Monday, August 13, 2012

Who published the first phylogenetic tree?

It is usually acknowledged that Jean-Baptiste Pierre Antoine de Monet, Chevalier de Lamarck (1744-1829), published an early evolutionary tree (Lamarck 1809). However, his published trees differ from our modern phylogenetic diagrams in having contemporary higher-level taxonomic groups at both the internal and external nodes, so that each tree represents a transformation series among the taxonomic groups. Thus, while his trees were based on the idea of transmutation, they do not match our current type of tree.

The later published trees of, for example, Charles-Hélion de Barbançois, Hugh Edwin Strickland, and Alfred Russel Wallace, followed the style of Lamarck. Other trees published in the first half of the 19th century, such as those of Jean Louis Rodolphe Agassiz, Augustin Augier, Heinrich Georg Bronn, and Edward Hitchcock, were not intended to be evolutionary diagrams, because their authors did not believe in evolution (Ragan 2009; Tassy 2011).

Charles Darwin (1859) is usually credited as being the originator of modern phylogenetic trees, with contemporary taxa at the leaves and ancestors at the internal nodes. Therefore, an answer to the question posed in the title must involve a post-Darwinian person. There appear to be four candidates for who published the first empirical Darwinian tree, in the period 1865-1866, two of them palaeontologists and two comparative morphologists, two with strong religious beliefs and two apparently without, and including one Englishman, one Frenchman and two Germans. I list them here in the probable order of publication.

St George Jackson Mivart (1827-1900)

St George Mivart was a comparative morphologist who was an early British convert to Darwinism, although he later fell out with Thomas Henry Huxley and therefore with Darwin. His work was principally on the comparative anatomy of primates, for which he provided very detailed comparisons of the skeletons of a large number of species, notably in Mivart (1865) and Mivart (1867).

The paper by Mivart (1865) therefore seems to be the first publication to contain an explicitly Darwinian tree. This is ironic, given the fact that Mivart later became one of Darwin's strongest critics. That it took 6 years (from 1859) for a biologist to produce such a tree may reflect the fact that Darwin himself published only a single theoretical sketch, thus leaving others to work out how to apply his ideas to empirical data.

The 1865 paper was read before the Zoological Society of London on 27 June 1865, and then appeared as a regular part of the Society's journal later that year (see Dickinson 2005). It was based on a detailed osteological analysis of the spinal columns of 29 primate genera. As noted by Bigoni & Barsanti (2011): "Not only does he use taxonomic names still largely in use today, but, surprisingly, Homo is not the apex or culmination of evolution ..., in fact it is placed on a lateral diverging branch. This position of humans provides his tree with a particularly modern appearance and is perfectly consistent with the trees or bushes that Darwin drew." Mivart's paper is available from the publishers John Wiley & Sons and also the Biodiversity Heritage Library.

Unfortunately, Mivart's tree does deviate from Darwin's ideas in that the leaves and many of the branches refer to higher taxonomic groups, rather than to species. In this sense his trees look similar to Ernst Haeckel's (see below), although it is doubtful that they were constructed in the same way. Note that Mivart's labels occur along the terminal twigs, rather than at their end, as his contemporaries chose to present them (and as we do today).

Also, being based on different data sets, the 1867 tree (based on the appendicular skeleton, or limbs) does differ in topology from the 1865 one (based on the axial skeleton, or spinal column), thus foreshadowing a problem with phylogeny reconstruction from different data sources that continues to this day (see this later blog post). Mivart explicitly noted in a letter to Darwin (1870): "The diagram in the Pro. Z. Soc. expresses what I believe to be the degree of resemblance as regards the spinal column only. The diagram in the Phil. Trans. expresses what I believe to be the degree of resemblance as regards the appendicular skeleton only" (Darwin Correspondence Project letter 7170). Indeed, in the 1865 paper Mivart also noted that the data for the spinal column "lead to an arrangement of groups and an interpretation of affinities somewhat differing from, yet in part agreeing with, the classification founded on cranial and dental characters".

Mivart's work is discussed in detail by Bigoni & Barsanti (2011). Mivart's views on evolution and theology are presented in Mivart (1871).

From Mivart (1865) p. 592. Click to enlarge.
From Mivart (1867) p. 425. Click to enlarge.

Franz Martin Hilgendorf (1839-1904)

Franz Hilgendorf was a palaeontologist, among other zoological pursuits, although he is relatively unknown today. He was one of the first Germans to accept Darwin's ideas (Reif 1986), and he is also credited with being the first to introduce evolutionary theory into Japan (c. 1873) (Yajima 2007). He could also have been the first to publish a Darwinian tree, but he did not actually do it.

Hilgendorf's PhD work was on the fossil gastropods of the middle Miocene basin at Steinheim, in southern Germany, which he visited in 1862. He studied the morphological variation, in the different stratigraphic layers, of the various fossil forms of what he referred to as Planorbis multiformis. The resulting thesis (Hilgendorf 1863) was passed in April 1863 but was otherwise unpublished, and it apparently contained no images. Nevertheless, Hilgendorf discussed in detail the relationship between a complete stratigraphic series of fossils and Darwin's evolutionary ideas, concluding that the Planorbis fossils could be arranged in a phyletic tree; and Reif (1983) found that Hilgendorf's notes did, indeed, contain a preliminary phylogenetic diagram. Reif (1983) presents a version of this phylogeny based on Hilgendorf's notes, which is also reproduced by Janz (1999).

Hilgendorf may thus have been the first to produce a Darwinian tree, even though he did not publish it. His ideas were Darwinian by including ancestral and descendant forms, splitting of lineages, and gradual transition between forms, with the ancestral taxa being varieties, not higher taxa. Interestingly, in the thesis Hilgendorf also raised the possibility that two of the lineages may have fused. He noted: "This does not fit the nice picture of a tree with many branches that Darwin presented to illustrate the descent of species — the branches of a tree never fuse again" [translation taken from Janz 1999].

Hilgendorf then made another excursion to the Steinheim basin in 1865, and wrote up the results for publication, this time with an explicit tree showing the relationship between the 19 different fossil forms that he recognized. This was read as a paper before the Royal Prussian Academy of Sciences on 19 July 1866, and was apparently published simultaneously as an offprint (Hilgendorf 1866). The paper then appeared as a regular part of the Academy's journal (Hilgendorf 1867) — these two versions are evidently identical save only the absence of the subtitle in the latter [which translates as "an example of morphological change through time"]. This is thus Hilgendorf's first published Darwinian tree.

There are actually two versions of the tree in the paper, as shown here, taken from the Biodiversity Heritage Library. The first tree emphasizes which stratigraphic layers each morphological form occupies (there are ten layers), whereas the second tree emphasizes the forms themselves. There is no suggestion of lineage fusion in either tree.

Hilgendorf's work is discussed in detail by Reif (1983), and more generally by Janz (1999).

From Hilgendorf (1867) p. 479. Click to enlarge.
From Hilgendorf (1867) after p. 502. Click to enlarge.

Jean Albert Gaudry (1827-1908)

Albert Gaudry was a palaeontologist who was one of the very few French scientists to promote Darwinian evolution. Indeed, Darwin noted in a letter to Jean Louis Armand de Quatrefages de Bréau (1870): "It is curious how nationality influences opinion: a week hardly passes without my hearing of some naturalist in Germany who supports my views, & often puts an exaggerated value on my works; whilst in France I have not heard of a single zoologist except M[onsieur] Gaudry (and he only partially) who supports my views" (APS 379; An Annotated Calendar of the Letters of Charles Darwin in the Library of the American Philosophical Society 1799-1882, p. 212).

The paper by Gaudry (1866) was a separately paginated offprint of the second chapter of part 1 (pp. 325-370) of a larger work about the fossil mammals from the late Miocene locality of Pikermi in Attica, in Greece, which was completed in 1867 (Animaux Fossiles et Géologie de l’Attique d’après les recherches faites en 1855–56 et en 1860 sous les auspices de l’Académie des sciences). In this offprint Gaudry expressed his views on palaeontology and evolution. He noted that the Pikermi fossils showed characteristics of two or more groups of animals, so that he could see the passage from order to order, family to family, genus to genus, and species to species in these intermediate forms.

He included five trees showing the relationships among different groups of extant and extinct fossil mammals, within a stratigraphic framework. The pictures shown here are taken from Google Books. I do not know exactly when this offprint was published, but Darwin acknowledged on 17 September 1866 that he received it "some time ago", so that it might pre-date Hilgendorf's own offprint.

As emphasized by Tassy (2006, 2011), Gaudry's trees were Darwinian by including ancestral and descendant species, splitting, gradualism and extinction, with the ancestral taxa being species or sub-species, not higher taxa. However, Gaudry did not fully embrace Darwinism, for religious reasons. As Darwin noted in a letter to Gaudry thanking him for a copy of the 1866 offprint: "I will venture to make one little criticism, namely that you do not fully understand what I mean by 'the struggle for existence', or concurrence vitale; but this is of little importance as you do not at all accept my views on the means by which species have been modified." (Darwin Correspondence Project letter 5213). Gaudry attributed evolutionary change to God, rather than to natural selection, as indicated in the closing sentence of his 1866 work: "Mais, nous n'eu douterons pas, l'artiste qui pétrissait était le Créateur lui-même, car chaque transformation a porté un reflet de sa beauté infinite."

Gaudry's work is discussed in detail by Tassy (2006), if you read French, and more briefly by Tassy (2011), if you do not.

From Gaudry (1866) p. 36. Click to enlarge.
From Gaudry (1866) p. 38. Click to enlarge.
From Gaudry (1866) p. 41. Click to enlarge.
From Gaudry (1866) p. 44. Click to enlarge.
From Gaudry (1866) p. 46. Click to enlarge.

Ernst Heinrich Philipp August Haeckel (1834-1919)

Ernst Haeckel is best known today as a comparative morphologist, but he was also an important popularizer of science, as well as a brilliant artist. He was an early German convert to Darwinism, and it has been noted that "more people by the turn of the century had learned of evolutionary theory through Haeckel's depictions than even from Darwin's own writings" (Richards 2011).

Haeckel actually coined the word "phylogeny" (along with many others, including "ontogeny" and "ecology"), and his first phylogenetic trees were published in the second volume of his two-volume opus about animal morphology (Haeckel 1866). Haeckel had the ambitious plan to reform the study of morphology, by synthesizing Darwin's ideas on genealogical descent with the transformational evolutionism of Lamarck, along with the German tradition of naturphilosophie (represented by Johann Wolfgang von Goethe). As noted by Hopwood (2006), for Haeckel: "evolution was the organizing principle of a cosmic synthesis that would unify science, religion, and art on a biological foundation."

There were eight trees in the book, showing the relationships between animals, plants and (for the first time) protists, and within plants and different animal groups. Haeckel used morphology to reconstruct the phylogenetic history of animals, and in the absence of fossils used embryology as evidence of ancestors. The pictures here are taken from the Biodiversity Heritage Library. These are frequently credited as being the first phylogenetic trees published, although Mivart, at least, published earlier. Haeckel claimed to have started the book "several years" before 1864, which is when he apparently started work on the phylogenetic trees (as he mentions in a letter to Darwin), but the Foreword is dated 14 September 1866.

Unfortunately, Haeckel's tree-construction method seems to have owed more to Lamarck than to Darwin (see Dayrat 2003), with the branches indicating morphological transformation among the named groups rather than strictly representing genealogy. Moreover, the trees show higher taxonomic groups at the internal branches, while Darwin treated them as representing extinct species. Thus, it is not clear just how Darwinian Haeckel really was. Indeed, Di Gregorio (2005) has noted: "Haeckel's view of evolution (or rather evolutionism) ..., from the very beginning, reminds one more of Jean-Baptiste Lamarck than Darwin."

One intriguing detail about Haeckel's early trees is that many, if not most, of the labels occur in the spaces between the terminal twigs, like seeds enclosed within a fruit. All of the trees shown above distinctly label the leaves, even though it it likely that their presentation format was derived independently of each other. Haeckel, on the other hand, appears to be much more vague about exactly what is being labelled. Perhaps this is a by-product of the fact that his images are distinctly tree-like in form, rather than being stick figures; or perhaps it comes from the rather speculative nature of many of the relationships proposed (the trees of Mivart, Hilgendorf and Gaudry were based on detailed empirical data, whereas Haeckel's were much more ambitiously hypothetical).

It is perhaps also worth noting that Haeckel first publicly endorsed Darwin's theory in his work on the Radiolaria (Haeckel 1862). On page 234 of that work (see the Biodiversity Heritage Library) he produced what he called a "Verwandtschaftstabelle der Familien, Subfamilien und Gattungen der Radiolarien", which is thus his first attempt at a genealogical diagram. It was not drawn as a tree, and is thus somewhat hard to interpret, but in the same chapter he discussed ancestral and transitional forms, and on pages 231–232 he made clear that he was attempting to implement Darwin's ideas.

Heackel's life and work are discussed in detail by Di Gregorio (2005) and Richards (2008).

From Haeckel (1866) Taf. I. Click to enlarge.
From Haeckel (1866) Taf. II. Click to enlarge.
From Haeckel (1866) Taf. III. Click to enlarge.
From Haeckel (1866) Taf. IV. Click to enlarge.
From Haeckel (1866) Taf. V. Click to enlarge.
From Haeckel (1866) Taf. VI. Click to enlarge.
From Haeckel (1866) Taf. VII. Click to enlarge.
From Haeckel (1866) Taf. VIII. Click to enlarge.


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