Professional Documents
Culture Documents
Journal of
Molecular Evolution
© Springer-Verlag New York Inc. 1987
Michael Syvanen
Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, CA 95616, USA
Summary. This paper discusses recent evidence though what I will refer to is transfer of any flucleotide
suggesting that genetic information from one species sequence from the germ line of one species to that of
occasionally transfers to another remotely related another. My discussion focuses on molecular evolution
species. Besides addressing the issue of whether or not in animals, but it is notable that in plants, sequence
the molecular data are consistent with a widespread convergence is so frequent that it is hard to construct
influence of horizontal gene transfer, the paper shows phylogenies from molecular data (Peacock and Boulter
that horizontal gene flow would not necessarily preclude 1975). (This convergence could reflect the operation of
a linear molecular clock or change the rate of molecular plant hybridization mechanisms that are nonexistent or
evolution (assuming the neutral allele theory). A much less active in animals. Virally mediated gene
pervasive influence of horizontal gene transfer is more transfers may also play a role.) This paper discusses
than just consistent with the data of molecular evolution, three topics: (1) possible examples of the interspecies
it also provides a unique explanation for a number of exchange of genetic information, (2) how this exchange
possibly conflicting phylogenies and contradictory may influence molecular evolution and the molecular
clocks. This phenomenon might explain why some clock, and (3) the resolution of conflicts between
protein clocks are linear while the superoxide dismutase molecular and organismal systematics, with specific
clock is not, how the molecular data on the phylogeny of examples.
apes and Australian song birds are not necessarily in
conflict with those based on morphology, and, finally,
why the mycoplasmas have an accelerated molecular Cross-Species Gene Transfer
clock.
Only a few cases of whole genes being transferred
Key words: Relative rate test — Globin genes — across animal species barriers have been reported. For
Cytochromes — Pseudogenes — Coadaptation —Viruses — reasons given below, I do not think these cases will turn
Viral host range — Bacteria — Songbirds out to be the most important. The possible transfer of
— Apes parts of genes may prove to be more important. This was
first suggested from an analysis of four sequenced
mammalian ß-globin genes (Syvanen 1 984a) where
intron-mediated cross-species gene conversion events
Introduction were proposed. This example is controversial because it
can be argued that the conserved “silent” regions of the
I explore the formal possibility that the molecular clock ß-globin gene that I documented are still conserved by
may be experiencing influences that limit its functional constraint and not by the cross-species gene
genealogical utility. I refer to the possible movement of conversion events. This pattern of unusually highly con-
genetic information from one species to another. This served regions in the vicinity of introns has also been
process is called cross-species gene exchange, reported from a comparison of the xxx-y-globin genes
from human, chimpanzee, and gorilla (Scott et al. 1984;
Slightom et al. 1985). The significance of the conserved
gaps in this latter case is statistically
lation geneticists and empirical evidence has been protein would be expected to show continual
provided for it by molecular biologists working with divergence with time.
hybrid phages (Furth and Yates 1978; Susskind and Proteins frequently cited as supporting a constant
Botstein 1978), from reversion studies of bacterial molecular clock hypothesis include cytochrome-c,
mutants (Ebright et al. 1985), and from interspecific xxxa-globin, and ß-globin, all of which are physically
hybrids of the mammalian cytochrome chain (Fer- complexed to other proteins. This can be contrasted
guson-Miller et al. 1976; Osheroffet al. 1983). Coad- with the superoxide dismutase clock, recently de-
aptation is seen with genes encoding proteins that scribed by Lee et al. (1985), which is grossly non-
physically interact with specific DNA sequences or linear. Superoxide dismutase is an enzyme that is
with other proteins, and that are functionally con- involved in detoxifying 02 radicals. As such it is a
strained by their partner’s primary sequences. The soluble cytoplasmic enzyme for which there is no
range of possible amino acid substitutions in such a evidence to suggest, nor reason to believe, that this
protein will, in part, be determined by its partner’s enzyme specifically interacts with other proteins. Thus,
primary sequence and will in turn influence its partner. superoxide dismutase from any one species is probably
This will lead to codivergence of an interacting pair unconstrained to function in other organisms.
such that they continue to be coadapted with each other.
Cann et a!. (1984) have presented rate data directly The Relative Rate Test
supporting the notion that cytochrome-c and A constant rate of molecular evolution in many
cytochrome oxidase coevolved. As a homologous pair different lineages has been supported by the results of
diverges from its common ancestor, a point will be the relative rate test. One might argue from this that
reached where transfer of a functional protein from one cross-species gene exchange cannot strongly in-
species to another will be forbidden. Thus, a coadapted
20
why such a transfer mechanism would exist in the first Dickerson RE (1980) Evolution and gene transfer in purple
place. In this paper the discussion has dealt with photosynthetic bacteria. Nature 283:210—212
Duesberg PH (1983) Retroviral transforming genes in normal cells?
molecular c!ock data, which probably reflect the fixation Nature 304:219—226
of neutral events through the action of stochastic Ebright RH, Cossart P. Gisquel-Sanzy B, Beckwith J (1984) Mutations
processes. Evolution is more than this; it is also a that alter the DNA sequence specificity of the catabolite gene activator
progression of improved forms that are fixed by natural protein of E. coli. Nature 311:232—235
selection. As I have argued elsewhere, natural selection Emori Y, Shiba T, Kenaya 5, Inouye 5, Yuki 5, Saigo K (1985) The
nucleotide sequence of copia and copia-related RNA in Drosophila
acting on many separate lineages could possibly act to virus-like particles. Nature 3 15:773—776
select indirectly for the mechanism of cross-species gene Erwin DH, Valentine JW (1984) Hopeful monsters, transpoSons and
transfer simply through the increase in the rate of metazoan radiation. Proc Natl Acad Sci USA 81: 5482—5483
acquisitive evolution such a process would effect Evans AS (1976) Viral infections; epidemiology and control. Plenum,
(Syvanen 1985). Since such a process would not be New York
Fenner F, White DO (1970) Medical virology. Academic Press, New
teleological, one would therefore expect it to act on York
neutral positions as well. Ferguson-MillerS, Bautigan D, Chaviano A, Margoliash E (1976)
Kinetic control of electron transfer in primate and non primate
Addendum cytochromes C. Fed Proc 35:1605
Furth ME, Yates JL (1978) Specificity determinants for bacteriophage
Since this paper was written there have been three reports of unusually lambda DNA replication. J Mol Biol 126:227—245
homologous genes between highly unrelated species that possibly Garfinkel DJ, Boeke JD, Fink GR (1985) Ty element transposition:
constitute examples of gene transfers from eukaryotes to bacteria. The reverse transcriptase and virus-like particles. Cell 42:507—517
prokaryotic genes involved are a glutamine synthetase II from Gerlach JH, Endicott JA, Juranka PF, Henderson G, Sarangi F,
Bradyrhizobium japonicum (Carlson and Chelm 1986), a hemolysin Deuchars KL, Ling V (1986) Homology between P-glycoprotein and a
transport protein from Escherichia coli (Gerlach et at. 1986), and a bacterial haemolysin transport protein suggests a model for multidrug
self-processing intron from bacteriophage T4 (Michel and Dujon resistance. Nature 324:485—489
1986). Another major incongruency between a minimal tree based on Gruskin KD, Smith TF, Goodman M (1987) Possible origin of a
morphological characters and one based on protein sequences has been calmodulin gene that lacks intervening sequences. Proc Natl Acad Sci
reported where the geographically isolated assemblages show much USA 84:1605—1608
closer relatedness on the basis of sequence data than they do on the Harris 5, Thackeray JR, Jeifreys AJ, Weiss ML (1986) Nucleotide
basis of morphological characters. This case involves the relationship sequence analysis of the lemur ß-globin gene family:
of two lemur families to other African primates (Harris et al. 1986). In evidence for major rate fluctuations in globin polypeptide
addition, Wyss et at. (1987) have defended the use of morphological evolution. Mol Biol Evol 3:465—484
data in tree construction by showing that in mammals, morphological Hartman H (1976) Speculations on viruses, cells and evolution. Evol
character sets are not less consistent (as measured by the consistency Theory 3:159—163
index) than are protein sequences. Hauber J, Nelböck-Hochstetter T. Feldmann H (1985) Nucleotide
sequence and characteristics of a Ty element from yeast. Nucleic Acids
Acknowledgments. I thank Steve McCommas and Sue Greenwald for Res 13:2745—2758
helpful discussion and for critically reading the manuscript. Kidwell MG (1983) Evolution of hybrid dysgenesis determinants in
Drosophila melanogaster. Proc Natl Acad Sci USA 80: 1655—1659
Kimura M (1968) Evolutionary rate at the molecular level. Nature
References
217:624—626
Lee YM, Friedman D, Ayala F (1985) Superoxide dismutase:
Ambler RP, Meyer TE, Kamen MD (1979) Cytochrome C2 sequence an evolutionary puzzle. Proc Natl Acad Sci USA 82:824—828
variation among the recognised species of purple non sulfur Li WH, Gojobori T, Nei M (1981) Pseudogenes as a paradigm
photosynthetic bacteria. Nature 278:659—660 of neutral evolution. Nature 292:237—239
Benveniste RE, Todaro GJ (1974) Evolution of c-type viral genes: Michel F, Dujon B (1986) Genetic exchanges between bacteriophage
inheritance ofexogenously acquired viral genes. Nature T4 and filamentous fungi? Cell 46:323
252:456—459 Miller DW, Miller LK (1982) A virus mutant with an insertion of a
Bishop JM (1983) Cellular oncogenes and retroviruses. Annu Rev copia-like transposable element. Nature 299:562—564
Biochem 52:30 1—354 Miyata T, Hayashida H (1981) Extraordinary high evolutionary rate of
Bishop JM (1985) Viral oncogenes. Cell 42:23—38 pseudogenes: evidence for the presence of selective pressure against
Boeke JD, Garfinkel DJ, Styles CA, Fink GR (1985) Ty elements changes between synonymous codons. Proc Natl Acad Sci USA
transpose through an RNA intermediate. Cell 40:491— 500 78:5739—5743
Cann RC, Brown WM, Wilson AC (1984) Polymorphic sites and the Miyata T, Yasuga T (1981) Rapidly evolving mouse a-globin pseudo
mechanism of evolution in human mitochondrial DNA. Genetics gene and its evolutionary history. Proc Natl Acad Sci USA 78:450—
106:479—499 453
Carlson TA, Chelm BK (1986) Apparent eukaryotic origin of Osheroff N, Speck 5, Margoliash E, Veerman E, Wilms J, Konig B,
glutamine synthetase II from the bacterium Bradyrhizobium Muijsers A (1983) The reaction of primate cytochromes C with
japonicum. Nature 322:568—670 cytochrome C oxidase. J Biol Chem 258:5731—5738
Clare J, Farabaugh P (1985) Nucleotide sequence of a yeast Ty Peacock D, Boulter D (1975) Use of amino acid sequence data in
element: evidence for an unusual mechanism of gene expression. Proc phylogeny and evaluation of methods using computer simulation. J Mol
Natl Acad Sci USA 82:2829—2833 Biol 95:513—527
23
Reanney D (1976) Extrachromosomal elements as possible agents primates, as indicated by DNA—DNA hybridization. J Mol Evol
of adaptation and development. Bacteriol Rev 40:552— 590 20:2—15
Ryan JL, Morowitz HJ (1969) Partial purification of native sRNA Slightom JL, Chang L-YE, Koop BF, Goodman M (1985)
and tRNA cistrons from Mycoplasma sp. (KID). Proc Natl Acad Chimpanzee fetal xxx°‘y and A globin gene nucleotide sequences
7