The naked ape as an evolutionary model, 50 years later

in Animal Biology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Abstract

Evolution acts through a combination of four different drivers: (1) mutation, (2) selection, (3) genetic drift, and (4) developmental constraints. There is a tendency among some biologists to frame evolution as the sole result of natural selection, and this tendency is reinforced by many popular texts. “The Naked Ape” by Desmond Morris, published 50 years ago, is no exception. In this paper I argue that evolutionary biology is much richer than natural selection alone. I illustrate this by reconstructing the evolutionary history of five different organs of the human body: foot, pelvis, scrotum, hand and brain. Factors like developmental tinkering, by-product evolution, exaptation and heterochrony are powerful forces for body-plan innovations and the appearance of such innovations in human ancestors does not always require an adaptive explanation. While Morris explained the lack of body hair in the human species by sexual selection, I argue that molecular tinkering of regulatory genes expressed in the brain, followed by positive selection for neotenic features, may have been the driving factor, with loss of body hair as a secondary consequence.

The naked ape as an evolutionary model, 50 years later

in Animal Biology

Sections

References

AielloL. & DeanC. (2006) An Introduction to Human Evolutionary Anatomy. Elsevier Scientific PressAmsterdam, Netherlands.

AlmécijaS.WallaceI.J.JudeaS.AlbaD.M. & Moyà-SolàS. (2015) Human Evolution. Comment on “Human-like hand use in Australopithecus africanus. Science348(6239) 1101.

BennettM.R.HarrisJ.W.K.RichmondB.G.BraunD.R.MbuaE.KiuraP.OlagoD.KibunjiaM.OmuomboC.BehrensmeyerA.K.HuddartD. & GonzalezS. (2009) Early hominin foot morphology based on 1.5-million-year-old footprints from Ileret, Kenya. Science323(5918) 1197-1201.

CharrierC.JoshiK.Coutinho-BuddJ.KimJ.-E.LambertN.De MarchenaJ.JinW.-J.VanderhaeghenP.GhoshA.SassaT. & PolleuxF. (2012) Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine formation. Cell149923-935.

D’AoûtK. & AertsP. (2008) The evolutionary history of the human foot. In: K. D’AoûtK. LescrenierB. Van Geluwhe & D. De Clercq (Eds) Advances in Plantar Pressure Measurements in Clinical and Scientific Research pp. 44-68. Shaker Publishing BVMaastricht, Netherlands.

DavisJ.M.SearlesV.B.AndersonN.KeeneyJ.RaznahanA.HorwoodL.J.FergussonD.M.KennedyM.A.GieddJ. & SikelaJ.M. (2015) DUF1220 copy number is linearly associated with increased cognitive function as measured by total IQ and mathematical aptitude scores. Hum. Genet.13467-75.

DennisM.Y.NuttleX.SudmantP.H.AntonacciF.GravesT.A.NefedovM.RosenfieldJ.A.SajjadianS.MaligM.KotkiewiczH.CurryC.J.ShaferS.ShafferL.G.De JongP.J.WilsonR.K. & EichlerE.E. (2012) Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell149912-922.

DeSilvaJ.M.HoltK.G.ChurchillS.E.CarlsonK.J.WalkerC.S.ZipfelB. & BergerL.R. (2013) The lower limb and mechanics of walking in Australopithecus sediba. Science340(6129) 163-165.

FranklinA.BevisL.LingY. & HurlbertA. (2009) Biological components of colour preference in infancy. Dev. Sci.13346-354.

GiladY.OshlackA.SmythG.K.SpeedT.P. & WhiteK.P. (2006) Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature440(7081) 242-245.

GoffmanE. (1956) The Presentation of Self in Everyday Life. Monograph No. 2. University of Edinburgh Social Science Research CentreEdinburgh, UK.

GouldS.J. & LewontinR.C. (1979) The spandrels of San Marco and the panglossian paradigm. Proc. R. Soc. Lond. B Biol. Sci.205581-598.

GouldS.J. & VrbaE.S. (1982) Exaptation – a missing term in the science of form. Paleobiology84-15.

GrussL.T. & SchmittD. (2015) The evolution of the human pelvis: changing adaptations to bipedalism, obstetrics and thermoregulation. Phil. Trans. R. Soc. Lond. B Biol. Sci.37020140063.

Harcourt-SmithW.E.H. & AielloL.C. (2004) Fossils, feet and the evolution of human bipedal locomotion. J. Anat.204403-416.

HarmandS.LewisJ.E.FeibelC.S.LepreC.J.PratS.LenobleA.BoësX.QuinnR.L.BrenetM.ArroyoA.TaylorN.ClémentS.DaverG.BrugalJ.P.LeakeyL.MortlockR.A.WrightJ.D.LokorodiS.KirwaC.KentD.V. & RocheH. (2015) 3.3-million-year-old stone tools from Lomekwi 3, West Turkana, Kenya. Nature521(7552) 310-315.

HurlbertA. & LingY. (2007) Biological components of sex differences in color preference. Curr. Biol.17R623-R625.

JacobF. (1977) Evolution and tinkering. Science196(4295) 1161-1166.

JacobF. (1981) Le jeu des possibles. Essai sur la diversité du vivant. Librairie Arthème FayardParis, France.

KeeneyJ.G.DumasL. & SikelaJ.M. (2014) The case for DUF1220 domain dosage as a primary contributor to anthropoid brain expansion. Front. Hum. Neurosci.8427.

KeeneyJ.G.DavisJ.M.SiegenthalerJ.PostM.D.NielsenB.S.HopkinsW.D. & SikelaJ.M. (2015) DUF1220 protein domains drive proliferation in human neural stem cells and are associated with increased cortical volume in anthropoid primates. Brain Struct. Funct.2203053-3060.

KivellT.L.KibiiJ.M.ChurchillS.E.SchmidP. & BergerL.R. (2011) Australopithecus sediba hand demonstrates mosaic evolution of locomotor and manipulative abilities. Science333(6048) 1411-1417.

KleisnerK.IvellR. & FlegrJ. (2010) The evolutionary history of testicular externalization and the origin of the scrotum. J. Biosci.3527-37.

KooninE.V. (2017) Splendor and misery of adaptation, or the importance of neutral null for understanding evolution. BMC Biol.14114.

Linde-MedinaM. (2011) Adaptation or exaptation? The case of the human hand. J. Biosci.36575-585.

LovejoyC.O.LatimerB.SuwaG.AsfawB. & WhiteT.D. (2009) Combining prehension and propulsion: the foot of Ardipithecus ramidus. Science326(5949) 72e1-8.

LynchM. (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. Proc. Natl. Acad. Sci. USA104(Suppl. 1) 8597-8604.

McPherronS.P.AlemsegedZ.MareanC.W.WynnJ.G.ReedD.GeraadsD.BobeR. & BéaratH.A. (2010) Evidence for stone-tool assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature466(7308) 857-860.

Minugh-PurvisN. & McNamaraK.J. (Eds) (2002) Human Evolution Through Developmental Change. The Johns Hopkins University PressBaltimore, MD, USA.

MorrisD. (1967) The Naked Ape. A Zoologist Study of the Human Animal. Vintage BooksLondon, UK.

O’BlenessM.S.DickensC.M.DumasL.J.Kehrer-SawatzkiH.G.WyckoffJ. & SikelaJ.M. (2012) Evolutionary history and genome organization of DUF1220 protein domains. G3 (Bethesda)2977-986.

PigliucciM. & KaplanJ. (2000) The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later. Trends Ecol. Evol.1566-70.

Ponce de LeónM.S.GolovanovaL.DoronichevV.RomanovaG.AkazawaT.KondoO.IshidaH. & ZollikoferP.E. (2008) Neanderthal brain size at birth provides insights into the evolution of human life history. Proc. Natl. Acad. Sci. USA10513764-13768.

PontzerH.CampbellR.RightmireG.P.JashashviliT.Ponce de LeónM.S.LordkipanidzeD. & ZollikoferC.P.E. (2010) Locomotor anatomy and biomechanics of the Dmanisi hominins. J. Hum. Evol.58492-504.

PortmannA. (1969) Einführung in die vergleichende Morphologie der Wirbeltiere. Vierte überarbeitete und ergänzte Auflage. Schwabe & Co VerlagBasel, Switserland/Stuttgart, Germany.

PrauseN.ParkJ.LeungS. & MillerG. (2015) Women’s preferences for penis size: a new research method using selection among 3D models. PLoS One10133079.

ReidR.G.B. (2007) Biological Emergences. Evolution by Natural Experiment. MIT PressCambridge, MA, USA.

RobertsA. (2014) The Incredible Unlikeliness of Being. Evolution and the Making of Us. Heron BooksLondon, UK.

SimpsonS.W.QuadeJ.LevinN.E.ButlerR.Dupont-NivetG.EverettM. & SemawS. (2008) A female Homo erectus pelvis from Gona, Ethiopia. Science322(5904) 1089-1092.

SkinnerM.M.StephensN.B.TsegaiZ.J.FooteA.C.NguyenN.H.GrossT.PahrD.H.HublinJ.-J. & KivellT.L. (2015) Human evolution. Human-like hand use in Australopithecus africanus. Science347(6220) 395-399.

TocheriM.W.OrrC.M.JacofskyM.C. & MarzkeM.W. (2008) The evolutionary history of the hominin hand since the last common ancestor of Pan and Homo. J. Anat.212544-562.

TocheriM.W.SolhanC.R.OrrC.M.FemianiJ.FrohlichB.GrovesC.P.Harcourt-SmithW.E.RichmondB.G.ShoelsonB. & JungersW.L. (2011) Ecological divergence and medial cuneiform morphology in gorillas. J. Hum. Evol.60171-184.

WhiteT.D.AsfawB.BeyeneY.Haile-SelassieY.LovejoyC.O.SuwaG. & WoldeGabrielG. (2009) Ardipithecus ramidus and the paleobiology of early hominids. Science326(5949) 75-86.

WoodB. (2014) Fifty years after Homo habilis. Nature50831-33.

ZimmerF. & MontgomeryS.H. (2015) Phylogenetic analysis supports a link between DUF1220 domain number and primate brain expansion. Genome Biol. Evol.72083-2088.

Figures

  • View in gallery

    Four different driving processes influence the process of evolution. These drivers are not equally important in every evolutionary change, but all four have to be taken into account, as well as their interactions, in evolutionary explanation.

  • View in gallery

    Estimates of hallux abduction (A) from fossil footprints (B) at Laetoli (Tanzania) and Ileret (Kenia), compared with modern human footprints from the Holocene and recent times. G133 (Laetoli, 3.7 million years old) is ascribed to Australopithecus afarensis. GAJi10 and FwJj14 (Ileret, 1.5 million years old) are ascribed to Homo erectus. From Bennett, M.R. et al. (2009) Early hominin foot morphology based on 1.5-million-year-old footprints from Ileret, Kenia. Science, 323, 1179-1201. Reprinted with permission from AAAS.

  • View in gallery

    Illustration of the profound changes of the pelvis during hominin evolution, using three landmark species, Australopithecus afarensis (3.5 million years old), Homo erectus (1.5 million years old) and Homo heidelbergensis (600 000 years old). Reproduced with permission from the Royal Society from L.T. Gruss & D. Schmit (2015) The evolution of the human pelvis: Changing adaptations to bipedalism, obstetrics and thermoregulation. Philosophical Transactions B, 370, 20140063.

  • View in gallery

    Position of the testis in a number of vertebrates. The descent of testicles in a scrotum observed in several species of mammals including Homo sapiens is part of a trend of compaction and caudal migration that already started in the fish. Reproduced with modifications from A. Portmann (1969) Einführung in die vergleichende Morphologie der Wirbeltiere. Vierte überarbeitete und ergänzte Auflage, Schwabe & Co Verlag, Basel/Stuttgart. The human image is from the Pioneer 10 plaquette, launched 1972, with testicles marked in black.

  • View in gallery

    Simplified timeline of hand morphologies and manipulative capacities in the hominoid-hominin evolutionary lineage. The figure illustrates that human-like hand use predated the systematic use of stone tools by many millions of years. From Almécija, S. et al. (2015) Comment on “Human-like hand use in Australopithecus africanus”, Science 348, 1101-a. Reprinted with permission from AAAS.

  • View in gallery

    Reconstruction of the evolutionary changes leading to extreme DUF1220 domain amplification in vertebrates (A) and in detail after the chimpanzee-human split (B). The number of domains in various groups is indicated on the right. DUF1220 appeared first in primitive mammals after a partial duplication from PDE4DIP (Phosphodiesterase 4D Interacting Protein). The new domain became part of the NBPF genes (Neuroblastoma Breakpoint Family) and after various rearrangements came under control of core mammalian promoter, CM, and an unrelated promotor from the EVI5 gene (Ecotopic Viral Integration Site 5). The rate of duplication increased after the formation of a human-lineage specific (HLS) triplet formation and insertion of HERV(K) (Human Endogenous Retrovirus K). Reproduced under Creative Commons Licence from O’Bleness, M.S. et al. (2012) Evolutionary history and genome organization of DUF1220 protein domains. G3 Genes|Genomes|Genetics 2, 977-986, with permission from the authors.

  • View in gallery

    Overview of evolutionary processes and principles illustrated by five different organs of the human body discussed in this paper. The various processes do not exclude each other, but are shown to illustrate which factor has been the main driver determining the direction of change.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 32 32 23
Full Text Views 8 8 7
PDF Downloads 4 4 3
EPUB Downloads 1 1 0