HGT networks

Introgression is the transfer of genetic material from one species to another via sexual reproduction, and this process has been recognized for a long time. If sex is not involved (such as between distantly related organisms) then we usually refer to it as horizontal gene transfer (HGT), and this has only relatively recently come to the general attention of biologists.

During the 1990s, HGT among prokaryotes began to be taken seriously in phylogenetics (Smith et al. 1992; Syvanen 1994), and more than a decade later also in eukaryotes (see Bock 2010; Boto 2010; Renner & Bellot 2012). However, the question still remains as to when it was first considered within phylogenetics, as opposed to other areas of biology.

It seems that the first report of what was probably HGT in prokaryotes is due to Flu (1927), who of course did not recognize it as such. Indeed, Lederberg & Tatum (1946) also apparently observed HGT, but mistakenly attributed it to sexual recombination (in prokaryotes). This emphasizes just how difficult it can be to identify processes from looking at data patterns.

Further observations were reported by Freeman (1951) and Lederberg et al. (1951). Shortly afterwards, experimental work was published concerning mechanisms for the transfer of genetic material between micro-organisms via what we now call transduction (Zinder & Lederberg 1952; Stocker et al. 1953). The effect of this on phylogenetics was soon considered (Stocker 1955), although no diagrams representing reticulation were presented at this time. The focus was still on elucidating the processes rather than illustrating the phylogenies.

It seems that the first people to actually illustrate HGT among species were Jones & Sneath (1970). In their review of HGT, they not only considered the accumulating evidence for the processes, they explicitly illustrated all of the known cases. These were presented as a series of 18 unrooted phenetic diagrams with known HGT connections linking the bacterial taxa. A single example is shown here.

For eukaryotes, the possibility was early on considered that the asexual transfer of genetic units may be of more general occurrence (Ravin 1955). Indeed, Went (1971) presented a strong case for HGT among plants, based on morphological and anatomical data (ie. phenotypic rather than genotypic evidence). Benveniste & Todaro (1974) then suggested the possibility of exogenously acquired viral genes in mammals. However, it was not really until molecular sequencing became available in the 1980s that biologists really started presenting evidence for gene transfer among eukaryotes (Shilo & Weinberg 1981; Singh et al. 1981; Buslinger et al. 1982; Hyldig-Nielson et al. 1982; Engels 1983).

Most of these suggestions turned out to be spurious, once more evidence accumulated (Smith et al. 1992; Syvanen 1994). However, this did not stop Syvanen (1987) from explicitly considering the effect of HGT on the assessment of evolutionary relationships, apparently being the first to do so. Interestingly, he concluded that "horizontal gene flow would not necessarily preclude a linear molecular clock or change the rate of molecular evolution (assuming the neutral allele theory)."

References

Benveniste RE, Todaro GJ (1974) Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature 252: 456-459.

Bock R (2010) The give-and-take of DNA: horizontal gene transfer in plants. Trends in Plant Science 15: 11-22.

Boto L (2010) Horizontal gene transfer in evolution: facts and challenges. Proceedings of the Royal Society of London B: Biological Sciences 277: 819-827.

Busslinger M, Rusconi S, Birnstiel ML (1982) An unusual evolutionary behaviour of a sea urchin histone gene cluster. EMBO Journal 1: 27-33.

Engels WR (1983) The P family of transposable elements in Drosophila. Annual Review of Genetics 17: 315-344.

Flu P-C (1927) Sur la nature du bactériophage. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 96(1): 1148-1149.

Freeman VJ (1951) Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. Journal of Bacteriology 61: 675-688.

Hyldig-Nielson, JJ, Jensen EØ, Paludan K, Wiburg O, Garrett R, Jørgensen P, Marcker KA (1982) The prnmary structures of two lehemoglobin genes from soybean. Nucleic Acids Research 10: 689-701.

Jones D, Sneath PH (1970) Genetic transfer and bacterial taxonomy. Bacteriology Reviews 34: 40-81.

Lederberg J, Lederberg EM, Zinder ND, Lively ER (1951) Recombination analysis of bacterial heredity. Cold Spring Harbor Symposium on Quantitative Biology 16: 413-443.

Lederberg J, Tatum EL (1946) Gene recombination in Escherichia coli. Nature 158: 558.

Ravin AW (1955) Infection by viruses and genes. American Scientist 43: 468-478.

Renner SS, Bellot S (2012) Horizontal gene transfer in eukaryotes: fungi-to-plant and plant-to-plant transfers of organellar DNA. Advances in Photosynthesis and Respiration 35: 223-235.

Shilo BZ, Weinberg RA (1981) DNA sequences homologous to vertebrate oncogenes are conserved in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 78: 6789-6792.

Singh L, Purdom IF, Jones KW (1981) Conserved sex chromosome-associated nucleotide sequences in eukaryotes. Cold Spring Harbor Symposium on Quantitative Biology 45: 805-813.

Smith MW, Feng D-F, Doolittle RF (1992) Evolution by acquisition: the case for horizontal gene transfers. Trends in Biochemical Science 17: 489-493.

Stocker BAD (1955) Bacteriophage and bacterial classification. Journal of General Microbiology 12: 375-379.

Stocker BAD, Zinder ND, Lederberg J (1953) Transduction of flagellar characters in Salmonella. Journal of General Microbiology 9: 410-433.

Syvanen M (1987) Molecular clocks and evolutionary relationships: possible distortions due to horizontal gene flow. Journal of Molecular Evolution 26: 16-23.

Syvanen M (1994) Horizontal gene transfer: evidence and possible consequences. Annual Review of Genetics 28: 237-261.

Went FW (1971) Parallel evolution. Taxon 20: 197-226.

Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. Journal of Bacteriology 64: 679-699.