the high end of the range for extant 1.0 mammalian carnivores. This sharp drop in dental ecomorphological Mean body size (kg) 0.01 0.5 Figure 2 | Temporal patterns of multituberculate dental complexity, taxonomic richness, body size and angiosperm ecological diversification. 0 d a, Dental complexity (measured by OPC) for 41 multituberculate genera (solid black lines) and estimated for 24 additional genera (dashed black lines; see Supplementary Information) with mean dental complexity (OPC; red line) and 40 16 Leaf-vein density disparity as standard deviations of OPC (blue line) in 5-Myr bins. Lengths of (mm per mm horizontal lines represent temporal ranges of taxa or uncertainties in ages of 30 12 fossil localities. Labels for dietary classes are positioned at the lower end of their range based on OPC values in modern mammals18. Green shaded area represents plant-dominated omnivory (PD omni) and herbivory. 20 8 2 ) b, Taxonomic richness is equal to the number