title: The evolution of bat vestibular systems in the face of potential antagonistic selection pressures for flight and echolocation.
abstract: The vestibular system maintains the body's sense of balance and, therefore, was probably subject to strong selection during evolutionary transitions in locomotion. Among mammals, bats possess unique traits that place unusual demands on their vestibular systems. First, bats are capable of powered flight, which in birds is associated with enlarged semicircular canals. Second, many bats have enlarged cochleae associated with echolocation, and both cochleae and semicircular canals share a space within the petrosal bone. To determine how bat vestibular systems have evolved in the face of these pressures, we used micro-CT scans to compare canal morphology across species with contrasting flight and echolocation capabilities. We found no increase in canal radius in bats associated with the acquisition of powered flight, but canal radius did correlate with body mass in bat species from the suborder Yangochiroptera, and also in non-echolocating Old World fruit bats from the suborder Yinpterochiroptera. No such trend was seen in members of the Yinpterochiroptera that use laryngeal echolocation, although canal radius was associated with wing-tip roundedness in this group. We also found that the vestibular system scaled with cochlea size, although the relationship differed in species that use constant frequency echolocation. Across all bats, the shape of the anterior and lateral canals was associated with large cochlea size and small body size respectively, suggesting differential spatial constraints on each canal depending on its orientation within the skull. Thus in many echolocating bats, it seems that the combination of small body size and enlarged cochlea together act as a principal force on the vestibular system. The two main groups of echolocating bats displayed different canal morphologies, in terms of size and shape in relation to body mass and cochlear size, thus suggesting independent evolutionary pathways and offering tentative support for multiple acquisitions of echolocation.
authors: School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom. kalinadavies@gmail.com
authors: Kalina T J
authors: KT
authors: Davies
authors: Paul J J
authors: PJ
authors: Bates
authors: Ibnu
authors: I
authors: Maryanto
authors: James A
authors: JA
authors: Cotton
authors: Stephen J
authors: SJ
authors: Rossiter
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002685:Chiroptera / Q000033:anatomy & histology* / Q000145:classification / Q000502:physiology*; D003051:Cochlea / Q000033:anatomy & histology; D045303:Cytochromes b / Q000235:genetics; D007758:Ear, Inner / Q000033:anatomy & histology* / Q000000981:diagnostic imaging; D004455:Echolocation / Q000502:physiology*; D010802:Phylogeny; D011859:Radiography; D012641:Selection, Genetic; D012665:Semicircular Canals / Q000033:anatomy & histology; D014921:Wings, Animal / Q000033:anatomy & histology
chemical_list: D045303:Cytochromes b
references: J Anat. 2010 Jan;216(1):37-47
references: 20002227
references: Nature. 2002 May 9;417(6885):163-6
references: 12000957
references: Integr Comp Biol. 2002 Feb;42(1):141-8
references: 21708703
references: PLoS Biol. 2006 May;4(5):e88
references: 16683862
references: Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9929-34
references: 16785431
references: BMC Evol Biol. 2007 Nov 08;7:214
references: 17996036
references: Proc Biol Sci. 2012 Oct 7;279(1744):3932-9
references: 22859594
references: Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):17914-9
references: 23045679
references: J Theor Biol. 1999 Jun 7;198(3):405-37
references: 10366494
references: J Anat. 2010 May;216(5):600-10
references: 20525088
references: J Anat. 2004 Feb;204(2):71-92
references: 15032915
references: Nature. 2010 Aug 19;466(7309):E8; discussion E9
references: 20724993
references: J Exp Biol. 2009 Apr;212(Pt 7):945-53
references: 19282491
references: Trends Ecol Evol. 2004 Aug;19(8):430-8
references: 16701301
references: Trends Ecol Evol. 1997 Feb;12(2):53-8
references: 21237972
references: Science. 2005 Jan 28;307(5709):580-4
references: 15681385
references: Nature. 2003 Oct 30;425(6961):950-3
references: 14586467
references: Trends Ecol Evol. 2006 Mar;21(3):149-56
references: 16701491
references: Hear Res. 1995 May;85(1-2):18-30
references: 7559173
references: J Morphol. 1995 Jun;224(3):303-11
references: 7595956
references: Bioinformatics. 2007 Nov 1;23(21):2947-8
references: 17846036
references: Nature. 2010 Feb 18;463(7283):939-42
references: 20098413
references: Nature. 2003 Mar 27;422(6930):421-4
references: 12660781
references: J Exp Biol. 2005 Apr;208(Pt 7):1309-19
references: 15781891
references: Mol Biol Evol. 2007 Jan;24(1):26-53
references: 17047029
references: J Neurophysiol. 2007 Dec;98(6):3197-205
references: 17913986
references: Heredity (Edinb). 2012 May;108(5):480-9
references: 22167055
references: J Anat. 2012 Jun;220(6):529-43
references: 22404255
references: J Comp Neurol. 1980 Aug 15;192(4):883-902
references: 6968325
references: J Anat. 2010 Mar;216(3):368-80
references: 20039977
references: J Anat. 2010 Apr;216(4):496-509
references: 20210819
references: Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1431-6
references: 11805285
references: Mol Biol Evol. 2005 Sep;22(9):1869-86
references: 15930153
references: J Exp Biol. 2006 May;209(Pt 9):1725-36
references: 16621953
references: Oecologia. 2000 Aug;124(3):332-342
references: 28308770
references: J Vestib Res. 2004;14(1):17-32
references: 15156093
references: J Hum Evol. 2008 Aug;55(2):326-39
references: 18395770
references: Proc R Soc Lond B Biol Sci. 1963 Mar 26;157:403-19
references: 14041997
references: Nature. 2008 Feb 14;451(7180):818-21
references: 18270539
references: Science. 2011 Oct 28;334(6055):521-4
references: 21940861
references: Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):10808-12
references: 17576932
references: J Exp Biol. 1970 Oct;53(2):501-14
references: 5481668
references: Am J Phys Anthropol. 1998;Suppl 27:211-51
references: 9881527
references: J Comp Neurol. 2001 Oct 1;438(4):433-44
references: 11559899
references: J Morphol. 1993 Oct;218(1):85-98
references: 8230237
references: Proc Biol Sci. 2008 May 22;275(1639):1203-8
references: 18285282
references: Nature. 2003 Jul 10;424(6945):187-91
references: 12853955
references: J Anat. 2008 Nov;213(5):583-96
references: 19014365
references: J Anat. 2009 Oct;215(4):444-51
references: 19619167
references: Genome Res. 2007 Apr;17(4):413-21
references: 17322288
references: Science. 2006 Jan 6;311(5757):73-7
references: 16400146
references: Comp Biochem Physiol A Mol Integr Physiol. 1999 Jun;123(2):173-8
references: 10425737
references: Nature. 2004 Jun 10;429(6992):654-7
references: 15190351
references: Syst Biol. 2012 Jan;61(1):150-64
references: 21900649