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Phylogenomic Evidence of Adaptive Evolution in the Ancestry of Humans

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Phylogenomic Evidence of Adaptive Evolution in the Ancestry of Humans Phylogenomic evidence of adaptive evolution in the ancestry of humans Morris Goodmana,b,1 and Kirstin N. Sternera aCenter for Molecular Medicine and Genetics and bDepartment of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit, MI 48201 In Charles Darwin’s tree model for life’s evolution, natural selection nomic studies of human evolution. We then highlight the concepts adaptively modifies newly arisen species as they branch apart from that motivate our own efforts and discuss how phylogenomic evi- their common ancestor. In accord with this Darwinian concept, the dence has enhanced our understanding of adaptive evolution in the phylogenomic approach to elucidating adaptive evolution in genes ancestry of modern humans. and genomes in the ancestry of modern humans requires a well supported and well sampled phylogeny that accurately places Darwin’s Views humans and other primates and mammals with respect to one In The Descent of Man, and Selection in Relation to Sex (5), Charles another. For more than a century, first from the comparative immu- Darwin suggested that Africa was the birthplace for humankind. nological work of Nuttall on blood sera and now from comparative The following five passages encapsulate for us Darwin’s thinking genomic studies, molecular findings have demonstrated the close about the place of humans in primate phylogeny and about the kinship of humans to chimpanzees. The close genetic correspond- uniqueness of modern humans. ence of chimpanzees to humans and the relative shortness of our evolutionary separation suggest that most distinctive features of If the anthropomorphous apes be admitted to form a natural subgroup, then as man agrees with them, not only in all those the modern human phenotype had already evolved during our characters which he possesses in common with the whole Cata- ancestry with chimpanzees. Thus, a phylogenomic assessment of rhine group, but in other peculiar characters, such as the absence being human should examine earlier stages of human ancestry as of a tail and of callosities, and in general appearance, we may well as later stages. In addition, with the availability of a number of infer that some ancient member of the anthropomorphous sub- mammalian genomes, similarities in phenotype between distantly group gave birth to man (ref. 5, p. 160). related taxa should be explored for evidence of convergent or par- It is therefore probable that Africa was formerly inhabited by allel adaptive evolution. As an example, recent phylogenomic evi- extinct apes closely allied to the gorilla and chimpanzee; and as dence has shown that adaptive evolution of aerobic energy these two species are now man’s nearest allies, it is somewhat metabolism genes may have helped shape such distinctive modern more probable that our early progenitors lived on the African human features as long life spans and enlarged brains in the ances- continent than elsewhere (ref. 5, p. 161). tries of both humans and elephants. In regard to bodily size or strength, we do not know whether man is descended from some small species, like the chimpanzee, or from aerobic energy metabolism | brain | Charles Darwin | natural selection | one as powerful as the gorilla; and, therefore, we cannot say whether primate genomes man has become larger and stronger, or smaller and weaker, than his ancestors. We should, however, bear in mind that an animal harles Darwin proposed that natural selection favors inherited possessing great size, strength, and ferocity, and which, like the fi gorilla, could defend itself from all enemies, would not perhaps Cmodi cations that better adapt the organisms of a species to the have become social: and this would most effectually have checked environment of that species (1). Darwin also proposed the tree the acquirement of the higher mental qualities, such as sympathy ’ model for life s evolution. In this model, natural selection adaptively and the love of his fellows. Hence it might have been an immense modifies newly arisen species as they branch apart from their com- advantage to man to have sprung from some comparatively weak mon ancestor (1). Although there is now evidence that symbiotic creature (ref. 5, p. 65). fi merges produced the rst eukaryotes and that prokaryotic species As far as differences in certain important points of structure are engage in reticulate evolution (2–4), Darwin’s model of tree-like concerned, man may no doubt rightly claim the rank of a Suborder; branching appears to hold for the evolution of primates and other and this rank is too low, if we look chiefly to his mental faculties. vertebrates. Having deduced that species share common ancestors, Nevertheless, from a genealogical point of view it appears that this Darwin also reasoned that a truly natural system for classifying rank is too high, and that man ought to form merely a Family, or species would be genealogical, i.e., species should be classified possibly even only a Subfamily (ref. 5, p. 158). according to how recently they last shared a common ancestor. The Nevertheless the difference in mind between man and the higher hierarchical ranking in such a genealogical system could then be used animals, great as it is, certainly is one of degree and not of kind to indicate how relatively close or distant in geological time extant (ref. 5, p. 130). species are from their last common ancestor (LCA). Darwin’s application of the theory of evolution by natural In accord with this Darwinian framework, the phylogenomic selection to discussions of our own origins and place within approach to elucidating adaptive evolution in the ancestry of nature laid the foundation for modern phylogenetic and phylo- modern humans involves identifying the changes in genes and genomic studies of human evolution. He proposed that human- genomes on a phylogenetic tree that accurately places humans within the order Primates and, more widely, within the class Mammalia. Viewing the ancestries of many mammals, not just the ancestry of modern humans, could provide examples of convergent This paper results from the Arthur M. Sackler Colloquium of the National Academy of fi Sciences, “In the Light of Evolution IV: The Human Condition,” held December 10–12, adaptive evolution, which may point to speci c categories of genetic 2009, at the Arnold and Mabel Beckman Center of the National Academies of Sciences changes that are associated with important phenotypic changes. and Engineering in Irvine, CA. The complete program and audio files of most presentations This phylogenomic approach could help identify the positively are available on the NAS Web site at www.nasonline.org/SACKLER_Human_Condition. selected genetic changes that shaped such distinctive modern Author contributions: M.G. and K.N.S. designed research; M.G. analyzed data; and M.G. human features as prolonged prenatal and postnatal development, and K.N.S. wrote the paper. lengthened life spans, strong social bonds, enlarged brains, and high The authors declare no conflict of interest. cognitive abilities. In this article, we first briefly sketch out the his- This article is a PNAS Direct Submission. torical background of ideas and findings that have led to phyloge- 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.0914626107 PNAS Early Edition | 1of6 Downloaded by guest on September 29, 2021 kind originated from man-like apes (first quote) in Africa and molecular clock model the LCA of humans, chimpanzees, and that humans are most allied to chimpanzees and gorillas (second gorillas was placed at only 5 Mya (13, 14). quote). Further, Darwin seems to have thought that our pro- The determination of the actual amino acid sequences of genitors were more like chimpanzees than gorillas (third quote). proteins began in the 1950s (15) and, in the ensuing decades, Darwin challenged the then orthodox view that a whole taxo- provided important information about human evolution. Phylo- nomic order, the Bimana, should consist of only one species, our genetic analysis of hemoglobin amino acid sequences pointed to own Homo sapiens. Instead, Darwin noted that genealogically, the possibility that chimpanzees and humans were more closely we humans should have no more than a family or even just a related to each other than either was to gorillas (16–18). This subfamily to ourselves (fourth quote), suggesting that Darwin analysis grouped chimpanzee and gorilla with human rather than might have been willing to have a family Hominidae that grou- with orangutan hemoglobin (17, 18) and showed human and ped modern humans with man-like apes. Moreover, Darwin also chimpanzee hemoglobin to be identical and slightly divergent commented on the most widely cited example of human from gorilla hemoglobin (16–18). uniqueness, the modern human mind. He postulated that the Estimates of interspecies genetic similarities were also obtained by difference between the modern human mind and the mind of DNA–DNA hybridization data. An initial set of such data reported other higher animals was one of degree not of kind (fifth quote). in 1972 (19), similar to the hemoglobin amino acid sequence data, Nearly a century after Darwin first proposed the theory of evo- suggested that instead of a human–chimpanzee–gorilla trichotomy, lution by natural selection, molecular evolution emerged as a humans and chimpanzees shared the more recent common ancestor. scientific field and molecular methods began to be used toward During the 1980s, extensive DNA–DNA hybridization data clearly the study of human evolution. Molecular evidence inferred from placed chimpanzees closer to humans than to gorillas (20, 21). Direct proteins and DNA data generated during the past 50 years have measurements of interspecies genetic similarities were provided by vindicated Darwin’s foresightedness and have decisively estab- the actual nucleotide sequences of orthologous DNAs, each set of lished that among living species modern humans have their these DNA orthologues apparently having descended from the same closest kinship to common and bonobo chimpanzees.
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