The naked ape as an evolutionary model, 50 years later

in Animal Biology
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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



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    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.

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    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.

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    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.

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    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.

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    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.

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    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.

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    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.

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