Northern Pygmy Right Whales Highlight Quaternary Marine Mammal

1 This is the peer reviewed version of the following article: Tsai C-H, Collareta A, Fitzgerald 2 EMG, et al. (2017) Northern pygmy right whales highlight Quaternary marine mammal 3 interchange. Current Biology, 27, R1058-R1059, which has been published in final form at 4 http://www.cell.com/current-biology/fulltext/S0960-9822(17)31096-5. 5 6 Northern pygmy right whales highlight Quaternary marine 7 mammal interchange 8 9 Cheng-Hsiu Tsai1,2,†, Alberto Collareta3,4,†, Erich M. G. Fitzgerald5,6, Felix G. 10 Marx5,7,8,*, Naoki Kohno1,9, Mark Bosselaers8,10, Gianni Insacco11, Agatino Reitano11, 11 Rita Catanzariti12, Masayuki Oishi13,14 and Giovanni Bianucci3 12 13 14 The pygmy right whale, Caperea marginata, is the most enigmatic living whale. 15 Little is known about its ecology and behaviour, but unusual specialisations of visual 16 pigments [1], mitochondrial tRNAs [2], and postcranial anatomy [3] suggests a 17 lifestyle different from that of other extant whales. Geographically, Caperea 18 represents the only major baleen whale lineage entirely restricted to the Southern 19 Ocean. Caperea-like fossils, the oldest of which date to the Late Miocene, are 20 exceedingly rare and likewise limited to the Southern Hemisphere [4], despite a more 21 substantial history of fossil sampling north of the equator. Two new Pleistocene 22 fossils now provide unexpected evidence of a brief and relatively recent period in 23 geological history when Caperea occurred in the Northern Hemisphere. 24 The new material, referable to Caperea sp. and cf. Caperea, respectively, 25 consists of a fragmentary skull with ear bones (USNM 358972) from the upper 26 portion of the Naha Formation of Okinawa-jima, Japan, dating to 0.9–0.5 Ma; and a 27 tympanic bulla (MSNC 4451) from an unnamed deposit on Penisola Maddalena, near 28 Syracuse (Sicily, Italy), dating to 1.9–1.7 Ma (Supplemental Information). The 29 tympanic bullae of both specimens are highly diagnostic, and identifiable based on 30 their (i) rectangular Eustachian outlet; (ii) flattened involucrum lacking any sign of an 31 inner posterior prominence; (iii) broadly convex medial margin; (iv) prominent, 32 angular anteromedial corner; and (v) L-shaped dorsal profile of the involucrum 33 (Figure 1). USNM 358972 furthermore shares with extant Caperea the presence of 34 (vi) an elongate squamosal fossa; (vii) a foramen pseudovale enclosed entirely by the 35 pterygoid; (viii) a narrow, sulcus-like Eustachian notch; (ix) a delicate connection 36 between the anterior process and the body of the periotic; (x) an anteriorly directed 37 anteroexternal sulcus on the anterior process of the periotic; and (xi) a robust, conical 38 and externally exposed compound posterior process of the tympanoperiotic (Figure 1; 39 Supplemental Information). In features (vii) and (ix), USNM 358972 differs from the 40 only named extinct relative of Caperea, Miocaperea pulchra, from the Late Miocene 41 of Peru [5]. MSNC 4451 and Miocaperea currently cannot be compared as the bulla 42 morphology remains unknown for the latter. Nevertheless, the notable similarity of 43 MSNC 4451 and living pygmy right whales justifies referral to cf. Caperea. 44 The Northern Hemisphere material of Caperea could conservatively be 45 interpreted as extralimital occurrences of the living species, yet it also provides 40% 46 of the total putative fossil record of the family, two thirds of the undisputed record, 47 and the only fossil evidence of Caperea itself [4]. Considering the vagaries of fossil 48 preservation, the occurrence of two geologically young northern specimens is thus 49 likely more than a chance event. Instead, the striking absence of Caperea in 50 comparatively well-studied northern Miocene–Pliocene fossil assemblages suggests a 51 Pleistocene ecological regime change. The latter was presumably glacially-driven, 52 e.g. via changes in seasonal nutrient distributions, and temporarily allowed localised 53 marine mammal species to disperse across the normally impermeable tropics. 54 Evidence of such dispersal exists among living cetaceans and pinnipeds in the form of 55 antitropical species pairs, such as Eubalaena, Lissodelphis and Mirounga 56 (Supplemental Discussion). 57 The new Caperea fossils from the Northern Hemisphere demonstrate that 58 there was likely a greater degree of marine faunal interchange during the Pleistocene 59 than hitherto assumed, and that it affected even highly localised specialists. In light of 60 our findings, other highly unusual occurrences, even southern walruses and northern 61 penguins, should be anticipated. The fact that the two fossils are separated by as much 62 as one million years raises the tantalising possibility that a separate long-lived 63 population, or even species, of Caperea may once have inhabited northern seas. 64 Given the sparseness of available material, it is equally likely, however, that Caperea 65 crossed the equator more than once during successive glacial periods (Supplementary 66 Material), and then disappeared again as interglacial conditions interrupted the 67 connection with the south. 68 Together, extant antitropical species pairs and sudden range extensions like 69 that of Caperea emphasise that, at times, physical and biotic barriers play a major role 70 in marine mammal evolution [6, 7]. The Pleistocene with its constant change between 71 glacial and interglacial conditions is a prime example, with the relaxation and 72 subsequent re-establishment of an equatorial barrier driving range extensions, 73 speciations and, in the case of Caperea, local extinctions. A globally poor Pleistocene 74 fossil record likely obscures the true extent of this Quaternary marine interchange. 75 Nevertheless, faunal interchange during the Pleistocene had a pronounced effect on 76 marine mammal richness and community structure, and can be seen as the last major 77 step in the emergence of modern marine mammal assemblages. This adds a new layer 78 on to previous studies, which suggested that faunal modernisation primarily occurred 79 in response to a related, yet independent (Late) Pliocene turnover event (Supplemental 80 Discussion). 81 While Pliocene turnover was likely driven by the onset of Northern 82 Hemisphere glaciation (resulting in the loss of coastal habitats) [8], the Quaternary 83 marine interchange is related to the change between glacial and interglacial periods, 84 and as such still ongoing – albeit now with a human dimension. Just as glacial- 85 interglacial dynamics affect marine barriers to dispersal, anthropogenic climate 86 change may ultimately drive a reorganisation of current marine mammal ranges, with 87 implications for future speciation and, crucially, extinction. For example, a warmer 88 world might see poleward range shifts among extant marine mammals [9] and the 89 establishment of a ‘permanent’ El Niño state in the tropics [10], thereby cementing 90 the impassability of the equator and further restricting (or obliterating) gene flow 91 between existing populations. 92 93 SUPPLEMENTAL INFORMATION 94 Supplemental Information including further details on morphology and stratigraphic 95 context can be found with this article online at XXX 96 97 AUTHOR CONTRIBUTIONS 98 A.R. discovered and G.I. collected MSNC 4451. M.O., A.C. and M.B. first identified 99 the fossils. A.C., R.C., N.K., C.-H.T. and F.G.M. established their provenance and 100 age. F.G.M, E.M.G.F. and G.B. organised the collaborative project. All authors 101 discussed and wrote the paper. 102 103 ACKNOWLEDGEMENTS 104 C.-H.T. was funded by a University of Otago Doctoral Scholarship and a postdoctoral 105 fellowship from the Japan Society for the Promotion of Science (P15329). E.M.G.F. 106 was supported by a postdoctoral fellowship from the Smithsonian Institution, and 107 funding from the Harold Mitchell Foundation and Museums Victoria. F.G.M. was 108 funded by an EU Marie Skłodowska-Curie Global Postdoctoral fellowship (656010/ 109 MYSTICETI) and by a postdoctoral fellowship from the Japan Society for the 110 Promotion of Science (P13505). N.K. was funded by a JSPS Grant-in-Aid for 111 Scientific Research C (15K05333). M.O. was funded by an Oversea Dispatch 112 Training for Curators of the Ministry of Education, Japan and Kamei Social- 113 Education Promotion Foundation. N. Pyenson, D. Bohaska, the late F. Whitmore, J. 114 Mead, C. Potter, J. Ososky, K. Date, K. Roberts, O. Lambert and S. Bruaux provided 115 access to museum collections. Thanks to O. Lambert and two anonymous reviewers 116 for their helpful comments, as well as C. Buell for his illustration. 117 118 REFERENCES 119 1. 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