Who first used the term "phylogenetic network"?

In a previous blog post (Ngrams and phylogenetics) I noted that Google Books first detects the use of the term "phylogenetic network" in the late 1970s. However, the history of the use (and meaning) of this expression is actually rather confused.

Sadly, none of the early uses of the term actually referred to a reticulating network — they all referred to a non-reticulated tree. Indeed, the very first illustrations of phylogenetic networks (way back in the 1700s) were actually described as trees: “arbre généalogique” (French: family tree). (NB. This terminology is quite natural, because a family pedigree is actually a network when both parents are included from each generation — each offspring is then a hybrid of two parents.)

Grant (1953) came close to modern usage when he used the expression "phylogenetic net" to refer to what we would now call a "hybridization network" in his study of the plant genus Gilia:

The occurrence of sporadic hybridizations during the course of Angiosperm evolution may be the factor which has caused this group to grow up, not as a phylogenetic tree, but as a gigantic, snarled phylogenetic net.

He illustrated this with a rather reticulate genealogy.

Unfortunately, Holmquist (1978) then muddied the water by using the expression "phylogenetic network" to refer to an abstract phylogenetic tree. Although not explicit, he used "tree" to refer to a rooted phylogenetic diagram and "network" to refer to the unrooted topology of the tree. This is very similar to the use of the term "network" in cladistics, as discussed in an earlier blog post (Some odd network definitions and terms). (NB. The cladistic idea was that an unrooted tree represents a set of rooted trees, one potential root per edge in the tree.)

Throughout the 1980s there were a number of literature uses of "phylogenetic network" that were a reference to Holmquist's paper, although the usage seems to have died out after that. There were also other references to unrooted trees as "networks", but the term "unrooted tree" finally became universal, instead of "network".

Avise et al. (1979a,b) then used the term "phylogenetic network" to refer to what is now called a "haplotype network". They manually created unrooted haplotype graphs by combining several gene networks. However, while there could be reticulations in the individual gene networks, the combined haplotype data had no reticulations, and they thus formed non-reticulate trees.

Throughout the 1980s there were a number of literature uses of "phylogenetic network" that were a reference to this work, although most people actually referred to the paper by Lansman et al. (1983), since this contained a detailed description of the manual technique. It seems to be Excoffier & Smouse (1994) who first generalized haplotype trees to networks, but they did not call them "phylogenetic networks". (NB. They used the union of all minimum spanning trees as a minimum spanning network.)

Finally, it was Bandelt (1994) who formalized the reference to unrooted splits graphs as "phylogenetic networks"; previously, these had been simply called "splits graphs". This use of the term "phylogenetic" does not refer to genealogies, of course, since the graphs are unrooted and thus have no time dimension.

Thus, before the 1990s the term "phylogenetic network" was actually used to refer to various forms of unrooted tree. During that decade the concept was explicitly generalized from trees to unrooted reticulate networks. Only Verne Grant was referring to a rooted genealogy, and he preferred to use the term "net" rather than "network".

That leaves open the question of who first used the expression "phylogenetic network" explicitly in reference to a genealogy.

References

Avise JC, Giblin-Davidson C, Laerm J, Patton JC, Lansman RA (1979 Dec) Mitochondrial DNA clones and matriarchal phylogeny within and among geographic populations of the pocket gopher, Geomys pinetis. Proceedings of the National Academy of Sciences of the United States of America 76(12): 6694-6698.

Avise JC, Lansman RA, Shade RO (1979 May) The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. I. Population structure and evolution in the genus Peromyscus. Genetics 92: 279-295.

Bandelt H-J (1994) Phylogenetic networks. Verhandlungen des Naturwissenschaftlichen Vereins Hamburg 34: 51-71.

Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136: 343-359.

Grant V (1953) The role of hybridization in the evolution of the leafy-stemmed gillias. Evolution 7: 51-64.

Holmquist R (1978) A measure of the denseness of a phylogenetic network. Journal of Molecular Evolution 11: 225-231.

Lansman RA, Avise JC, Aquadro CF, Shapira JF, Daniel SW (1983) Extensive genetic variation in mitochondrial DNA's among geographic populations of the deer mouse, Peromyscus maniculatus. Evolution 37: 1-16.