Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Apr;85(8):2658–2661. doi: 10.1073/pnas.85.8.2658

Sequence analyses of herpesviral enzymes suggest an ancient origin for human sexual behavior.

G A Gentry 1, M Lowe 1, G Alford 1, R Nevins 1
PMCID: PMC280057  PMID: 3128793

Abstract

Comparison of the amino acid sequences of the deoxythymidine kinases of herpes simplex (HSV) and of marmoset herpes viruses (MHV) suggests a divergence time of 8 to 10 million years ago for HSV-1 and -2. Like MHV, HSV-1 and -2 cause local infections in their natural hosts, and direct contact between two individuals during the brief period of infectivity is needed for transmission. Because B virus, a nearer relative of HSV, depends on both oral and genital routes of transmission, we postulate that ancestral HSV (aHSV) was similar, and that for HSV-1 and -2 to diverge, genital and oral sites had to become microbiologically somewhat isolated from each other, while oral--oral and genital--genital contact had to be facilitated to maintain both aHSV strains. We propose that acquisition of continual sexual attractiveness by the ancestral human female and the adoption of close face-to-face mating, two hallmarks of human sexual behavior, provided the conditions for the divergence.

Full text

PDF
2659

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baer R., Bankier A. T., Biggin M. D., Deininger P. L., Farrell P. J., Gibson T. J., Hatfull G., Hudson G. S., Satchwell S. C., Séguin C. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature. 1984 Jul 19;310(5974):207–211. doi: 10.1038/310207a0. [DOI] [PubMed] [Google Scholar]
  2. Boyle D. B., Coupar B. E., Gibbs A. J., Seigman L. J., Both G. W. Fowlpox virus thymidine kinase: nucleotide sequence and relationships to other thymidine kinases. Virology. 1987 Feb;156(2):355–365. doi: 10.1016/0042-6822(87)90415-6. [DOI] [PubMed] [Google Scholar]
  3. Britten R. J. Rates of DNA sequence evolution differ between taxonomic groups. Science. 1986 Mar 21;231(4744):1393–1398. doi: 10.1126/science.3082006. [DOI] [PubMed] [Google Scholar]
  4. Caras I. W., Levinson B. B., Fabry M., Williams S. R., Martin D. W., Jr Cloned mouse ribonucleotide reductase subunit M1 cDNA reveals amino acid sequence homology with Escherichia coli and herpesvirus ribonucleotide reductases. J Biol Chem. 1985 Jun 10;260(11):7015–7022. [PubMed] [Google Scholar]
  5. Carlson J., Fuchs J. A., Messing J. Primary structure of the Escherichia coli ribonucleoside diphosphate reductase operon. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4294–4297. doi: 10.1073/pnas.81.14.4294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coen D. M., Schaffer P. A., Furman P. A., Keller P. M., St Clair M. H. Biochemical and genetic analysis of acyclovir-resistant mutants of herpes simplex virus type 1. Am J Med. 1982 Jul 20;73(1A):351–360. doi: 10.1016/0002-9343(82)90122-x. [DOI] [PubMed] [Google Scholar]
  7. Corey L., Spear P. G. Infections with herpes simplex viruses (2). N Engl J Med. 1986 Mar 20;314(12):749–757. doi: 10.1056/NEJM198603203141205. [DOI] [PubMed] [Google Scholar]
  8. Dahl J. F. The external genitalia of female pygmy chimpanzees. Anat Rec. 1985 Jan;211(1):24–28. doi: 10.1002/ar.1092110105. [DOI] [PubMed] [Google Scholar]
  9. Davison A. J., Scott J. E. The complete DNA sequence of varicella-zoster virus. J Gen Virol. 1986 Sep;67(Pt 9):1759–1816. doi: 10.1099/0022-1317-67-9-1759. [DOI] [PubMed] [Google Scholar]
  10. Dayhoff M. O., Barker W. C., Hunt L. T. Establishing homologies in protein sequences. Methods Enzymol. 1983;91:524–545. doi: 10.1016/s0076-6879(83)91049-2. [DOI] [PubMed] [Google Scholar]
  11. Desrosiers R. C., Falk L. A., Jr Herpesvirus tamarinus and its relation to herpes simplex virus. J Gen Virol. 1981 Sep;56(Pt 1):119–130. doi: 10.1099/0022-1317-56-1-119. [DOI] [PubMed] [Google Scholar]
  12. Earl P. L., Jones E. V., Moss B. Homology between DNA polymerases of poxviruses, herpesviruses, and adenoviruses: nucleotide sequence of the vaccinia virus DNA polymerase gene. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3659–3663. doi: 10.1073/pnas.83.11.3659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fitch W. M., Margoliash E. Construction of phylogenetic trees. Science. 1967 Jan 20;155(3760):279–284. doi: 10.1126/science.155.3760.279. [DOI] [PubMed] [Google Scholar]
  14. Fleagle J. G., Bown T. M., Obradovich J. D., Simons E. L. Age of the earliest african anthropoids. Science. 1986 Dec 5;234(4781):1247–1249. doi: 10.1126/science.234.4781.1247. [DOI] [PubMed] [Google Scholar]
  15. Galloway D. A., Swain M. A. Organization of the left-hand end of the herpes simplex virus type 2 BglII N fragment. J Virol. 1984 Mar;49(3):724–730. doi: 10.1128/jvi.49.3.724-730.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gibbs J. S., Chiou H. C., Hall J. D., Mount D. W., Retondo M. J., Weller S. K., Coen D. M. Sequence and mapping analyses of the herpes simplex virus DNA polymerase gene predict a C-terminal substrate binding domain. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7969–7973. doi: 10.1073/pnas.82.23.7969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gibson T., Stockwell P., Ginsburg M., Barrell B. Homology between two EBV early genes and HSV ribonucleotide reductase and 38K genes. Nucleic Acids Res. 1984 Jun 25;12(12):5087–5099. doi: 10.1093/nar/12.12.5087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heilbronn R., Jahn G., Bürkle A., Freese U. K., Fleckenstein B., zur Hausen H. Genomic localization, sequence analysis, and transcription of the putative human cytomegalovirus DNA polymerase gene. J Virol. 1987 Jan;61(1):119–124. doi: 10.1128/jvi.61.1.119-124.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Knopf C. W. Nucleotide sequence of the DNA polymerase gene of herpes simplex virus type 1 strain Angelotti. Nucleic Acids Res. 1986 Oct 24;14(20):8225–8226. doi: 10.1093/nar/14.20.8225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koop B. F., Goodman M., Xu P., Chan K., Slightom J. L. Primate eta-globin DNA sequences and man's place among the great apes. Nature. 1986 Jan 16;319(6050):234–238. doi: 10.1038/319234a0. [DOI] [PubMed] [Google Scholar]
  21. Littler E., Zeuthen J., McBride A. A., Trøst Sørensen E., Powell K. L., Walsh-Arrand J. E., Arrand J. R. Identification of an Epstein-Barr virus-coded thymidine kinase. EMBO J. 1986 Aug;5(8):1959–1966. doi: 10.1002/j.1460-2075.1986.tb04450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lovejoy C. O. The origin of man. Science. 1981 Jan 23;211(4480):341–350. doi: 10.1126/science.211.4480.341. [DOI] [PubMed] [Google Scholar]
  23. McLauchlan J., Clements J. B. DNA sequence homology between two co-linear loci on the HSV genome which have different transforming abilities. EMBO J. 1983;2(11):1953–1961. doi: 10.1002/j.1460-2075.1983.tb01684.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McLauchlan J., Clements J. B. Organization of the herpes simplex virus type 1 transcription unit encoding two early proteins with molecular weights of 140000 and 40000. J Gen Virol. 1983 May;64(Pt 5):997–1006. doi: 10.1099/0022-1317-64-5-997. [DOI] [PubMed] [Google Scholar]
  25. Meyer T. E., Cusanovich M. A., Kamen M. D. Evidence against use of bacterial amino acid sequence data for construction of all-inclusive phylogenetic trees. Proc Natl Acad Sci U S A. 1986 Jan;83(2):217–220. doi: 10.1073/pnas.83.2.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nadler R. D. Reproductive physiology and behaviour of gorillas. J Reprod Fertil Suppl. 1980;Suppl 28:79–89. [PubMed] [Google Scholar]
  27. Nikas I., McLauchlan J., Davison A. J., Taylor W. R., Clements J. B. Structural features of ribonucleotide reductase. Proteins. 1986 Dec;1(4):376–384. doi: 10.1002/prot.340010411. [DOI] [PubMed] [Google Scholar]
  28. Otsuka H., Kit S. Nucleotide sequence of the marmoset herpesvirus thymidine kinase gene and predicted amino acid sequence of thymidine kinase polypeptide. Virology. 1984 Jun;135(2):316–330. doi: 10.1016/0042-6822(84)90189-2. [DOI] [PubMed] [Google Scholar]
  29. Parris D. S., Harrington J. E. Herpes simplex virus variants restraint to high concentrations of acyclovir exist in clinical isolates. Antimicrob Agents Chemother. 1982 Jul;22(1):71–77. doi: 10.1128/aac.22.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Quinn J. P., McGeoch D. J. DNA sequence of the region in the genome of herpes simplex virus type 1 containing the genes for DNA polymerase and the major DNA binding protein. Nucleic Acids Res. 1985 Nov 25;13(22):8143–8163. doi: 10.1093/nar/13.22.8143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schwartz R. M., Dayhoff M. O. Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science. 1978 Jan 27;199(4327):395–403. doi: 10.1126/science.202030. [DOI] [PubMed] [Google Scholar]
  32. Sibley C. G., Ahlquist J. E. The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol. 1984;20(1):2–15. doi: 10.1007/BF02101980. [DOI] [PubMed] [Google Scholar]
  33. Sjöberg B. M., Hahne S., Mathews C. Z., Mathews C. K., Rand K. N., Gait M. J. The bacteriophage T4 gene for the small subunit of ribonucleotide reductase contains an intron. EMBO J. 1986 Aug;5(8):2031–2036. doi: 10.1002/j.1460-2075.1986.tb04460.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Soeda E., Maruyama T., Arrand J. R., Griffin B. E. Host-dependent evolution of three papova viruses. Nature. 1980 May 15;285(5761):165–167. doi: 10.1038/285165a0. [DOI] [PubMed] [Google Scholar]
  35. Standart N. M., Bray S. J., George E. L., Hunt T., Ruderman J. V. The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs. J Cell Biol. 1985 Jun;100(6):1968–1976. doi: 10.1083/jcb.100.6.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Swain M. A., Galloway D. A. Herpes simplex virus specifies two subunits of ribonucleotide reductase encoded by 3'-coterminal transcripts. J Virol. 1986 Mar;57(3):802–808. doi: 10.1128/jvi.57.3.802-808.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Swain M. A., Galloway D. A. Nucleotide sequence of the herpes simplex virus type 2 thymidine kinase gene. J Virol. 1983 Jun;46(3):1045–1050. doi: 10.1128/jvi.46.3.1045-1050.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thelander L., Berg P. Isolation and characterization of expressible cDNA clones encoding the M1 and M2 subunits of mouse ribonucleotide reductase. Mol Cell Biol. 1986 Oct;6(10):3433–3442. doi: 10.1128/mcb.6.10.3433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tsurumi T., Maeno K., Nishiyama Y. Nucleotide sequence of the DNA polymerase gene of herpes simplex virus type 2 and comparison with the type 1 counterpart. Gene. 1987;52(2-3):129–137. doi: 10.1016/0378-1119(87)90039-4. [DOI] [PubMed] [Google Scholar]
  40. Vawter L., Brown W. M. Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science. 1986 Oct 10;234(4773):194–196. doi: 10.1126/science.3018931. [DOI] [PubMed] [Google Scholar]
  41. Wagner M. J., Sharp J. A., Summers W. C. Nucleotide sequence of the thymidine kinase gene of herpes simplex virus type 1. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1441–1445. doi: 10.1073/pnas.78.3.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wilson A. C., Carlson S. S., White T. J. Biochemical evolution. Annu Rev Biochem. 1977;46:573–639. doi: 10.1146/annurev.bi.46.070177.003041. [DOI] [PubMed] [Google Scholar]
  43. Wyles J. S., Kunkel J. G., Wilson A. C. Birds, behavior, and anatomical evolution. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4394–4397. doi: 10.1073/pnas.80.14.4394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zwartouw H. T., Boulter E. A. Excretion of B virus in monkeys and evidence of genital infection. Lab Anim. 1984 Jan;18(1):65–70. doi: 10.1258/002367784780864929. [DOI] [PubMed] [Google Scholar]
  45. Zwartouw H. T., MacArthur J. A., Boulter E. A., Seamer J. H., Marston J. H., Chamove A. S. Transmission of B virus infection between monkeys especially in relation to breeding colonies. Lab Anim. 1984 Apr;18(2):125–130. doi: 10.1258/002367784780891352. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES