Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans.
Retroviral infections of the germline have the potential to episodically alter gene function and genome structure during the course of evolution. Horizontal transmissions between species have been proposed, but little evidence exists for such events in the human/great ape lineage of evolution. Based on analysis of finished BAC chimpanzee genome sequence, we characterize a retroviral element (Pan troglodytes endogenous retrovirus 1 [PTERV1]) that has become integrated in the germline of African great ape and Old World monkey species but is absent from humans and Asian ape genomes. We unambiguously map 287 retroviral integration sites and determine that approximately 95.8% of the insertions occur at non-orthologous regions between closely related species. Phylogenetic analysis of the endogenous retrovirus reveals that the gorilla and chimpanzee elements share a monophyletic origin with a subset of the Old World monkey retroviral elements, but that the average sequence divergence exceeds neutral expectation for a strictly nuclear inherited DNA molecule. Within the chimpanzee, there is a significant integration bias against genes, with only 14 of these insertions mapping within intronic regions. Six out of ten of these genes, for which there are expression data, show significant differences in transcript expression between human and chimpanzee. Our data are consistent with a retroviral infection that bombarded the genomes of chimpanzees and gorillas independently and concurrently, 3-4 million years ago. We speculate on the potential impact of such recent events on the evolution of humans and great apes.
Yohn
Chris T
CT
Department of Genetics, Case Western Reserve University, Cleveland, Ohio, USA.
Jiang
Zhaoshi
Z
McGrath
Sean D
SD
Hayden
Karen E
KE
Khaitovich
Philipp
P
Johnson
Matthew E
ME
Eichler
Marla Y
MY
McPherson
John D
JD
Zhao
Shaying
S
Pääbo
Svante
S
Eichler
Evan E
EE
D000818:Animals; D002874:Chromosome Mapping; D020077:Endogenous Retroviruses / Q000235:genetics*; D006071:Gorilla gorilla / Q000235:genetics / Q000821:virology; D015186:Hominidae / Q000235:genetics* / Q000821:virology; D006801:Humans; D007438:Introns / Q000235:genetics; D008969:Molecular Sequence Data; D002679:Pan troglodytes / Q000235:genetics* / Q000821:virology; D011148:Pongo pygmaeus / Q000235:genetics* / Q000821:virology; D014176:Protein Biosynthesis; D018626:Retroelements / Q000235:genetics; D013045:Species Specificity; D014158:Transcription, Genetic
D018626:Retroelements
Nature. 2004 Oct 21;431(7011):931-45
15496913
Genome Res. 2004 Aug;14(8):1462-73
15289471
Nature. 1976 May 13;261(5556):101-8
179013
J Mol Evol. 1980 Dec;16(2):111-20
7463489
J Virol. 1982 Sep;43(3):914-24
6292470
Nature. 1984 Apr 5-11;308(5959):501-5
6424028
Mol Biol Evol. 1986 Sep;3(5):418-26
3444411
Trends Genet. 1991 Jan;7(1):22-7
1848377
Genomics. 1993 May;16(2):380-94
8390965
Methods Enzymol. 1993;225:681-701
8231879
J Virol. 1995 Dec;69(12):7877-87
7494300
Comput Appl Biosci. 1995 Dec;11(6):615-9
8808577
Nucleic Acids Res. 1997 Jul 15;25(14):2745-51
9207020
Genome Res. 1998 Mar;8(3):175-85
9521921
J Virol. 2000 Feb;74(3):1578-86
10627573
Bioessays. 2000 Feb;22(2):161-71
10655035
J Virol. 2000 Apr;74(8):3715-30
10729147
Genome Res. 2000 Jun;10(6):839-52
10854415
Am J Hum Genet. 2001 Feb;68(2):444-56
11170892
J Mol Diagn. 2000 Aug;2(3):128-31
11229516
Nature. 2001 Feb 15;409(6822):860-921
11237011
Nat Genet. 2001 Apr;27(4):361-5
11279513
Genome Res. 1998 Mar;8(3):195-202
9521923
Am J Hum Genet. 1999 Jan;64(1):31-9
9915940
J Virol. 1999 Mar;73(3):2442-9
9971829
Nature. 2001 Jul 12;412(6843):175-8
11449271
J Gen Virol. 2001 Aug;82(Pt 8):1829-34
11457988
Nat Genet. 2001 Dec;29(4):487-9
11704760
Mol Biol Evol. 2002 Apr;19(4):526-33
11919294
Am J Hum Genet. 2002 Jun;70(6):1490-7
11992255
J Virol. 2002 Jun;76(11):5540-7
11991982
Nature. 2002 Jul 11;418(6894):145-51
12110880
Cell. 2002 Aug 23;110(4):521-9
12202041
Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11748-53
12186979
Genomics. 2002 Sep;80(3):331-43
12213204
Genome Res. 2002 Oct;12(10):1483-95
12368240
Genetics. 2003 Jan;163(1):395-404
12586724
Nature. 2003 Mar 6;422(6927):61-5
12621432
Science. 2003 Jun 13;300(5626):1749-51
12805549
Genetics. 2003 Aug;164(4):1645-56
12930768
J Virol. 2004 Apr;78(8):4370-5
15047851
Proc Natl Acad Sci U S A. 2004 Apr 6;101(14):4894-9
15044706
Am J Phys Anthropol. 2004 Jun;124(2):99-108
15160364
Genome Res. 2004 Jun;14(6):1068-75
15173113
Proc Natl Acad Sci U S A. 1975 Jun;72(6):2315-9
49058