Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid–cercopithecoid divergence

Steiper, Michael E.; Young, Nathan M.; Sukarna, Tika Y.

doi:10.1073/pnas.0407270101

Cited by 143 publications

(89 citation statements)

References 74 publications

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“…A comparison of the estimated and assumed time ratios resolves this discrepancy. For example, our ratios from 0.21 to 0.20 are consistent with the 0.21 value reported in analyses conducted by using Ͼ150,000 bp of noncoding data by Stieper et al (40), 97 protein-coding genes by Wildman et al (9), and complete mitochondrial DNA by Schrago et al (ref. 41; see also ref.…”

Section: Bayesian Inference Of the Minimum Time For Human-chimpanzeesupporting

confidence: 79%

“…The difference between hominoids and OWM is similar in magnitude to that reported in an analysis of large data sets by Yi et al (38) and Kumar and Subramanian (39). It is one-half of that reported by Steiper et al (40), whose estimates of relative rates depend on fossil-based divergence times for within-hominoid and withincercopithecoid species, although an outgroup was not used in their analyses.…”

Section: Bayesian Inference Of the Minimum Time For Human-chimpanzeementioning

confidence: 69%

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Placing confidence limits on the molecular age of the human–chimpanzee divergence

Kumar

Filipski

Swarna

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

191

102

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Molecular clocks have been used to date the divergence of humans and chimpanzees for nearly four decades. Nonetheless, this date and its confidence interval remain to be firmly established. In an effort to generate a genomic view of the human-chimpanzee divergence, we have analyzed 167 nuclear protein-coding genes and built a reliable confidence interval around the calculated time by applying a multifactor bootstrap-resampling approach. Bayesian and maximum likelihood analyses of neutral DNA substitutions show that the human-chimpanzee divergence is close to 20% of the ape-Old World monkey (OWM) divergence. Therefore, the generally accepted range of 23.8 -35 millions of years ago for the ape-OWM divergence yields a range of 4.98 -7.02 millions of years ago for human-chimpanzee divergence. Thus, the older time estimates for the human-chimpanzee divergence, from molecular and paleontological studies, are unlikely to be correct. For a given the ape-OWM divergence time, the 95% confidence interval of the human-chimpanzee divergence ranges from ؊12% to 19% of the estimated time. Computer simulations suggest that the 95% confidence intervals obtained by using a multifactor bootstrapresampling approach contain the true value with >95% probability, whether deviations from the molecular clock are random or correlated among lineages. Analyses revealed that the use of amino acid sequence differences is not optimal for dating humanchimpanzee divergence and that the inclusion of additional genes is unlikely to narrow the confidence interval significantly. We conclude that tests of hypotheses about the timing of human-chimpanzee divergence demand more precise fossil-based calibrations.Bayesian analysis ͉ molecular clock ͉ hominid ͉ fossil ͉ primate D etermining the age of the most recent common ancestor of humans and their closest African ape relatives has been the subject of scientific inquiry for over a century. This age is important for assessing the evolutionary rate of morphological and molecular changes in humans, assigning key fossils in hominoid phylogeny, and estimating when the common ancestor of all humans lived. The paleontological approach has been hampered by the paucity of fossils of some lineages. The first chimpanzee fossil, for example, was only just reported in 2005 (1). As recently as the mid-1960s (2), the African apes were considered to be distant relatives of the human lineage, but subsequent molecular phylogenetic analyses have shown that the chimpanzee and human are sister species and have led to a revision of the age of their divergence (3-13). Currently, the earliest unequivocal upright hominids at 4.2 millions of years ago (Ma) provide the minimum age for human-chimpanzee divergence (14), and some recently proposed early hominids dated between 5 and slightly more than 6 Ma are thought to provide an estimate close to the actual species divergence (15-19). However, a divergence time of 12.5 Ma for humans and chimpanzees has been entertained recently as well (20), and so the fossil record and its inte...

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Section: Bayesian Inference Of the Minimum Time For Human-chimpanzeesupporting

confidence: 79%

Section: Bayesian Inference Of the Minimum Time For Human-chimpanzeementioning

confidence: 69%

Placing confidence limits on the molecular age of the human–chimpanzee divergence

Kumar

Filipski

Swarna

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

191

102

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“…The relaxed molecular clock was calibrated with the three independent primate calibration dates: a human/chimpanzee split (4.2 to 8.0 Ma), an Old World monkey/hominoid split (20.6 to 30.0 Ma), and a Theropithecus/Papio split (4.0 to 6.0 Ma). The more recent limits of these calibration point ranges are based on the fossil record (17,30,31), whereas the more ancient limits were inferred from present knowledge of primate evolution (12,46,52,53).…”

Section: Vol 83 2009 Novel Retroviruses In Red Colobus Monkeys 11319mentioning

confidence: 99%

Coinfection of Ugandan Red Colobus ( Procolobus [ Piliocolobus ] rufomitratus tephrosceles ) with Novel, Divergent Delta-, Lenti-, and Spumaretroviruses

Goldberg

Sintasath

Chapman

et al. 2009

J Virol

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Nonhuman primates host a plethora of potentially zoonotic microbes, with simian retroviruses receiving heightened attention due to their roles in the origins of human immunodeficiency viruses type 1 (HIV-1) and HIV-2. However, incomplete taxonomic and geographic sampling of potential hosts, especially the African colobines, has left the full range of primate retrovirus diversity unexplored. Blood samples collected from 31 wild-living red colobus monkeys (Procolobus [Piliocolobus] rufomitratus tephrosceles) from Kibale National Park, Uganda, were tested for antibodies to simian immunodeficiency virus (SIV), simian T-cell lymphotrophic virus (STLV), and simian foamy virus (SFV) and for nucleic acids of these same viruses using genus-specific PCRs. Of 31 red colobus tested, 22.6% were seroreactive to SIV, 6.4% were seroreactive to STLV, and 97% were seroreactive to SFV. Phylogenetic analyses of SIV polymerase (pol), STLV tax and long terminal repeat (LTR), and SFV pol and LTR sequences revealed unique SIV and SFV strains and a novel STLV lineage, each divergent from corresponding retroviral lineages previously described in Western red colobus (Procolobus badius badius) or black-and-white colobus (Colobus guereza). Phylogenetic analyses of host mitochondrial DNA sequences revealed that red colobus populations in East and West Africa diverged from one another approximately 4.25 million years ago. These results indicate that geographic subdivisions within the red colobus taxonomic complex exert a strong influence on retroviral phylogeny and that studying retroviral diversity in closely related primate taxa should be particularly informative for understanding host-virus coevolution.The discovery of lentiviruses closely related to the pandemic strain of human immunodeficiency virus type 1 (HIV-1; group M) in central African chimpanzees (Pan troglodytes troglodytes [16]) has created considerable interest in the natural history of primate retroviruses, as has the discovery of lentiviruses related to HIV-2 in West African sooty mangabeys (Cercocebus atys [25]). The diversity of naturally circulating simian retroviruses is now known to be high, with most African primates harboring simian immunodeficiency viruses (SIVs) (1), simian T-cell lymphotrophic viruses (STLVs) (36), and simian foamy viruses (SFVs) (60). Nevertheless, our knowledge of the full range of primate retrovirus diversity remains incomplete due to limited taxonomic and geographic sampling of potential hosts.Although phylogenetic relationships of SFV lineages generally coincide with patterns of evolutionary relatedness among hosts (60), notable examples of natural cross-species transmission have been documented for each of the three retrovirus groups (3,8,16,29,33,64,(66)(67)(68). For SIV, some lineages seem to have cospeciated with simian hosts, but this appears to be the exception rather than the rule, with frequent host switching most parsimoniously explaining congruent host and SIV evolutionary histories (7). In contrast, STLV phylogeny typically parallels...

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“…In the first model, which we refer to as the ''two-rate model,'' rates of the human and chimpanzee lineages are assumed to be the same, whereas it is allowed to differ in the lineage leading to baboon, following the well established ''hominoid rate slowdown'' (5,6,8,9,14). An alternative model, which we refer to as the ''three-rate model,'' allows the human, chimpanzee, and baboon lineages to have different rates.…”

Section: Slower Molecular Clock In Humans Than In Chimpanzeesmentioning

confidence: 99%

Variable molecular clocks in hominoids

Elango

Thomas²,

Program³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Generation time is an important determinant of a neutral molecular clock. There are several human-specific life history traits that led to a substantially longer generation time in humans than in other hominoids. Indeed, a long generation time is considered an important trait that distinguishes humans from their closest relatives. Therefore, humans may exhibit a significantly slower molecular clock as compared to other hominoids. To investigate this hypothesis, we performed a large-scale analysis of lineage-specific rates of single-nucleotide substitutions among hominoids. We found that humans indeed exhibit a significant slowdown of molecular evolution compared to chimpanzees and other hominoids. However, the amount of fixed differences between humans and chimpanzees appears extremely small, suggesting a very recent evolution of human-specific life history traits. Notably, chimpanzees also exhibit a slower rate of molecular evolution compared to gorillas and orangutans in the regions analyzed.comparative genomics ͉ generation time ͉ hominoid evolution ͉ primate genomics H umans (Homo sapiens) have a longer generation time than any other extant hominoid because of differences in several life history traits. Humans take almost twice as long to reach sexual maturity as chimpanzees (Pan troglodytes) and gorillas (Gorilla gorillas) (1), have a longer lifespan, and have a longer gestation period as compared to any nonhuman hominoid (2). These traits are believed to have played important roles in human evolution. In particular, life span and the length of gestation are highly correlated with the size of the brain, which is approximately three times larger in humans than in other hominoids (2-4).Difference in generation times may leave a molecular signature by affecting evolutionary rates. Specifically, species with longer generation times are expected to exhibit slower rates of molecular evolution than those with shorter generation times. This hypothesis, called the ''generation-time effect hypothesis'' (5-7), is based on the idea that most germ-line mutations originate from errors in DNA replication. Because species with longer generation times go through fewer numbers of replications in germ cells per unit time, fewer substitutions will accumulate. This hypothesis has been strongly supported by molecular data (5-9).Therefore, the human lineage may exhibit a slower rate compared to other hominoids. However, genomic sequences of humans and other hominoids are extremely similar. For example, the alignable portions of human and chimpanzee genomes are 98.8% identical (9-13). Therefore, to detect subtle changes in the neutral substitution rates between these species, we need to perform high-quality, large-scale sequence comparisons. The recent accumulation of genomic sequence data from the chimpanzee genome (12, 13) and from several other catarrhines provide the opportunity to perform such comparisons.In this study, we analyzed an extensive amount of sequence data from humans and other hominoids to determine whether there...

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Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid–cercopithecoid divergence

Cited by 143 publications

References 74 publications

Placing confidence limits on the molecular age of the human–chimpanzee divergence

Placing confidence limits on the molecular age of the human–chimpanzee divergence

Coinfection of Ugandan Red Colobus ( Procolobus [ Piliocolobus ] rufomitratus tephrosceles ) with Novel, Divergent Delta-, Lenti-, and Spumaretroviruses

Variable molecular clocks in hominoids

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