title: Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull.
abstract: BACKGROUND
  Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity.
  
  
  RESULTS
  Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm.
  
  
  CONCLUSIONS
  The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.
authors: Center for Functional Anatomy and Evolution, Johns Hopkins University, Baltimore, MD, USA. Katrina.jones30@gmail.com.|Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA. Katrina.jones30@gmail.com.
authors: Katrina E
authors: KE
authors: Jones
authors: Department of Anthropology, Stony Brook University, Stony Brook, New York, NY, 11794-4364, USA. jeroen.smaers@stonybrook.edu.
authors: Jeroen B
authors: JB
authors: Smaers
authors: Department of Genetics, Evolution & Environment, University College London, Gower Street, London, WC1E 6BT, UK. a.goswami@ucl.ac.uk.|Department of Earth Sciences, University College London, Gower Street, London, WC1E 6BT, UK. a.goswami@ucl.ac.uk.
authors: Anjali
authors: A
authors: Goswami
mesh_terms: D000818:Animals; D005075:Biological Evolution; D010872:Caniformia / Q000033:anatomy & histology / Q000145:classification / Q000235:genetics; D002335:Carnivora / Q000033:anatomy & histology* / Q000145:classification / Q000235:genetics*; D017753:Ecosystem; D005580:Fossils; D010802:Phylogeny; D012886:Skull / Q000033:anatomy & histology*
references: Nature. 1999 Oct 28;401(6756):877-84
references: 10553904
references: Acta Otolaryngol. 2001 Sep;121(6):689-95
references: 11678167
references: Am J Phys Anthropol. 2003 Feb;120(2):153-70
references: 12541333
references: Science. 2003 Aug 15;301(5635):961-4
references: 12920297
references: Science. 2004 Jan 16;303(5656):356-9
references: 14726588
references: Nat Rev Genet. 2004 Apr;5(4):288-98
references: 15131652
references: Anat Rec A Discov Mol Cell Evol Biol. 2005 Apr;283(2):288-99
references: 15747351
references: Proc Biol Sci. 2005 Mar 22;272(1563):619-25
references: 15817436
references: Syst Biol. 2005 Apr;54(2):317-37
references: 16012099
references: Evolution. 2006 Jan;60(1):169-83
references: 16568641
references: Mol Phylogenet Evol. 2006 Nov;41(2):345-54
references: 16815048
references: Science. 2006 Jul 14;313(5784):224-6
references: 16840700
references: Proc Biol Sci. 2006 Aug 22;273(1597):1987-98
references: 16846905
references: Oecologia. 2006 Nov;150(2):318-29
references: 16865408
references: Am Nat. 2006 Aug;168(2):270-80
references: 16874636
references: Ecology. 2007 Feb;88(2):347-58
references: 17479753
references: Evol Dev. 2007 Nov-Dec;9(6):555-65
references: 17976052
references: J Exp Biol. 2008 Mar;211(Pt 5):699-708
references: 18281332
references: Am Nat. 2002 Aug;160(2):147-57
references: 18707482
references: Evolution. 2008 Dec;62(12):3135-56
references: 18786183
references: Am J Phys Anthropol. 2009 Jun;139(2):193-203
references: 19051256
references: J Anat. 2009 May;214(5):671-8
references: 19438762
references: Am J Phys Anthropol. 1991 Sep;86(1):1-36
references: 1951658
references: Evolution. 2010 Apr 1;64(4):934-43
references: 19895554
references: Mol Phylogenet Evol. 2010 Mar;54(3):726-45
references: 19900567
references: Am Nat. 2010 Mar;175(3):289-301
references: 20095825
references: Mol Phylogenet Evol. 2010 Jul;56(1):49-63
references: 20138220
references: PLoS One. 2010 Mar 03;5(3):e9517
references: 20209089
references: Nature. 2010 Mar 25;464(7288):583-6
references: 20220757
references: Am Nat. 2010 Jun;175(6):623-39
references: 20412015
references: Evolution. 2010 Sep;64(9):2731-45
references: 20455931
references: Evolution. 2010 Aug;64(8):2385-96
references: 20455932
references: Proc Biol Sci. 2010 Oct 22;277(1697):3097-104
references: 20484243
references: J Morphol. 2010 Nov;271(11):1386-98
references: 20799339
references: Proc Biol Sci. 2011 Jun 22;278(1713):1831-9
references: 21106595
references: J Anat. 2011 Mar;218(3):298-310
references: 21198587
references: Mol Ecol Resour. 2011 Mar;11(2):353-7
references: 21429143
references: Integr Comp Biol. 2007 Jul;47(1):147-63
references: 21672827
references: BMC Biol. 2012 Feb 27;10:12
references: 22369503
references: Evolution. 2012 Mar;66(3):752-762
references: 22380438
references: Nature. 2012 Jul 19;487(7407):366-9
references: 22722840
references: Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18006-11
references: 23071335
references: Mol Phylogenet Evol. 2013 Mar;66(3):748-56
references: 23147269
references: Proc Biol Sci. 2013 Jan 7;280(1750):20122244
references: 23173207
references: Anat Rec (Hoboken). 2013 Jul;296(7):1049-63
references: 23653179
references: Philos Trans R Soc Lond B Biol Sci. 2014 Aug 19;369(1649):20130254
references: 25002699
references: Syst Biol. 2014 Nov;63(6):902-18
references: 25077513
references: Evolution. 1970 Sep;24(3):546-559
references: 28562995
references: Evolution. 1997 Oct;51(5):1341-1351
references: 28568616
references: Am Nat. 2004 Dec;164(6):683-695
references: 29641928
references: J Morphol. 1974 May;143(1):21-75
references: 4826105
references: Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6764-71
references: 8041695
references: J Acoust Soc Am. 1998 Apr;103(4):2216-28
references: 9566340
references: Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9402-6
references: 9689092