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Swimming Mode Inferred from Skeletal Proportions in the Fossil Pinnipeds Enaliarctos and Allodesmus (Mammalia, Carnivora)

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Abstract

Swimming modes are crucial for understanding evolutionary transitions from land to sea, because locomotion affects many aspects of an animal’s life. The modern pinniped families Otariidae (fur seals and sea lions), Phocidae (true seals), and Odobenidae (walruses) are thought to share a common origin, but each differs in its primary mode of aquatic locomotion. Previous studies of locomotor evolution in pinnipeds suggested: (1) forelimb swimming was ancestral; (2) hind limb swimming evolved once at the base of the clade including Phocidae, Odobenidae, and the extinct Desmatophocidae; and (3) reversal to forelimb swimming occurred in the odobenid subfamily Dusignathinae. The oldest and most basal pinnipedimorph Enaliarctos mealsi has been portrayed as a forelimb swimmer, and the desmatophocid Allodesmus kelloggi has been portrayed as a hind limb swimmer. These interpretations have been questioned by others and are tested here. Principal components analysis of trunk and limb measurements from 58 modern semiaquatic mammals demonstrates that Enaliarctos is most similar in skeletal proportions to hind limb-dominated swimmers, whereas Allodesmus is most similar to forelimb-dominated swimmers. Principal components and discriminant function analyses of trunk and limb measurements from 24 modern pinniped species demonstrate that Enaliarctos is most similar to hind limb-swimming phocids, while Allodesmus is most similar to forelimb-swimming otariids. These interpretations complicate previous portrayals of swimming evolution in pinnipeds and can paint a very different picture of how this behavior evolved when viewed in the context of alternative phylogenetic hypotheses.

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References

  • Árnason Ú, Bodin K, Gullberg A, Ledje C, Suzette M (1995) A molecular view of pinniped relationships with particular emphasis on the true seals. J Mol Evol 40:78–85 doi:10.1007/BF00166598

    Article  PubMed  Google Scholar 

  • Árnason Ú, Gullberg A, Janke A, Kullberg M (2007) Mitogenomic analyses of caniform relationships. Mol Phylogenet Evol 45:863–874 doi:10.1016/j.ympev.2007.06.019

    Article  PubMed  CAS  Google Scholar 

  • Árnason Ú, Gullberg A, Janke A, Kullberg M, Lehman N, Petrov EA et al (2006) Pinniped phylogeny and a new hypothesis for their origin and dispersal. Mol Phylogenet Evol 41:345–354 doi:10.1016/j.ympev.2006.05.022

    Article  PubMed  Google Scholar 

  • Árnason Ú, Widegren B (1986) Pinniped phylogeny enlightened by molecular hybridization using highly repetitive DNA. Mol Biol Evol 3:356–365

    Google Scholar 

  • Barnes LG (1972) Miocene Desmatophocinae (Mammalia: Carnivora) from California. Univ Calif Publ Geol Sci 89:1–76

    Google Scholar 

  • Barnes LG (1987) An early Miocene pinniped of the genus Desmatophoca (Mammalia: Otariidae) from Washington. Contrib Sci Nat Hist Mus LA Co 382:1–20

    Google Scholar 

  • Barnes LG (1989) A new enaliarctine pinniped from the Astoria Formation, Oregon, and a classification of the Otariidae (Mammalia: Carnivora). Contrib Sci Nat Hist Mus LA Co 403:1–28

    Google Scholar 

  • Barnes LG (1990) A new Miocene enaliarctine pinniped of the genus Pteronarctos (Mammalia: Otariidae) from the Astoria Formation, Oregon. Contrib Sci Nat Hist Mus LA Co 422:1–20

    Google Scholar 

  • Barnes LG (1992) A new genus and species of middle Miocene enaliarctine pinniped (Mammalia, Carnivora, Otariidae) from the Astoria Formation in coastal Oregon. Contrib Sci Nat Hist Mus LA Co 431:1–27

    Google Scholar 

  • Barnes LG (2008) Otarioidea. In: Janis CM, Gunnell GF, Uhen MD (eds) Evolution of Tertiary Mammals of North America, Volume 2: Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, New York, pp 523–541

    Google Scholar 

  • Barnes LG, Hirota K (1994) Miocene pinnipeds of the otariid subfamily Allodesminae in the North Pacific Ocean: systematics and relationships. Isl Arc 3:329–360 doi:10.1111/j.1440-1738.1994.tb00119.x

    Article  Google Scholar 

  • Barnes LG, Raschke RE (1991) Gomphotaria pugnax, a new genus and species of late Miocene dusignathine otariid pinniped (Mammalia: Carnivora) from California. Contrib Sci Nat Hist Mus LA Co 426:1–16

    Google Scholar 

  • Berta A (1991) New Enaliarctos (Pinnipedimorpha) from the Oligocene and Miocene of Oregon and the role of “enaliarctids” in pinniped phylogeny. Smithson Contrib Paleobiol 69:1–33

    Google Scholar 

  • Berta A (1994) A new species of phocoid pinniped Pinnarctidion from the early Miocene of Oregon. J Vertebr Paleontol 14:405–413

    Google Scholar 

  • Berta A, Adam PJ (2001) Evolutionary biology of pinnipeds. In: Mazin J-M, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr Friedrich Pfeil, München, pp 235–260

    Google Scholar 

  • Berta A, Ray CE (1990) Skeletal morphology and locomotor capabilities of the archaic pinniped Enaliarctos mealsi. J Vertebr Paleontol 10:141–157

    Google Scholar 

  • Berta A, Ray CE, Wyss AR (1989) Skeleton of the oldest known pinniped, Enaliarctos mealsi. Science 244:60–62 doi:10.1126/science.244.4900.60

    Article  PubMed  Google Scholar 

  • Berta A, Sumich JL, Kovacs KM (2006) Marine Mammals: Evolutionary Biology. Academic, San Diego

    Google Scholar 

  • Berta A, Wyss AR (1994) Pinniped phylogeny. Proc San Diego Soc Nat Hist 29:33–56

    Google Scholar 

  • Buchholtz EA (1998) Implications of vertebral morphology for locomotor evolution in early Cetacea. In: Thewissen JGM (ed) The Emergence of Whales: Evolutionary Patterns in the Origin of Cetacea. Plenum, New York, pp 325–351

    Google Scholar 

  • Campbell NA, Atchley WR (1981) The geometry of canonical variate analysis. Syst Zool 30:268–280 doi:10.2307/2413249

    Article  Google Scholar 

  • Dagg AI, Windsor DE (1972) Swimming in northern terrestrial mammals. Can J Zool 50:117–130 doi:10.1139/z72-019

    Article  Google Scholar 

  • Davis CS, Delisle I, Stirling I, Siniff DB, Strobeck C (2004) A phylogeny of the extant Phocidae inferred from complete mitochondrial DNA coding regions. Mol Phylogenet Evol 33:363–377 doi:10.1016/j.ympev.2004.06.006

    Article  PubMed  CAS  Google Scholar 

  • Delisle I, Strobeck C (2005) A phylogeny of the Caniformia (Order Carnivora) based on 12 complete protein-coding mitochondrial genes. Mol Phylogenet Evol 37:192–201 doi:10.1016/j.ympev.2005.04.025

    Article  PubMed  CAS  Google Scholar 

  • Deméré TA (1994) The family Odobenidae: a phylogenetic analysis of fossil and living taxa. Proc San Diego Soc Nat Hist 29:99–123

    Google Scholar 

  • Deméré TA, Berta A (2002) The Miocene pinniped Desmatophoca oregonensis Condon, 1906 (Mammalia: Carnivora), from the Astoria Formation, Oregon. Smithson Contrib Paleobiol 93:113–147

    Google Scholar 

  • Deméré TA, Berta A, Adam PJ (2003) Pinnipedimorph evolutionary biogeography. Bull Am Mus Nat Hist 279:32–76 doi:10.1206/0003-0090(2003)279<0032:C>2.0.CO;2

    Article  Google Scholar 

  • English AW (1976a) Functional anatomy of the hands of fur seals and sea lions. Am J Anat 147:1–18 doi:10.1002/aja.1001470102

    Article  PubMed  CAS  Google Scholar 

  • English AW (1976b) Limb movements and locomotor function in the California sea lion (Zalophus californianus). J Zool 178:341–364

    Google Scholar 

  • English AW (1977) Structural correlates of forelimb function in fur seals and sea lions. J Morphol 151:325–352 doi:10.1002/jmor.1051510303

    Article  PubMed  CAS  Google Scholar 

  • Feldkamp SD (1987a) Foreflipper propulsion in the California sea lion, Zalophus californianus. J Zool (Lond) 212:43–57

    Google Scholar 

  • Feldkamp SD (1987b) Swimming in the California sea lion: morphometrics, drag, and energetics. J Exp Biol 131:117–135

    PubMed  CAS  Google Scholar 

  • Finarelli JA (2008) A total evidence phylogeny of the Arctoidea (Carnivora: Mammalia): relationships among basal taxa. J Mammal Evol (published online early)doi:10.1007/s10914-008-9074-x

  • Fish FE (1992) Aquatic locomotion. In: Tomasi TE, Horton TH (eds) Mammalian Energetics: Interdisciplinary Views of Metabolism and Reproduction. Cornell University Press, Ithaca, pp 34–63

    Google Scholar 

  • Fish FE (1993) Comparison of swimming kinematics between terrestrial and semiaquatic opossums. J Mammal 74:275–284 doi:10.2307/1382382

    Article  Google Scholar 

  • Fish FE (1994) Association of propulsive swimming mode with behavior in river otters (Lutra canadensis). J Mammal 75:989–997 doi:10.2307/1382481

    Article  Google Scholar 

  • Fish FE (1996) Transitions from drag-based to lift-based propulsion in mammalian swimming. Am Zool 36:628–641

    Google Scholar 

  • Fish FE (2000) Biomechanics and energetics in aquatic and semiaquatic mammals: platypus to whale. Physiol Biochem Zool 73:683–698 doi:10.1086/318108

    Article  PubMed  CAS  Google Scholar 

  • Fish FE (2001) A mechanism for evolutionary transition in swimming mode by mammals. In: Mazin J-M, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr Friedrich Pfeil, München, pp 261–287

    Google Scholar 

  • Fish FE, Innes S, Ronald K (1988) Kinematics and estimated thrust production of swimming harp and ringed seals. J Exp Biol 137:157–173

    PubMed  CAS  Google Scholar 

  • Flyger V, Townsend MR (1968) The migration of polar bears. Sci Am 218:108–116

    Article  Google Scholar 

  • Flynn JJ, Finarelli JA, Zehr S, Hsu J, Nedbal MA (2005) Molecular phylogeny of the Carnivora (Mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Syst Biol 54:317–337 doi:10.1080/10635150590923326

    Article  PubMed  Google Scholar 

  • Flynn JJ, Nedbal MA (1998) Phylogeny of the Carnivora (Mammalia): convergence vs incompatibility among multiple data sets. Mol Phylogenet Evol 9:414–426 doi:10.1006/mpev.1998.0504

    Article  PubMed  CAS  Google Scholar 

  • Flynn JJ, Nedbal MA, Dragoo JW, Honeycutt RL (2000) Whence the red panda? Mol Phylogenet Evol 17:190–199 doi:10.1006/mpev.2000.0819

    Article  PubMed  CAS  Google Scholar 

  • Flynn JJ, Neff NA, Tedford RH (1988) Phylogeny of the Carnivora. In: Benton MJ (ed) The Phylogeny and Classification of the Tetrapods, Volume 2. Clarendon, Oxford, pp 73–116

    Google Scholar 

  • Flynn JJ, Wesley-Hunt GD (2005) Carnivora. In: Rose KD, Archibald JD (eds) The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades. Johns Hopkins University Press, Baltimore, pp 175–198

    Google Scholar 

  • Fulton TL, Strobeck C (2006) Molecular phylogeny of the Arctoidea (Carnivora): effect of missing data on supertree and supermatrix analyses of multiple gene data sets. Mol Phylogenet Evol 41:165–181 doi:10.1016/j.ympev.2006.05.025

    Article  PubMed  CAS  Google Scholar 

  • Giffin EB (1992) Functional implications of neural canal anatomy in recent and fossil marine carnivores. J Morphol 214:357–374 doi:10.1002/jmor.1052140311

    Article  PubMed  CAS  Google Scholar 

  • Gingerich PD (2003) Land-to-sea transition in early whales: evolution of Eocene Archaeoceti (Cetacea) in relation to skeletal proportions and locomotion of living semiaquatic mammals. Paleobiol 29:429–454 doi:10.1666/0094-8373(2003)029<0429:LTIEWE>2.0.CO;2

    Article  Google Scholar 

  • Gingerich PD (2005) Aquatic adaptation and swimming mode inferred from skeletal proportions in the Miocene desmostylian Desmostylus. J Mamm Evol 12:183–194 doi:10.1007/s10914-005-5719-1

    Article  Google Scholar 

  • Gordon KR (1981) Locomotor behaviour of the walrus (Odobenus). J Zool 195:349–367

    Article  Google Scholar 

  • King JE (1966) Relationships of the hooded and elephant seals (genera Cystophora and Mirounga). J Zool (London) 148:385–398

    Google Scholar 

  • King JE (1983) Seals of the World. Cornell University Press, Ithaca

    Google Scholar 

  • Koretsky IA, Barnes LG (2008) Phocidae. In: Janis CM, Gunnell GF, Uhen MD (eds) Evolution of Tertiary Mammals of North America, Volume 2: Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, New York, pp 542–556

    Google Scholar 

  • Ledje C, Árnason Ú (1996a) Phylogenetic analyses of complete cytochrome b genes of the order Carnivora with particular emphasis on the Caniformia. J Mol Evol 42:135–144 doi:10.1007/BF02198839

    Article  PubMed  CAS  Google Scholar 

  • Ledje C, Árnason Ú (1996b) Phylogenetic relationships within caniform carnivores based on analyses of the mitochondrial 12S rRNA gene. J Mol Evol 43:641–649 doi:10.1007/BF02202112

    Article  PubMed  CAS  Google Scholar 

  • Lento GM, Hickson RE, Chambers GK, Penny D (1995) Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol 12:28–52

    PubMed  CAS  Google Scholar 

  • Mazin J-M, Buffrénil V de (eds) (2001) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr Friedrich Pfeil, München

  • McLaren IA (1960) Are the Pinnipedia biphyletic? Syst Zool 9:18–28 doi:10.2307/2411537

    Article  Google Scholar 

  • Mitchell ED (1966) The Miocene pinniped Allodesmus. Univ Calif Publ Geol Sci 61:1–105

    Google Scholar 

  • Mitchell ED (1968) The Mio-Pliocene pinniped Imagotaria. J Fish Res Bd Can 25:1843–1900

    Google Scholar 

  • Mitchell ED (1975) Parallelism and convergence in the evolution of Otariidae and Phocidae. Rapp P V Reun Cons Int Explor Mer 169:12–26

    Google Scholar 

  • Miyazaki S, Horikawa H, Kohno N, Hirota K, Kimura M, Hasegawa Y et al (1994) Summary of the fossil record of pinnipeds in Japan, and comparisons with that from the eastern North Pacific. Isl Arc 3:361–372 doi:10.1111/j.1440-1738.1994.tb00120.x

    Article  Google Scholar 

  • Muizon C de (1981) Les Vertébrés fossiles de la Formation Pisco (Pérou). Première partie. Deux nouveaux Monachinae (Phocidae, Mammalia) du Pliocène de Sud-Sacaco. Trav Inst Fran Etud Andines 22:1–160

    Google Scholar 

  • Repenning CA, Tedford RH (1977) Otarioid seals of the Neogene. US Geol Surv Prof Pap 992:1–93

    Google Scholar 

  • Rose KD, Koenigswald Wv (2005) An exceptionally complete skeleton of Palaeosinopa (Mammalia, Cimolesta, Pantolestidae) from the Green River Formation, and other postcranial elements of the Pantolestidae from the Eocene of Wyoming (USA). Palaeontogr Abt A 273:55–96

    Google Scholar 

  • Sarich VM (1969) Pinniped phylogeny. Syst Zool 18:416–422 doi:10.2307/2412185

    Article  PubMed  CAS  Google Scholar 

  • Sato JJ, Wolsan M, Suzuki H, Hosoda T, Yamaguchi Y, Hiyama K et al (2006) Evidence from nuclear DNA sequences sheds light on the phylogenetic relationships of Pinnipedia: single origin with affinity to Musteloidea. Zoolog Sci 23:125–146 doi:10.2108/zsj.23.125

    Article  PubMed  CAS  Google Scholar 

  • Smith FA, Lyons SK, Morgan Ernest SK, Jones KE, Kaufman DM, Dayan T et al (2003) Body mass of late Quaternary mammals. Ecology 84:3403 doi:10.1890/02-9003

    Article  Google Scholar 

  • Tarasoff FJ, Bisaillon A, Piérard J, Whitt AP (1972) Locomotory patterns and external morphology of the river otter, sea otter, and harp seal (Mammalia). Can J Zool 50:915–929 doi:10.1139/z72-124

    Article  PubMed  CAS  Google Scholar 

  • Tedford RH (1976) Relationship of pinnipeds to other carnivores (Mammalia). Syst Zool 25:363–374 doi:10.2307/2412511

    Article  Google Scholar 

  • Thewissen JGM, Taylor MA (2007) Aquatic adaptations in the limbs of amniotes. In: Hall BK (ed) Fins into Limbs: Evolution, Development, and Transformation. University of Chicago Press, Chicago, pp 310–322

    Google Scholar 

  • Uhen MD (2007) Evolution of marine mammals: back to sea after 300 million years. Anat Rec 290:514–522 doi:10.1002/ar.20545

    Article  Google Scholar 

  • Vrana PB, Milinkovitch MC, Powell JR, Wheeler WC (1994) Higher level relationships of arctoid Carnivora based on sequence data and ‘total evidence’. Mol Phylogenet Evol 3:47–58 doi:10.1006/mpev.1994.1006

    Article  PubMed  CAS  Google Scholar 

  • Williams TM (1983) Locomotion in the North American mink, a semi-aquatic mammal. I. Swimming energetics and body drag. J Exp Biol 103:155–168

    PubMed  CAS  Google Scholar 

  • Wyss AR (1987) The walrus auditory region and the monophyly of pinnipeds. Am Mus Novitates 2871:1–31

    Google Scholar 

  • Wyss AR (1988a) Evidence from flipper structure for a single origin of pinnipeds. Nature 334:427–428 doi:10.1038/334427a0

    Article  Google Scholar 

  • Wyss AR (1988b) On “retrogression” in the evolution of the Phocinae and phylogenetic affinities of the monk seals. Am Mus Novitates 2924:1–38

    Google Scholar 

  • Wyss AR (1989) Flippers and pinniped phylogeny: has the problem of convergence been overrated? Mar Mamm Sci 5:343–360 doi:10.1111/j.1748-7692.1989.tb00347.x

    Article  Google Scholar 

  • Wyss AR, Flynn JJ (1993) A phylogenetic analysis and definition of Carnivora. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Placentals. Springer, New York, pp 32–52

    Google Scholar 

  • Yu L, Li Q-W, Ryder OA, Zhang Y-P (2004) Phylogenetic relationships within mammalian order Carnivora indicated by sequences of two nuclear DNA genes. Mol Phylogenet Evol 33:694–705 doi:10.1016/j.ympev.2004.08.001

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Zhang Y-P (2006) Phylogeny of the caniform Carnivora: evidence from multiple genes. Genetica 127:65–79 doi:10.1007/s10709-005-2482-4

    Article  PubMed  CAS  Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric Morphometrics for Biologists: A Primer. Elsevier Academic, San Diego

    Google Scholar 

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Acknowledgments

I thank E Westwig at the American Museum of Natural History, New York, NY, USA, and JF Jacobs at the National Museum of Natural History, Washington, DC, USA, for providing access to the modern pinniped skeletons added to this study. DJ Bohaska at the National Museum of Natural History, Washington, DC, USA, and LG Barnes and HW Thomas at the Natural History Museum of Los Angeles County, Los Angeles, CA, USA, provided additional information and measurements of the Enaliarctos and Allodesmus specimens in their care. B Miljour helped with preparation of Fig. 2. PD Gingerich, AR Wood, JA Finarelli, and two anonymous reviewers provided feedback on earlier versions of this manuscript that improved it greatly.

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  1. Department of Ecology and Evolutionary Biology and Museum of Paleontology, University of Michigan, Ann Arbor, MI, 48109-1079, USA

    Ryan M. Bebej

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Bebej, R.M. Swimming Mode Inferred from Skeletal Proportions in the Fossil Pinnipeds Enaliarctos and Allodesmus (Mammalia, Carnivora). J Mammal Evol 16, 77–97 (2009). https://doi.org/10.1007/s10914-008-9099-1

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