Multiple L1 progenitors in prosimian primates: Phylogenetic evidence from ORF1 sequences

M. J. Stanhope, D. A. Tagle, M. S. Shivji, Masahira Hattori, Y. Sakaki, J. L. Slightom, M. Goodman

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

One of the uncertainties regarding the evolution of L1 elements is whether there are numerous progenitor genes. We present phylogenetic evidence from ORF1 sequences of slow loris (Nycticebus coucang) and galago (Galago crassicaudatus) that there were at least two distinct progenitors, active at the same time, in the ancestor of this family of prosimian primates. A maximum parsimony analysis that included representative L1s from human, rabbit, and rodents, along with the prosimian sequences, revealed that one of the galago L1s (Gc11) grouped very strongly with the slow loris sequences. The remaining galago elements formed their own unique and strongly supported clade. An analysis of replacement and silent site changes for each link of the most parsimonious tree indicated that during the descent of the Gc11 sequence approximately two times more synonymous than nonsynonymous substitutions had occurred, implying that the Gc11 founder was functional for some time after the split of galago and slow loris. Strong purifying selection was also evident on the galago branch of the tree. These data indicate that there were two distinct and contemporaneous L1 progenitors in the lorisoid ancestor, evolving under purifying selection, that were retained as functional L1s in the galago lineage (and presumably also in the slow loris). The prosimian ORF1 sequences could be further subdivided into subfamilies. ORF1 sequences from both the galago and slow loris have a premature termination codon near the 3' end, not shared by the other mammalian sequences, that shortens the open reading frame by 288 bp. An analysis of synonymous and nonsynonymous substitutions for the 5' and 3' portions, that included intra- and inter-subfamily comparisons, as well as comparisons among the other mammalian sequences, suggested that this premature stop codon is a prosimian acquisition that has rendered the 3' portion of ORF1 in these primates noncoding.

Original languageEnglish
Pages (from-to)179-189
Number of pages11
JournalJournal of Molecular Evolution
Volume37
Issue number2
Publication statusPublished - 1993
Externally publishedYes

Fingerprint

Galago
Strepsirhini
Lorisidae
ancestry
primate
Primates
substitution
Substitution reactions
Long Interspersed Nucleotide Elements
phylogenetics
parsimony analysis
phylogeny
rodent
replacement
Genes
gene
stop codon
Nonsense Codon
analysis
comparison

Keywords

  • Galago
  • L1
  • L1 source genes
  • LINE
  • ORF1
  • Slow loris

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)
  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry
  • Genetics
  • Molecular Biology
  • Genetics(clinical)

Cite this

Stanhope, M. J., Tagle, D. A., Shivji, M. S., Hattori, M., Sakaki, Y., Slightom, J. L., & Goodman, M. (1993). Multiple L1 progenitors in prosimian primates: Phylogenetic evidence from ORF1 sequences. Journal of Molecular Evolution, 37(2), 179-189.

Multiple L1 progenitors in prosimian primates : Phylogenetic evidence from ORF1 sequences. / Stanhope, M. J.; Tagle, D. A.; Shivji, M. S.; Hattori, Masahira; Sakaki, Y.; Slightom, J. L.; Goodman, M.

In: Journal of Molecular Evolution, Vol. 37, No. 2, 1993, p. 179-189.

Research output: Contribution to journalArticle

Stanhope, MJ, Tagle, DA, Shivji, MS, Hattori, M, Sakaki, Y, Slightom, JL & Goodman, M 1993, 'Multiple L1 progenitors in prosimian primates: Phylogenetic evidence from ORF1 sequences', Journal of Molecular Evolution, vol. 37, no. 2, pp. 179-189.
Stanhope MJ, Tagle DA, Shivji MS, Hattori M, Sakaki Y, Slightom JL et al. Multiple L1 progenitors in prosimian primates: Phylogenetic evidence from ORF1 sequences. Journal of Molecular Evolution. 1993;37(2):179-189.
Stanhope, M. J. ; Tagle, D. A. ; Shivji, M. S. ; Hattori, Masahira ; Sakaki, Y. ; Slightom, J. L. ; Goodman, M. / Multiple L1 progenitors in prosimian primates : Phylogenetic evidence from ORF1 sequences. In: Journal of Molecular Evolution. 1993 ; Vol. 37, No. 2. pp. 179-189.
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AB - One of the uncertainties regarding the evolution of L1 elements is whether there are numerous progenitor genes. We present phylogenetic evidence from ORF1 sequences of slow loris (Nycticebus coucang) and galago (Galago crassicaudatus) that there were at least two distinct progenitors, active at the same time, in the ancestor of this family of prosimian primates. A maximum parsimony analysis that included representative L1s from human, rabbit, and rodents, along with the prosimian sequences, revealed that one of the galago L1s (Gc11) grouped very strongly with the slow loris sequences. The remaining galago elements formed their own unique and strongly supported clade. An analysis of replacement and silent site changes for each link of the most parsimonious tree indicated that during the descent of the Gc11 sequence approximately two times more synonymous than nonsynonymous substitutions had occurred, implying that the Gc11 founder was functional for some time after the split of galago and slow loris. Strong purifying selection was also evident on the galago branch of the tree. These data indicate that there were two distinct and contemporaneous L1 progenitors in the lorisoid ancestor, evolving under purifying selection, that were retained as functional L1s in the galago lineage (and presumably also in the slow loris). The prosimian ORF1 sequences could be further subdivided into subfamilies. ORF1 sequences from both the galago and slow loris have a premature termination codon near the 3' end, not shared by the other mammalian sequences, that shortens the open reading frame by 288 bp. An analysis of synonymous and nonsynonymous substitutions for the 5' and 3' portions, that included intra- and inter-subfamily comparisons, as well as comparisons among the other mammalian sequences, suggested that this premature stop codon is a prosimian acquisition that has rendered the 3' portion of ORF1 in these primates noncoding.

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