Trends in Genetics
Volume 21, Issue 9, September 2005, Pages 511-517
Journal home page for Trends in Genetics

Moving primate genomics beyond the chimpanzee genome

https://doi.org/10.1016/j.tig.2005.06.012Get rights and content

The comparative DNA sequence data that already exist on individual genomic loci depict the phylogenetic relationships of nearly all extant primate genera. Such a phylogenetic representation of the primates, validated by many sequenced primate genomes, and encompassing the full adaptive diversity of the order, is a prerequisite for identifying the genetic basis of humankind, and for testing the proposed human uniqueness of these traits. Some of these traits have been discovered recently, particularly in genes encoding proteins that are important for brain function.

Introduction

There is mounting DNA evidence that the living members of the great ape clade (see Glossary) are common and bonobo chimpanzees, humans, gorillas and orangutans, with chimpanzees being the sister group to humans, gorillas to the chimpanzee-human clade, and orangutans to the chimpanzee-human–gorilla clade 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12. The degree of genetic similarity among the members of this great ape clade is reflected in the predominantly noncoding orthologous DNA sequences, which from human and chimpanzee nuclear genomes are on average ∼98.9% identical, whereas with gorilla orthologs they are on average ∼98.5% identical and with orangutan orthologs ∼97.0% identical 3, 6, 11, 12. These values are based on multispecies alignments in which the human, chimpanzee, gorilla, orangutan and other primate DNA sequences were aligned against one another. Humans and chimpanzee are equally divergent from gorillas, and human, chimpanzees and gorillas are equally divergent from orangutans. The close genetic kinship between humans and chimpanzees is now being documented by large-scale DNA comparisons involving a draft sequence of the entire chimpanzee genome (www.nhgri.nih.gov/11509418).

The proposal to sequence an entire chimpanzee genome was based on the premise that this genome sequence would be needed to search for the genetic basis of being human 13, 14. Supposedly, the search for the genetic basis could then be restricted to the small percentage of differing nucleotides between the human and chimpanzee genomes. However, that would be far too restrictive. Although uniquely human features have certainly emerged since the time of the last common ancestor (LCA) of humans and the common and bonobo chimpanzees, it is also true that many traits used to define humanity have much deeper roots. For example, the intricate capabilities that humans possess to make and use tools have their origins in the prehensile and opposable grasping hands that are shared by all clades in the order Primates. Indeed, to identify the genetic roots of being human the comparative primate genomic data need to be enlarged and placed in a phylogenetic framework that encompasses the entire order Primates. Here we present a molecular view of primate phylogeny as revealed by the comparative primate genomic data that currently exist. An accurate phylogenetic framework should facilitate the genomic search for the genetic roots that shaped being human. To illustrate our viewpoint, we discuss how comparative genomic data can test the model that depicts probable adaptive evolution of those genes involved in the process of encephalization in primates.

Section snippets

Primate phylogeny

Of the >300 species of >60 genera that represent the extant members of the order Primates, complete or nearly complete DNA sequences are as yet available only for the human and common chimpanzee genomes. However, sequencing of the rhesus macaque genome, a representative of the Old World monkey branch of primates, is far advanced and an assembled version of this genome was publicly released in May 2005 (http://www.genome.gov/11008262; http://www.hgsc.bcm.tmc.edu/projects/rmacaque). Additionally,

Darwinian evolution

Of the 20 000 to 25 000 genes in a human genome, relatively few as yet have sequenced orthologs from enough different primates to reflect the adaptive diversity of the order. Nevertheless the results gathered so far indicate that darwinian evolution frequently occurred, more often in common ancestral lineages or in one or another terminal non-human lineage than in the terminal human lineage 9, 26, 27, 28, 29, 30. A case in point is provided by a gene (SEMG2) encoding semenogelin, the main

Outlook and conclusion

The nearly complete human genome sequence (build 35) suggests that there are between 20 000 and 25 000 genes in our species [40]. Complete primate genome sequences will enable us to trace the evolution of all of these genes and their regulatory sequences. The upsurges in nonsynonymous substitutions, indicative of positive selection for protein sequence changes, should be readily detectable. In addition, via a variety of techniques including phylogenetic footprinting 41, 42, phylogenetic

Update

Nielsen et al. [52] have recently compared 13 731 annotated human genes with their chimpanzee orthologs and found that the strongest evidence of positive selection is afforded by genes involved in sensory perception or immune defenses, including tumor suppression and apoptosis as well as spermatogenesis. The design of these comparisons precluded investigating the evolutionary history of these genes showing evidence of more recently occurring positive selection in either humans or chimpanzees or

Acknowledgements

We thank Edwin McConkey, Jianzhi Zhang, Robert Shields and two anonymous reviewers for providing stimulating and thoughtful comments on this manuscript. We also acknowledge the generous support of the National Institutes of Health (DK-56927, GM-65580) and the National Science Foundation (BCS-0318375).

Glossary

Anthropoid:
a primate clade that includes catarrhines and New World monkeys. The sister group of tarsiers.
Ape:
a primate clade that as a crown group includes humans, common and bonobo chimpanzees, gorillas, orangutans, gibbons and siamangs. The sister group of Old World monkeys.
Catarrhine:
a primate clade that includes Old World monkeys and apes. The sister group of New World monkeys.
Clade:
a group of organisms united by evolutionary descent from a common ancestor. The group includes a most recent

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