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Molecular Clocks: Advanced article Determining the Age of Article Contents . Introduction . Considerations in Dating the Human–Chimpanzee the Human–Chimpanzee Divergence . Current Estimates, Conflicts and Resolution Divergence Online posting date: 30th April 2008 Michael I Jensen-Seaman, Duquesne University, Pittsburgh, Pennsylvania, USA Kathryn A Hooper-Boyd, Duquesne University, Pittsburgh, Pennsylvania, USA The approximate clocklike nature of the accumulation of nucleotide substitutions (the ‘molecular clock’) allows for the estimation of the time of divergence between modern species, dependent on calibrating the clock with known divergence dates from the fossil record. The molecular clock gives dates of approximately 6–8 million years ago for the human–chimpanzee divergence, in general agreement with the palaeontological evidence. Introduction differences among apes and humans (hominoids) were cal- ibrated with a fossil-based divergence date between ho- The idea that degrees of similarity among macromolecules minoids and Old World monkeys of 30 million years ago (deoxyribonucleic acid – DNA, ribonucleic acid – RNA (Mya), humans and chimpanzees diverged approximately 5 and protein) of different species could be used to construct Mya (Sarich and Wilson, 1967). Compared to interpreta- phylogenies of primates, to complement those from anat- tions of the fossil record at the time, which postulated a omy, is over 100 years old. When these differences were human–ape divergence in the middle Miocene (414 Mya; more accurately quantified and collected from numerous Pilbeam, 1968) or even earlier (Leakey, 1967), a human– species, it was suggested that changes in proteins may be chimpanzee divergence of only 5 Mya seemed remarkably occurring in a more or less regular manner, in proportion to recent. If Sarich and Wilson’s date was correct, then any evolutionary time (Zuckerkandl and Pauling, 1965); the fossil substantially older than this, including Ramapithecus same was suggested of DNA (Hoyer et al., 1965). Since, in (Pilbeam, 1968) and Kenyapithecus (Leakey, 1967), could principle, amino acid or nucleotide substitutions occur in not possibly be a hominin – that is, a species more closely direct proportion to time, this constant accumulation of related to humans than to chimps. This bold assertion that change was dubbed the ‘molecular clock’, and could be one must negate huge portions of the fossil record from used to date the time of divergence between extant species. consideration on the basis of molecular data led to the first The first attempt to use the molecular clock to date the major conflict between molecular and morphological data divergence between humans (Homo sapiens) and our clos- in the study of human evolution. Over the ensuing decade est relatives the chimpanzees (Pan troglodytes and Pan additional molecular data would support a recent date, paniscus) was by Vincent Sarich and Allan Wilson. In a while new fossil discoveries would reveal these early and series of papers in the late 1960s, they demonstrated that middle Miocene genera to be more ape-like than originally the amount of difference between serum albumin of described, supporting the possibility of a relatively recent primate species, as measured with quantitative cross- human–chimpanzee divergence (Greenfield, 1980). In reactions, was consistent with known phylogenies, that many ways this ‘victory’ for the molecular evolutionary the accumulation of differences occurs essentially ‘clock- biologists set the tone of confidence, if not arrogance, for like’ along different primate lineages, and that when the the ability of molecular data to inform – and indeed over- turn – interpretations based on the fossil record. ELS subject area: Evolution and Diversity of Life Considerations in Dating the Human– Chimpanzee Divergence How to cite: Jensen-Seaman, Michael I; and, Hooper-Boyd, Kathryn A (April 2008) Molecular Clocks: Determining the Age of the Human–Chimpanzee General principle Divergence. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, To estimate the time of divergence between humans and Ltd: Chichester. chimpanzees using the molecular clock, one needs an es- DOI: 10.1002/9780470015902.a0020813 timate of the evolutionary distance between these species, ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 1 Molecular Clocks: Determining the Age of the Human–Chimpanzee Divergence as well as an estimate of the substitution rate by calculating independent regions from different chromosomes. This the evolutionary distance between species whose time of also mitigates the possibility that selection is adversely divergence is known from the fossil record (Figure 1). The affecting the estimate of evolutionary distance, since it is evolutionary distance nowadays almost always comes unlikely to be acting to bias the estimate across all regions from comparing DNA sequences. If the molecular clock of the genome. The most pronounced intragenomic vari- ticks at the same rate in all relevant species, we can estimate ation in evolutionary distance between humans and chim- the nucleotide substitution rate (how fast the clock ticks) by panzees is seen in comparisons between the autosomes and dividing the evolutionary distance by the known time, and the sex chromosomes. The X-chromosome diverges more then apply this rate to the human–chimpanzee evolution- slowly than the autosomes, which in turn diverge more ary distance to calculate the unknown time. See also: slowly than the Y-chromosome (Innan and Watanabe, Molecular Clocks; Molecular Clocks 2006; Patterson et al., 2006); these differences are explained at least partly, but perhaps not entirely, by a higher mu- Estimating the evolutionary distance tation rate in the male germline (Makova and Li, 2002). Finally, the mitochondrial genome has a very high substi- There are several practical considerations in estimating the tution rate, but is almost entirely coding sequence. evolutionary distance between any two species. The first is Once nucleotide sequences are obtained from the rele- the choice of DNA sequences to use. Typically, noncoding vant species, they are aligned and an estimate of the evo- DNA (introns, intergenic regions or four-fold degenerate lutionary distance is made. The simplest measure would be sites) is used under the assumption that the rate of nucleo- to count the differences and divide by the total number of tide substitution reflects the underlying neutral mutation nucleotides to get the proportion of nucleotides that have rate, without being affected by natural selection which changed. This will, however, almost always be an under- could dramatically increase or decrease the rate of change estimate of the number of substations that have occurred in one lineage or another. Secondly, one must decide which because multiple substitutions at the same site may appear genes or what chromosomal regions to use. It is known that as a single change or no change. For this reason, many substantial variation in the local substitution rate exists different mathematical models have been developed to es- among regions of the human genome, perhaps due to var- timate the actual number of substitutions. In addition to iation in local GC (guanine–cytosine)-content, local re- correcting for multiple substitutions, increasingly complex combination rate and position relative to the telomere, models incorporate transition–transversion bias, unequal among other possible factors (CSAC, 2005). For this rea- nucleotide frequencies, and among site rate variation. son, sequences ideally would be chosen from many See also: Evolutionary Distance; Evolutionary Distance: Estimation Hominoid Cercopithecoid The final major consideration in estimating the evolu- tionary distance is whether the substitution rate is the same in all lineages; that is, does the molecular clock tick uni- Hominine Pongine formly across species? It is now well accepted that the nu- cleotide substitution rate does, in fact, vary among taxa. Hominin Old World monkeys, apes and humans (the catarrhines) have slower molecular clocks than the mammalian average Human Chimpanzee Orangutan Macaque (Yi et al., 2002), while rodents seem to have particularly fast molecular clocks. Within catarrhines, apes and humans (the hominoids) possess a slower molecular clock than Old World monkeys, an idea first proposed over four-and- ? a-half decades ago (Goodman, 1961) and now well- supported with large amounts of genomic sequence (Yi et al., 2002). The lack of a universal, or global, clock does not preclude the ability to estimate divergence dates since if Known date the clock ticks approximately uniformly in the relevant species (i.e. a ‘local clock’), it is still useful; furthermore, more complex models that incorporate substitution rate variation among lineages can be used to account for the Known date lack of a universal clock within primates. See also: Mole- cular Clocks; Molecular Clocks Calibrating with the fossil record Figure 1 Estimating the time of divergence between human and chimpanzee relies on a calibration based on a known divergence time – in this In order to convert the estimated evolutionary distance case either the hominine–pongine split or the hominoid–cercopithecoid into an estimate of species divergence in geologic time, it split. Note the taxonomy used herein. needs to be calibrated with the evolutionary distance 2 ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net Molecular Clocks: Determining the Age of the Human–Chimpanzee
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