Current Biology Magazine

B Extant Correspondence A -120 -90 -60 -30 0 30 60 Caperea 0

USNM 358972 Northern pygmy 1 MSNC 4451 USNM MSNC 4451 Northern right whales 2 hemisphere

358972 Pleistocene highlight Quaternary 3 Northern Miocaperea hemisphere marine pulchra 4 glaciation Pliocene interchange Extant Caperea marginata 5 MPEF-PV2572 NMV NMV P161709 6 P161709 Cheng-Hsiu Tsai1,2,15, Alberto 3,4,15 5,6 C 7 Miocaperea Collareta , Erich M.G. Fitzgerald , 30 mm v pulchra 5,7,8, 1,9 a Felix G. Marx *, Naoki Kohno , 8 8,10 11 Mark Bosselaers , Gianni Insacco , Delicate attachment Agatino Reitano11, Rita Catanzariti12, 9 of anterior process Southern hemisphere 13,14 Masayuki Oishi , Enlarged compound 10 MPEF-PV2572 3 posterior process and Giovanni Bianucci D

The , Caperea 30 mm marginata, is the most enigmatic living whale. Little is known about its ecology and behaviour, but unusual specialisations of visual pigments Prominent [1], mitochondrial tRNAs [2], and Squared anterior 20 mm E border of bulla anteromedial postcranial anatomy [3] suggest a corner lifestyle different from that of other extant whales. Geographically, Caperea Flattened dorsal profile of involucrum represents the only major baleen F L-shaped whale lineage entirely restricted to involucrum the Southern Ocean. Caperea-like fossils, the oldest of which date to the Late Miocene, are exceedingly rare and likewise limited to the Southern Hemisphere [4], despite a more substantial history of fossil Convex medial sampling north of the equator. Two a margin of bulla a new Pleistocene fossils now provide m v unexpected evidence of a brief and relatively recent period in geological Figure 1. Pygmy right whales in the Northern and Southern hemispheres. history when Caperea occurred in the (A) Global map showing the presumed distribution of extant Caperea marginata (in blue), Caperea Northern Hemisphere (Figure 1A,B). fossils from the Northern Hemisphere (red squares), and Caperea-like fossils from the Southern The new material, referred to as Hemisphere (green squares). (B) Global sea-level change over time compared to the age of the fossils shown in (A). See Supplemental Information for data sources. Note the clustering of North- Caperea sp. and cf. Caperea, consists ern Hemisphere specimens during the Pleistocene. (C) Right periotic and compound posterior of, respectively, a fragmentary skull with process of extant Caperea marginata, NMV C28531, compared to Caperea sp., USNM 358972. ear bones (USNM 358972) from the (D) Tympanic bulla of extant Caperea marginata, NMNZ MM002119 (right bulla, mirrored horizon- upper portion of the Naha Formation tally for comparison), compared to (E) Caperea sp., USNM 358972 and (F) cf. Caperea, MSNC of Okinawa-jima, Japan (0.9–0.5 Ma) 4451. Drawing of Caperea by Carl Buell. and a tympanic bulla (MSNC 4451) from an unnamed deposit on Penisola profi le of the involucrum, in dorsal and a robust, conical and externally Maddalena, near Syracuse, Sicily, view (Figure 1C–F). USNM 358972 exposed compound posterior process Italy (1.9–1.7 Ma) (Supplemental furthermore shares with extant Caperea of the tympanoperiotic (Figure 1C, Information). The tympanic bullae of the presence of: an elongate squamosal S2A–D,F). In the morphology of both specimens are highly diagnostic, fossa; a foramen pseudovale enclosed the foramen pseudovale and the and identifi able based on their: entirely by the pterygoid; a narrow, connection of the anterior process rectangular Eustachian outlet; fl attened sulcus-like Eustachian notch; a delicate to the periotic, USNM 358972 differs involucrum lacking any sign of an inner connection between the anterior from the only named extinct relative of posterior prominence; broadly convex process and the body of the periotic; an Caperea — Miocaperea pulchra, from medial margin; prominent, angular anteriorly directed anteroexternal sulcus the Late Miocene of Peru [5]. MSNC anteromedial corner; and L-shaped on the anterior process of the periotic; 4451 and Miocaperea currently cannot

R1058 Current Biology 27, R1037–R1059, October 9, 2017 © 2017 Elsevier Inc. Current Biology Magazine

be compared, as the bulla morphology play a major role in marine mammal established their provenance and age. F.G.M, remains unknown for the latter. evolution [6,7]. The Pleistocene E.M.G.F. and G.B. organised the collaborative Nevertheless, the notable similarity of with its constant change between project. All authors discussed and wrote the MSNC 4451 and living pygmy right glacial and interglacial conditions is paper. whales justifi es referral to cf. Caperea. a prime example, with the relaxation The Northern Hemisphere material and subsequent re-establishment of REFERENCES of Caperea could conservatively be an equatorial barrier driving range 1. Meredith, R.W., Gatesy, J., Emerling, C.A., interpreted as extralimital occurrences extensions, speciations and, in the York, V.M., and Springer, M.S. (2013). Rod of the living species, yet it also case of Caperea, local extinctions. A monochromacy and the coevolution of cetacean retinal opsins. PLoS Genet 9, e1003432. provides 40% of the total putative globally poor Pleistocene fossil record 2. Montelli, S., Peruffo, A., Patarnello, T., Cozzi, B., fossil record of the family, two thirds likely obscures the true extent of and Negrisolo, E. (2016). Back to water: signature of adaptive evolution in cetacean of the undisputed record, and the this Quaternary marine interchange. mitochondrial tRNAs. PLoS One 11, e0158129. only fossil evidence of Caperea itself Nevertheless, faunal interchange during 3. Buchholtz, E.A. (2011). Vertebral and rib [4]. Considering the vagaries of fossil the Pleistocene had a pronounced anatomy in Caperea marginata: implications for evolutionary patterning of the mammalian preservation, the occurrence of two effect on marine mammal richness vertebral column. Mar. Mamm. Sci. 27, 382–397. geologically young northern specimens and community structure, and can 4. Buono, M.R., Dozo, M.T., Marx, F.G., and Fordyce, R.E. (2014). A Late Miocene potential is thus likely more than a chance be seen as the last major step in the neobalaenine mandible from Argentina sheds event. Instead, the striking absence of emergence of modern marine mammal light on the origins of the living pygmy right Caperea in comparatively well-studied assemblages. This adds a new layer whale. Acta Palaeontol. Pol. 59, 787–793. 5. Bisconti, M. (2012). Comparative osteology northern Miocene–Pliocene fossil to previous studies, which suggested and phylogenetic relationships of Miocaperea assemblages suggests a Pleistocene that faunal modernisation primarily pulchra, the fi rst fossil pygmy right whale genus and species (, Mysticeti, ). ecological regime change. The latter occurred in response to a related, yet Zool. J. Linn. Soc. Lond. 166, 876–911. was presumably glacially driven (for independent (Late) Pliocene turnover 6. Davies, J.L. (1963). The antitropical factor in example, via changes in seasonal event (Supplemental Discussion). cetacean speciation. Evolution 17, 107–116. 7. Lindberg, D.R. (1991). Marine biotic nutrient distributions) and temporarily While Pliocene turnover was likely interchange between the northern and southern allowed localised marine mammal driven by the onset of Northern hemispheres. Paleobiology 17, 308–324. 8. Pimiento, C., Griffi n, J.N., Clements, C.F., species to disperse across the normally Hemisphere glaciation (resulting in Silvestro, D., Varela, S., Uhen, M.D., and impermeable tropics. Evidence of the loss of coastal habitats) [8], the Jaramillo, C. (2017). The Pliocene marine such dispersal exists among living Quaternary marine interchange is megafauna extinction and its impact on functional diversity. Nat. Ecol. Evol. 1, 1100–1106. cetaceans and pinnipeds in the form related to the switch between glacial 9. Kaschner, K., Tittensor, D.P., Ready, J., of antitropical species pairs, such as and interglacial periods, and as such Gerrodette, T., and Worm, B. (2011). Current and future patterns of global marine mammal Eubalaena, Lissodelphis and Mirounga still ongoing — albeit now with a human biodiversity. PLoS One 6, e19653. (Supplemental Discussion). dimension. Just as glacial–interglacial 10. Fedorov, A.V., Dekens, P.S., McCarthy, M., The new Caperea fossils from the dynamics affect marine barriers to Ravelo, A.C., deMenocal, P.B., Barreiro, M., Pacanowski, R.C., and Philander, S.G. (2006). Northern Hemisphere demonstrate dispersal, anthropogenic climate change The Pliocene paradox (mechanisms for a that there was likely a greater degree may ultimately drive a reorganisation permanent El Niño). Science 312, 1485–1489. of marine faunal interchange during of current marine mammal ranges, the Pleistocene than hitherto assumed, with implications for future speciation 1Department of Geology and Palaeontology, and that this interchange affected and, crucially, extinction. For example, National Museum of Nature and Science, 2 even highly localised specialists. a warmer world might see poleward Tsukuba, 305-0005, Japan. Department of Geology, University of Otago, Dunedin, 9054, In light of our fi ndings, other highly range shifts among extant marine New Zealand. 3Dipartimento di Scienze della unusual occurrences, even southern [9] and the establishment Terra, Universitá di Pisa, Pisa, 56126, Italy. walruses and northern penguins, of a ‘permanent’ El Niño state in the 4Dottorato Regionale in Scienze della Terra should be anticipated. The fact that tropics [10], thereby cementing the Pegaso, Pisa, 56126, Italy. 5Geosciences, the two fossils are separated by as impassability of the equator and further Museums Victoria, Melbourne, Victoria, 6 much as one million years raises the restricting (or obliterating) gene fl ow 3001, Australia. National Museum of Natural History, Smithsonian Institution, Washington, tantalising possibility that a separate between existing populations. DC, 20013-7012, USA. 7School of Biological long-lived population, or even species, Sciences, Monash University, Clayton, Victoria, of Caperea may once have inhabited SUPPLEMENTAL INFORMATION 3800, Australia. 8D.O. Terre et Histoire de la northern seas. Given the sparseness Vie, Institut Royal des Sciences Naturelles de Belgique, Brussels, 1000, Belgium. 9Graduate of available material, it is equally Supplemental Information includes supple- School of Life and Environmental Sciences, likely, however, that Caperea crossed mental experimental procedures,discussion University of Tsukuba, Tsukuba, 305-8752, the equator more than once during and references, and two fi gures and can be Japan. 10Koninklijk Zeeuwsch Genootschap successive glacial periods, and then found with this article online at http://dx.doi. der Wetenschappen, Middelburg, 4331 JE, The disappeared again as interglacial org./10.1016.j.cub.2017.08.056. Netherlands. 11Museo Civico di Storia Naturale conditions interrupted the connection di Comiso, Comiso, 97013, Ragusa, Italy. with the south. 12Istituto di Geoscienze e Georisorse, IGG-CNR, AUTHOR CONTRIBUTIONS 13 Together, extant antitropical species Pisa, 56124, Italy. Iwate Prefectural Museum, Morioka, 020-0102, Japan. 14Tohoku University pairs and sudden range extensions A.R. discovered and G.I. collected MSNC Museum, Sendai, 980-8578, Japan. 15These like that of Caperea emphasise that, 4451. M.O., A.C. and M.B. fi rst identifi ed the authors contributed equally to the work. at times, physical and biotic barriers fossils. A.C., R.C., N.K., C.-H.T. and F.G.M. *E-mail: [email protected]

Current Biology 27, R1037–R1059, October 9, 2017 R1059