Cleopatra, ambition and family networks

There is an old saying in English that "Behind every great man there is a woman ... telling him to be great". This is intended to indicate that even in patrilineal societies women have influenced history, even if history has chosen not to formally recognize them (or historians have, anyway). However, every so often a woman has also stepped into the spotlight for herself, and recognizably influenced events in a way that has brought her name down through history.

The most famous of these is probably Cleopatra (or more properly Kleopatra), the last ruler of Ancient Egypt (as Cleopatra VII). Sadly, her ambition to become Empress of the known world seems to have destroyed two successive Roman rulers (Julius Caesar and Marc Antony) as well as her own two brothers (who would have ruled in her place); and her failure seems to have lost the country of which she was queen, so that Egypt became a Roman dependency. She ruled from 51-30 BCE, and modern Egypt did not regain its independence until 1953. This was one seriously influential woman.

As noted by Schiff (2010):

She lost her kingdom once; regained it; nearly lost it again; amassed an empire; lost it all. At the height of her power she controlled virtually the entire eastern Mediterranean coast, the last great kingdom of any Egyptian ruler. For a fleeting moment she held the fate of the Western world in her hands ... Catastrophe reliably cements a reputation, and Cleopatra's end was sudden and sensational.

Her interest to us, however, is her role in a dynasty that favored incest, and thus had a "family tree" that was a hybridization network, as shown in the figure. This particular family history is rather complex. Note that Cleopatra herself had at least four liaisons, two with her brothers (who successively ruled jointly with her as Ptolemy XIII and Ptolemy XIV, respectively) and two with Romans (Julius Caesar and Marc Anthony). Later, she also ruled jointly with her son by Julius Caesar (as Ptolemy XV).

Adapted from the Too Much Information blog, based on the information at Ian Mladjov's Genealogical Tables

The Ptolemaic dynasty was founded after the death of Alexander the Great (aka Alexander III of Macedon), when his empire was divided up among his Greek generals, and in 323 BCE Egypt ended up in the hands of Ptolemy, who subsequently ruled as the pharaoh Ptolemy I from 305-282 BCE. As Dray (2012) has noted:

His daughter, Arsinoe II, would start the tradition of incest. Married off to an old King of Thrace when she was still a teenager, she was the ultimate survivor. Her life was frequently in danger and she made many narrow escapes ... At some point, Arsinoe seems to have decided that if she wanted to be safe, she couldn’t trust anyone outside her immediate family. So, she returned to Egypt and married her full brother, Ptolemy II.

Now, the Greeks didn’t have a tradition of incest in their ruling families … but the pharaohs of Egypt did. By marrying her brother, Arsinoe was able to help create a link between the new Ptolemaic dynasty and the very old traditions of the native Egyptians. It served her extremely well as she became the first female pharaoh of the Ptolemaic dynasty, ruling not just as the wife of the king, but as a king in her own right.

Meeg (2009) suggests that:

According to tradition, incestuous marriages between the pharaohs and their sisters were common. If this was the case, it could have been done to emulate the god Osiris and his sister / wife the goddess Isis (the product of that union was Horus, the alleged ancestor of the Pharaoh), and/or to keep the sacred bloodline pure. When Alexander the Great's general Ptolemy seized control of Egypt around 323 BC, his descendants would continue the local custom of pharaonic brother-sister marriages. This practice was unknown among Greeks and Macedonians.

Indeed, Wikipedia notes:

In ancient Egypt, royal women carried the bloodlines and so it was advantageous for a pharaoh to marry his sister or half-sister; in such cases a special combination between endogamy and polygamy is found. Normally the old ruler's eldest son and daughter (who could be either siblings or half-siblings) became the new rulers. All rulers of the Ptolemaic dynasty from Ptolemy II were married to their brothers and sisters, so as to keep the Ptolemaic blood "pure" and to strengthen the line of succession. Cleopatra VII (also called Cleopatra VI) and Ptolemy XIII, who married and became co-rulers of ancient Egypt following their father's death, are the most widely known example.

Bevan (1927) continues the story [Note: he uses one number less for the Cleopatras and Ptolemies]:

Cleopatra VI found herself queen of Egypt at the age of seventeen or eighteen. By the custom of the house, and according to the will and testament of Ptolemy Auletes, the elder of her two brothers, then only nine or ten, was associated with her, as king (Ptolemy XII). They probably had, as a pair, the style of "Father-loving Gods" (Theoi Philopatores), though neither during the reign of Cleopatra with Ptolemy XII, nor during her reign, later on, with the younger brother, Ptolemy XIII (then about twelve), do the coins bear any head or name but that of the queen, and in Egyptian sepulchral inscriptions put up during the reign of Cleopatra with her younger brother (regnal years 5, 6, and 7 of Cleopatra) the regnal year of the boy-king is ignored. Ptolemy XIV was the acknowledged son of Julius Caesar and Cleopatra, and ruled as child king with his mother.

The involvement of royalty in consanguinity and incest is widespread. As noted by Dobbs (2010):

While virtually every culture in recorded history has held sibling or parent-child couplings taboo, royalty have been exempted in many societies, including ancient Egypt, Inca Peru, and, at times, Central Africa, Mexico, and Thailand [and also Hawaii].

I have already discussed incest in the family "trees" of the Egyptian 18th Dynasty, in Tutankhamun and extreme consanguinity (the other set of pharaohs where this was common); and I have covered the persistent inbreeding in the downfall of the modern Spanish branch of the Habsburgs, in Family trees, pedigrees and hybridization networks.

Not unexpectedly, this phenomenon has received attention from modern evolutionary biologists. Conventionally, the evolutionary advantage of sexual over non-sexual reproduction is considered to be the creation of genetic diversity through heterozygosity. Inbreeding, by reducing heterozygosity, then seems to negate the advantages of sexual reproduction. So, the near universality of incest avoidance in humans has a clear genetic dimension. Indeed, as I have noted in previous blog posts this is easily demonstrated in well-known families — (i) Charles Darwin's family pedigree network, (ii) Toulouse-Lautrec: family trees and networks.

The presence of incest among royal families then requires biological explanation. Indeed, van den Berghe & Mesher (1980) have provided one:

Royal incest (mostly brother-sister; less commonly father-daughter) represents the logical extreme of hypergyny. Women in stratified societies maximize [evolutionary] fitness by marrying up; the higher the status of a woman, the narrower her range of prospective husbands. This leads to a direct association between high status and inbreeding. Royal incest is a fitness maximizing strategy if the following conditions are met: polygyny, patrilineal succession, and parental control of royal succession. Under those conditions, the genetic risks of close inbreeding are more than accounted for by the production of a highly related male heir who has, himself, access to a large harem. Data from Ancient Egypt, Inca Peru, Hawaii, Thailand, Monomotapa, Bunyoro, Ankole, Buganda, Shilluk, Zande, Nyanga and Dahomey confirm hypotheses derived from the sociobiological paradigm of inclusive fitness.

Finally, to return to Cleopatra, she is usually credited with being fatally attractive due to her great beauty. However, there is no evidence that this was actually the case. Her attractiveness to men seems to have come much more from a strong personality, including determined diplomacy and an easy facility with languages. Also, her ancestors were Macedonian Greeks, rather than native Egyptians, giving her a stronger genetic and cultural tie to Europe rather than to Africa, which must have helped when trying to woo the rulers of the Roman Empire. It was this ancestry that the dynasty's consanguinity and incest were intended to protect. The Egyptian populace certainly didn't benefit from it.

Indeed, Cleopatra seems simply to have been the ultimate expression of her dynasty's heritage, as noted by Ager (2006):

royal incest, as practised by the Ptolemies, was only one of a larger set of behaviours, all of which were symbolic of power, and all of which were characterized by lavishness, immoderation, excess and the breaching of limits in general.

Interestingly, the potentially negative aspects of inbreeding seem not to have affected this dynasty — there is no convincing evidence of infertility, infant mortality or genetic defects, for example (Ager 2006). Instead, their main historical legacy has been their bizarre juxtaposition of either marrying each other or murdering each other, and sometimes both. Cleopatra's activities in this regard were no different to those of her ancestors.

References

Ager SL (2006) The power of excess: royal incest and the Ptolemaic dynasty. Anthropologica 48: 165-186.

Bevan ER (1927) The House of Ptolemy. Methuen Publishing, London.

Dobbs D (2010) The risks and rewards of royal incest. National Geographic Magazine.

Dray S (2012) Keeping it in the (Ptolemaic) family: when incest is best.

Meeg (2009) Royal inbreeding in Ancient Egypt.

Ian Mladjov's Genealogical Tables — The Ptolemies, kings of Egypt.

Schiff S (2010) Cleopatra: a biography. Little, Brown and Co, New York. [excerpted in Smithsonian Magazine]

van den Berghe PL, Mesher GM (1980) Royal incest and inclusive fitness. American Ethnologist 7: 300-317.

Wikipedia. Inbreeding.

Candy Crush network

King Digital, the creators of the popular smartphone game Candy Crush Saga were listed on the New York Stock Exchange two days after this game was shown to be NP-hard [1]. Could these two events be somehow related? Anyway, although the King Digital shares are not doing well, the NP-hardness proof still stands. A different NP-hardness proof for Candy Crush actually appeared on the arXiv a few weeks earlier [2], but was based on rules that are slightly different from the usual rules of Candy Crush.

So what is Candy Crush? It is a smartphone / tablet game having a rectangular board filled with different types of candies. A player can score points by swapping two adjacent candies in order to match three or more candies of the same type. This seems to be even more addictive than eating candies, which made the game the most popular game of Facebook, and led to a 568 million dollar profit for King Digital in 2013.

Interestingly, Candy Crush Saga is one of a large family of games that are all based on matching objects. These games all seem to be closely related. Moreover, their genealogy is not tree-like at all, as shown below. Many modern games have been derived by combining ideas from different older games. In other words, the genealogy of such games can best be described by a phylogenetic network.

A phylogenetic network for Bejeweled-type games, taken from [1], which was in turn taken (after modification) from [3].

This network is clearly a rooted, genealogical phylogenetic network (although it does not have a unique root).

So what does the NP-hardness of Candy Crush tell us? Nothing, of course, except that the 97 million people daily playing Candy Crush are pouring all their energy into solving a frivolous, but nevertheless intrinsically hard, problem. This is a pity because, since Candy Crush is NP-hard, one can (at least in theory) encode any NP-complete problem as a Candy Crush episode. This could be used to let all these 97 million people solve more useful NP-complete problems every day. For example, we could encode massive phylogenetic network reconstruction problems as Candy Crush episodes, and use this to construct the Web of Life in a few days!

References

[1] Luciano Gualà, Stefano Leucci, Emanuele Natale. Bejeweled, Candy Crush and other match-three games are (NP-)hard, http://arxiv.org/abs/1403.5830 (24 March 2014)

[2] Toby Walsh. Candy Crush is NP-hard, http://arxiv.org/abs/1403.1911 (8 March 2014)

[3] Jesper Juul. A casual revolution: reinventing video games and their players. The MIT Press, 2012.


Later note:
It turns out that the figure shown above is not actually taken from [3], in spite of the claim made in [1]. The figure in [3] is re-drawn from [4], and the genealogy as shown in [1] is edited directly from [4], not [3]. The editing consists of deleting all of the many other descendants of Tetris. The original complete figure is available here.

[4] Jesper Juul. Swap adjacent gems to make sets of three: a history of matching tile games. Artifact 1: 205-216, 2007.

Tutankhamun and extreme consanguinity

Consanguineous relationships involve people who are first cousins or more closely related. Apparently, about 15 percent of all marriages worldwide involve consanguineous partners, although this number has been higher in the past (Bittles 2012).

Our interest for this blog is that such relationships emphasize that so-called family trees (pedigrees) are hybridization networks not trees (see Pedigrees and phylogenies are networks not trees). Everyone can trace their maternal and paternal ancestors back into the past to a point where the lineages fuse again, and consanguineous marriages mean that this happens in the recent past rather than the distant past. To this end, we have had posts about Charles Darwin (Charles Darwin's family pedigree network), Henri Toulouse-Lautrec (Toulouse-Lautrec: family trees and networks) and Albert Einstein (Albert Einstein's consanguineous marriage). Not unexpectedly, it is royalty that provide the best-known examples (see Family trees, pedigrees and hybridization networks).

However, many cultures have taken consanguinity even further, as noted by Dobbs (2010):

While virtually every culture in recorded history has held sibling or parent-child couplings taboo, royalty have been exempted in many societies, including ancient Egypt, Inca Peru, and, at times, Central Africa, Mexico, and Thailand [and also Hawaii].

The reference to ancient Egypt includes both Cleopatra and Tutankhamun, each of whom was part of a dynasty that apparently adopted the practice of incest. As noted by Wikipedia:

In ancient Egypt, royal women carried the bloodlines and so it was advantageous for a pharaoh to marry his sister or half-sister; in such cases a special combination between endogamy and polygamy is found. Normally the old ruler's eldest son and daughter (who could be either siblings or half-siblings) became the new rulers.

Tutankhamun

Tutankhamun briefly ruled as Pharaoh from 1333-1323 BCE, at the end of the Amarna period, the 18th Dynasty. His failure to leave an heir ended the direct line of succession, and ultimately resulted in the transition to the 19th Dynasty, started by Rameses I. Tutankhamun seems to have been a rather minor king, becoming ruler at age 9 and dying at 19. He was surrounded by the power struggle that resulted from his father's attempt to found the first monotheistic religion, and being a minor he probably had little influence on the events of the time (Antanovskii 2013).

He became famous in 1922, when his near-intact tomb was discovered. He had been buried in a tomb not intended for royalty, and its location and even existence was quickly forgotten at the time — due to the political turmoil, his successors had deleted nearly all traces of the Amarna kings. In a classic case of irony, this situation made Tutankhamun's tomb safe from the robbers who removed much of the contents of other tombs in the Valley of Kings. Thus, more than 5,000 artifacts were found in his tomb, along with the well-preserved mummies (see the death mask pictured above). This has made Tutankhamun a better-known name ("King Tut") than that of anyone else from his period.

A note on names: Tutankhamun's father was Amenḥotep IV, who tried to replace the polytheistic worship associated with Amun (or Amen) and the other gods of the national pantheon with the monotheistic worship of Aten ("the disk of the sun"). He thus changed his name from Amenhotep ("Amun is satisfied") to Akhenaten ("beneficial to Aten"). His son was named Tutankhaten ("the living spirit of Aten"), but this was changed to Tutankhamun ("the living spirit of Amun") when the state religion was restored during his reign.

The history of the period surrounding Akhenaten and Tutankhamun is particularly confused, as Tutankhamun did not become pharaoh until 2 years after his father's death (Hawass 2010; Gabolde 2011). Nevertheless, the preservation of Tutankhamun's tomb has allowed us to reconstruct a possible genealogy for this period, as shown next.

Hawass et al. (2010) compared the DNA of the mummy of Tutankhamun with that of 10 royal mummies from the same period, ranging from 1,410 to 1,324 BCE. The mummy of the genetically identified father, found in grave No. 55 of the Valley of Kings, is considered to be Akhenaten. The identified mother, found in grave No. 35, was also identified to be the sister of Akhenaten. This is surprising, because only two wives of Akhenaten, Nefertiti and Kiya, are known to have had the title of Great Royal Wife, which the mother of the royal heir should bear.

Hawass et al. (2010) also looked for evidence of possible genetic effects of the consanguineous relationship (eg. homozygous genetic disorders):

An accumulation of malformations in Tutankhamun's family was evident. Several pathologies including Köhler disease II were diagnosed in Tutankhamun; none alone would have caused death. Genetic testing for genes specific for Plasmodium falciparum revealed indications of malaria tropica in four mummies, including Tutankhamun's. These results suggest avascular bone necrosis in conjunction with the malarial infection as the most likely cause of death in Tutankhamun. Walking impairment and malarial disease sustained by Tutankhamun is supported by the discovery of canes and an afterlife pharmacy in his tomb.

Incestuous marriages were nothing new to the pharaohs of Dynasty 18 (see Ian Mladjov's detailed genealogy). Part of the genealogy of its founding is shown in the next figure. Aahotep I and Sequenenra III were sister and brother, as were Aahmes-Nefertari and Aahmes (or Ahmose II). Aames (or Ahmose III) and Thotmes I were either sister and brother or half-siblings (the records are unclear).

Circles refer to females and squares to males.

Finally, it is worth noting that Marc Gabolde has an alternative explanation for the apparent genetic closeness of King Tutankhamun's parents (see Powell 2013). He suggests that Tutankhamun's mother was not his father's sister, but rather his father's first cousin, Nefertiti. The apparent genetic closeness is then not the result of a single brother-sister mating but due to three successive instances of marriage between first cousins. Nefertiti is recorded to have had six daughters with Akhenaten, but no son.

References

Antanovskii R (2013) Unmasking Tutankhamun : the figure behind the fame. Heritage Daily – Archaeology.

Bittles AH (2012) Consanguinity in Context. Cambridge University Press.

Dobbs D (2010) The risks and rewards of royal incest. National Geographic Magazine.

Gabolde M (2011) The end of the Amarna Period. BBC History – Ancient History in Depth.

Hawass Z (2010) King Tut's family secrets. National Geographic Magazine.

Hawass Z, et al. (2010) Ancestry and pathology in King Tutankhamun's family. Journal of the American Medical Association 303: 638-647.

Ian Mladjov's Genealogical Tables — The pharaohs of the New Kingdom in Egypt c. 1540-1070 BC.

Powell A (2013) A different take on Tut. Harvard Gazette.

Pedigrees and phylogenies are networks not trees

There is nothing in the etymology of the words 'genealogy' and 'phylogeny' that necessarily implies that they must be tree-like. Indeed, all genealogies are networks. For example, a human family "tree" is a tree only if it includes one sex alone. Otherwise, it must be a network when traced backwards from any single individual through both parents, because the lineages must eventually coalesce in a pair of shared common ancestors. This must happen if there is a single origin for Homo sapiens (ie. the species is monophyletic). The coalescence may not occur for thousands of years in the past, or it may be quite recent.

So, all pedigrees of sexually reproducing species involve conjoined lineages at both "ends", one in the common ancestor and one in the contemporary offspring.

Given the extent of inbreeding among royal families, this ancestral coalescence is quite likely to be recent among monarchs. For example, the most recent common ancestors of all of the currently reigning monarchs of Europe are John William Friso, Prince of Orange (1687-1711), and his wife, Marie Louise of Hesse-Kassel, Princess consort of Orange (1688-1765). This situation has existed since the abolition of the Albanian monarchy in 1939 (this particular monarchy was not related to the house of Orange).

Marie Louise (left) and her two children.

There used to be a Wikipedia page listing the contemporary descendants of this royal Dutch couple, but it has been deleted. It is, however, still available in the Internet Archive WayBack Machine (Royal descendants of John William Friso, Prince of Orange). This page shows that the lineages of all of the current monarchs coalesce in this couple in 7-11 generations. This is true of all 10 current monarchs (in Belgium, Denmark, Liechtenstein, Luxembourg, Monaco, the Netherlands, Norway, Spain, Sweden, the United Kingdom), many former monarchies (13 or so), many so-called pretenders or claimants (at least 21), plus two royal consorts. Interestingly, the progenitor couple achieved this set of family relationships even though they had only one daughter (Princess Amalia of Nassau-Dietz) and one son (William IV, Prince of Orange), who was born six weeks after his father's death by drowning.

Family trees were originally devised as a way for nobles to assert their nobility, by tracing their direct male ancestry from some "important" progenitor (see the picture below). The female lineages were usually ignored in such ancestries, with each woman appearing alone, solely as an isolated wife and mother. This was, of course, modelled on the genealogies listed in the christian Bible, in both Genesis 5 and 11, in which females are mentioned but only males appear to be named. However, the ancestral relationships of the current European monarchs do involve females as part of the direct lines of descent, in all cases (ie. none of the direct lines of descent can be traced solely through males).

On the left is part of a genealogy of Christ (from c. 1130-1205);
on the right is a genealogy of the House of Habsburg (c. 1540).
Reproduced from the Visual Complexity blog.

Thus, in the modern world, we should be constructing family networks not family trees, with all of the male and female lineages sharing equal prominence. This will make it clear that genealogies are networks not trees. This assumes, of course, that enough historical information can be collected to locate the actual points of coalescence. This is unlikely to be so for the likes of you and me, but the nobility seem to be able to do it quite regularly.

Family networks that reticulate within a few generations are not necessarily good things, of course. Sex-linked recessive traits such as heamophilia B are widespread among the royalty of Europe (Stevens 1999, Rogaev et al. 2009), as are autosomal dominant traits such as variegate porphyria (Cox et al. 2005). These diseases are much rarer amongst commoners.

A similar situation applies to phylogenies showing species relationships. If there is a single origin to life, then tracing phylogenies backwards in time must lead to the eventual coalescence of all lineages. Any species whose ancestry involves hybridization, introgression or horizontal gene transfer must form a network. Parts of this network might be tree-like if isolated from the rest, but the whole phylogeny cannot be anything other than a network.

Consider the following points:

Definitions:
A network is a series of overlapping groups
A tree is a set of nested groups

Observation:
Each evolutionary event defines a group (all of the descendants of the ancestor in which the event occurred)

Conclusions:
Dichotomous speciation leads to a tree, by definition
Other processes will lead to a network, by definition

We know that in biology there are both vertical (speciation) and horizontal (reticulation) evolutionary processes. Therefore, no biological data fit a tree perfectly (unless the data are carefully selected to do so). A network analysis will allow you to evaluate the relative contribution of the horizontal and vertical processes that have occurred.

References

Cox TM, Jack N, Lofthouse S, Watling J, Haines J, Warren MJ (2005) King George III and porphyria: an elemental hypothesis and investigation. Lancet 366: 332-335.

Rogaev EI, Grigorenko AP, Faskhutdinova G, Kittler ELW, Moliaka YK (2009) Genotype analysis identifies the cause of the "Royal Disease". Science 326: 817.

Stevens R. (1999) The history of hemophilia in the royal families of Europe.  British Journal of Haematology 105: 25-32.

Faux phylogenies II

It is possible to produce a phylogeny of any group of objects that vary in their intrinsic characteristics, and where those characteristics can be inferred to vary through time. I have previously reported some examples of a Tree of LIfe where "life" has been interpreted very broadly, to include legendary figures, cartoon animals, pokémon, and dragons (see Faux phylogenies). Here, I broaden the scope even further.

Phylogeny of taste

This first example comes from the July-August 1998 edition of the Annals of Improbable Research (vol. 4, no. 4), in which Joe Staton published an article entitled Tastes like chicken? It contains the following tetrapod phylogeny onto which has been mapped what they taste like. Note that Homo sapiens is included.

Phylogeny of breakfast

Following the taste theme, Nash Turley works on community phylogenetics, and this has lead him to contemplate the phylogenetics of his own breakfast. This vegetarian feast contains 15 species in 11 families.

Insect blog phylogenetics

Moving on to cultural evolution, Morgan Jackson has investigated how insect blogs are related to each other. His phylogenetic analysis of entomology blogs was based on blog morphology, physiology, geography, ecology and behaviour. It produced the following tree, onto which has been plotted the insect families concerned.

Evolution blog phylogenetics

In a similar vein, when the blogger known as Psi Wavefunction hosted the 20th Carnival of Evolution, this was summarized as a phylogenetic tree. The tree was produced by the simple expedient of aligning the URL addresses of the Carnival submissions and performing a parsimony analysis, based on treating the letters as amino acid codes. I can't believe that it worked.

Android bubble shooter games

Finally, Megafouna Software has produced a phylogeny of Android bubble shooter games, based on a small set of their features.

The dilemma of evolutionary networks and Darwinian trees

I have noted before that Franz Hilgendorf (1839-1904), a German palaeontologist, was apparently the first person to publish a Darwinian tree based on the fossil record, in 1866 (Who published the first phylogenetic tree?). Indeed, among the people who first produced trees inspired by Darwin's work, Hilgendorf seems to have been the only "real" Darwinian — St George Mivart later became a strong anti-Darwinist, Albert Gaudry accepted Darwin's genealogical ideas but rejected the idea of natural selection, and Ernst Haeckel was in practice more of a Lamarckian than a Darwinian. Hilgendorf, on the other hand, continued to pursue Darwinism throughout the rest of his career, even being the first to introduce evolutionary theory into Japan (c. 1873) .

What I wish to point out here is that he was also the first person to face what I will now christen "Hilgendorf's Dilemma", which is a problem that phylogenetics has faced ever since the publication of Darwin's book in 1859. Hilgendorf solved the problem in the same way that later phylogeneticists also did — it is only in the last 2-3 decades that a different solution has been widely adopted.

The problem is this: what do you do when your data are not tree-like but you accept the evolution-as-tree paradigm? The solution of choice has been: publish a tree anyway.

The history of phylogenetic metaphors

I have previously emphasized the important point that the earliest genealogical diagrams were networks, published in 1755 and 1766 by the Frenchmen Buffon and Duchesne, respectively (Networks of genealogy). However, genealogical diagrams were then mostly ignored for the next century, except by Lamarck — most published relationship diagrams were affinity networks rather than representing genealogy (see Affinity networks updated).

One of Darwin's main goals in 1859 was thus to re-introduce genealogy as being the most important relationship concept in biology. However, he chose the tree as his metaphor rather than the previously proposed network. This seems to have been a rhetorical device as much as anything else, alluding to the biblical Tree of Life (Hellström 2011, Penny 2011). Darwin succeeded in his goal, and genealogical trees have been the dominant metaphor since that time, rather than genealogical networks.

Franz Martin Hilgendorf

Hilgendorf knew and apparently accepted Darwin's ideas (Heinrich Bronn's German translation of the Origin had appeared in 1860), and he applied them to his PhD studies in 1862. He was investigating the fossil gastropods of the middle Miocene basin at Steinheim, in southern Germany. He studied the morphological variation, in the different stratigraphic layers, of the various fossil forms of what he referred to as Planorbis multiformis. Importantly, he recognized that the different morphological forms (which he called varieties) occurred exclusively in different stratigraphic layers. Thus, what he saw in the stratigraphy could be translated into a phylogenetic diagram, as shown in this next figure.

Adapted from Rasser (2013).

On the face of it, Hilgendorf's work provides strong support for Darwinism, and in his thesis (Hilgendorf 1863) he explicitly noted the relationship to Darwin's ideas. However, he did not include his phylogenetic diagram, and he did not publish his thesis. The 42-page thesis was hand-written, and he did not even leave a copy behind at the University of Tübingen. The only known copy (presumably the original) is now in the Museum für Naturkunde, Berlin, where Hilgendorf later worked, donated by Hilgendorf's heirs. It was discussed by Reif (1983), and has recently been transcribed by Glaubrecht (2012).

The usual explanation given for Hilgendorf's decision not to publish is the controversial nature of the subject of evolution (eg. Weltner 1906, Reif 1983, Janz 1999, Glaubrecht 2012), which was not even supported by his own supervisor (Friedrich von Quenstedt). However, it seems equally likely that the explanation was Hilgendorf's Dilemma.

Hilgendorf's Dilemma

Hilgendorf refers to this dilemma in the penultimate paragraph of his thesis. After discussing the Darwinian ideas that species are connected with each other through intermediate stages, and have evolved apart over time, he says:

Eine Beobachtung die, so viel ich weiß, mit den bisher aufgestellten Ansichten nicht stimmt, [wäre], daß früher getrennte Arten sich einander nähern und endlich miteinander Verschmelzen können. Darauf würde das schöne Bild, das Darwin uns vom Zusammenhange der Species in einem Zweige=reichen Baume vorführt, nicht passen; die Zweige eines Baumes wachsen nicht wieder zusammen.

An observation which, as far as I know, contradicts these previously discussed views, [would be], that formerly separate species approach each other and finally merge with each other. This would not fit the beautiful image that Darwin presented about the connection of species in a branch-rich tree; the branches of a tree do not fuse again.

The problem for Hilgendorf was that this is precisely what happened in his reconstructed phylogeny. Among the Hilgendorf artifacts found in the Institut und Museum für Geologie und Paläontologie, Tübingen, as discussed by Reif (1983), is a series of cards attributed to the time of his thesis work. These mostly illustrate some of Hilgendorf's proposed morphological transformation series, but one of them represents a phylogeny. This is shown in the next figure. This phylogeny shows gradual transformation of lineages (anagenesis), splitting of lineages (cladogenesis), and one lineage fusion. The diagram seems to accurately reflect the discussion in Hilgendorf's thesis, and so it is considered to be the phylogeny "missing" from that thesis.

The dilemma for Hilgendorf, then, was that he saw his work as supporting Darwin's evolutionary ideas but not supporting his metaphor. Under these circumstances, he decided not to rush into print. (Why publish on a controversial subject when you are not convinced by your evidence?)

What he did, instead, was return to Steinheim two years later (1865) and collect more data. This time his phylogenetic method produced a tree instead of a network (illustrated in Gastropods on Monday), and he subsequently published the result (Hilgendorf 1866, 1867). This paper makes no mention of Darwin at all. Interestingly, the first version had a subtitle ("an example of morphological change through time") that was not used in the final version, thus expunging all explicit references to evolutionary theory. It was not until Hilgendorf (1879) that he once again placed the Steinheim work into an explicitly Darwinian framework.

Hilgendorf could thus have been the third person to publish a genealogical network. Instead, he became the second person to publish a post-Darwinian phylogenetic tree. (Mivart had published the first tree in 1865, while Hilgendorf was prevaricating.)

Hilgendorf continued to defend his work in print against attacks from a number of people, notably Carl Sandberger, another German (who rejected transmutation entirely), and Alpheus Hyatt, an American (who was a Lamarckian) (see Reif 1983, Janz 1999, Rasser 2013). Ironically, these two anti-Darwinians seem to have convinced Darwin himself that Hilgendorf's work was not worthwhile (see Rasser 2013), and the only comment that Darwin added to later editions of his book was: "Hilgendorf has described a most curious case of ten graduated forms of Planorbis multiformis in the successive beds of a fresh-water formation in Switzerland [sic!]." As a result, Hilgendorf and his work have been ignored by most biologists.

Note that Darwin consistently down-played the importance of fossil evidence for his theory — he seemed to think that biogeographic evidence, for example, would be more convincing (as independently suggested by Alfred Russel Wallace). He thus failed to give due credence to the work of both Hilgendorf and Gaudry (a Frenchman digging in Greece), who each provided the first good examples of Darwinian evolution based on fossil stratigraphy.

The general Dilemma

I see Hilgendorf's personal history as the first example of a dilemma that all subsequent phylogeneticists have potentially faced, and when necessary have usually resolved in a similar manner. Darwin inappropriately changed the phylogenetic metaphor from a network to a tree, even in the face of then-known reticulation processes such as hybridization and introgression. And every time we are confronted with non-tree-like data we face the same dilemma; and most people have resolved it in the same way by publishing a tree instead of a network (see Phylogenetic networks 1900-1990).

It is only in the past couple of decades that we have started to behave in a more rational manner, and have returned to publishing networks instead of trees.

References

Darwin C. (1859) On the Origin of Species by Means of Natural Selection. John Murray, London.

Glaubrecht M. (2012) Franz Hilgendorf's dissertation "Beiträge zur Kenntnis des Süßwasserkalks von Steinheim" from 1863: transcription and description of the first Darwinian interpretation of transmutation. Zoosystematics & Evolution 88: 231-259.

Hellström N.P. (2011) The tree as evolutionary icon: TREE in the Natural History Museum, London. Archives of Natural History 38: 1-17.

Hilgendorf F. (1863) Beiträge zur Kenntniß des Süßwasserkalkes von Steinheim. Unpublished PhD Dissertation. Philosophische Fakultät, Universität Tübingen, 42 pp.

Hilgendorf F. (1866) Planorbis multiformis im Steinheimer Süßwasserkalk: ein beispiel von gestaltveränderung im laufe der zeit. Buchhandlung von W. Weber, Berlin, 36 pp.

Hilgendorf F. (1867) Über Planorbis multiformis im Steinheimer Süsswasserkalk. Monatsberichte der Königliche Preussischen Akademie der Wissenschaften zu Berlin 1866: 474-504.

Hilgendorf F. (1879) Zur Streitfrage des Planorbis multiformis. Kosmos 5: 10-22, 90-99.

Janz H. (1999) Hilgendorf's planorbid tree — the first introduction of Darwin's theory of transmutation into palaeontology. Paleontological Research 3/4: 287-293.

Penny D. (2011) Darwin's theory of descent with modification, versus the biblical Tree of Life. PLoS Biology 9: e1001096.

Rasser M.W. (2013) Darwin's dilemma: the Steinheim snails' point of view. Zoosystematics & Evolution 89: 13-20.

Reif W.-E. (1983) Hilgendorf's (1863) dissertation on the Steinheim planorbids (Gastropoda; Miocene): the development of a phylogenetic research program for paleontology. Paläontologische Zeitschrift 57: 7-20.

Weltner W. (1906) Franz Hilgendorf. 5 Dezember 1839 – 5 Juli 1904. Archiv für Naturgeschichte 72(1): I-XII.

Albert Einstein's consanguineous marriage

In previous blog posts, I have mentioned several well-known people who were involved in consanguineous marriages, which is defined as the union of two people who are related as closer than second cousins. In the first post (Charles Darwin's family pedigree network) I discussed in detail Charles Darwin (who married his first cousin); and in a later post (Toulouse-Lautrec: family trees and networks) I discussed the artist Henri Toulouse-Lautrec, who was the offspring of a marriage between first cousins. Now, it is the turn of Albert Einstein (1879-1955).

Einstein's first marriage (in 1903) was to a former fellow physics student, Mileva Marić (1875-1948). They had three children: Lieserl (1902-?), who was born the year before they married, Hans Albert (1904-1973) and Eduard (1910-1965). Einstein seems to have been far from the ideal husband or father, as detailed in the book by Roger Highfield & Paul Carter (The Private Lives of Albert Einstein, St. Martin's Griffin, 1994). Some brief information is given below.

When the marriage ended, Einstein married (in 1919) Elsa Löwenthal (née Einstein) (1876-1936), who brought with her two daughters from her own first marriage: Ilse (1897-1934) and Margot (1899-1986). As shown in the family pedigree below, Albert and Elsa were first cousins through their mothers (traced in red) and second cousins through their fathers (traced in blue). [NB. This is only part of the family tree.]

The main issue here is that this pedigree is a reticulating hybridization network, rather than a diverging tree, which clearly shows the problems with consanguineous marriages. The genetic diversity of any individual born from such a marriage has a much higher risk of expressing recessive genes in their phenotype, many of which cause serious health problems. For example, several of Darwin's children died young, and several others were apparently infertile. As well, Toulouse-Lautrec is well-known for his short stature and genetic deformities, and his brother died young, and several of his cousins (also the offspring of a consanguineous marriage) had the same genetic problem's as himself. Consanguineous marriages are not encouraged, if children are an intended outcome (see Bennett et al. 2002. Genetic counseling and screening of consanguineous couples and their offspring: recommendations of the National Society of Genetic Counselors. Journal of Genetic Counseling 11: 97-119).

Elsa and Albert are not known to have had any children (but see the note below), and it has been assumed that they had a relatively platonic relationship. So, this particular story does not have the same sad ending as those of Darwin and Toulouse-Lautrec. It would be interesting to know whether Albert and Elsa's childless state was a deliberate decision (in light of the possible genetic problems for any child), a consequence of age (they were in their 40s when they married, which makes pregnancy risky), or a result of (unreported) miscarriages.

The following note about Einstein as a husband is from The other side of Albert Einstein:

Einstein was far from the ideal husband. A year before they married, Maric gave birth to a daughter, Lieserl, while Einstein was away. The child's fate is unknown – she is presumed to have been given up for adoption, perhaps under pressure from Einstein, who is thought to have never seen his first born. After the marriage, Mileva bore two sons but the family was not to stay together. Einstein began an affair with his cousin Elsa Löwenthal while on a trip to Berlin in 1912, leaving Mileva and his family two years later. Einstein and Mileva finally divorced in 1919 ... Einstein married Elsa soon after the divorce [he had been living with Elsa for nearly five years], but a few years later began an affair with Betty Neumann, the niece of a friend. By one account, Elsa allowed Einstein to carry on with this affair to prevent him sneaking around. That relationship ended in 1924, but Einstein continued to have liaisons with other women until well after Elsa's death in 1936.

For information about a possible child of Albert and Elsa in 1932, see Einstein's son? It's a question of relativity.

Composers and consanguinity

There are many other people whose names are well-known and who were involved in a consanguineous marriage. Notably, there have been several composers of classical music:

• Johann Sebastian Bach married his second cousin, Maria Barbara Bach. The pair had seven children together, but only four survived to adulthood.
• Edvard Grieg married his first cousin, Nina Hagerup. Their only child, a daughter, died at the age of one. Around the same time Nina also had a miscarriage.
• Sergei Rachmaninoff married his first cousin, Natalya Satina. They had two daughters who survived to adulthood.
• Igor Stravinsky married his first cousin, Yekaterina Nossenko. They had four children surviving to adulthood – two sons and two daughters.

Note that this type of marriage was very unusual for Rachmaninoff and Stravinsky, because the Russian Orthodox Church explicitly forbids marriage between first cousins (both couples needed to get permission from the Czar), and so the families involved also opposed their marriages. Apparently, the relevant families also opposed Grieg's marriage. Indeed, it is reported that Edvard and Nina were surprised and disappointed to find out that they were not able to have children together.

Toulouse-Lautrec: family trees and networks

In a previous blog post (Charles Darwin's family pedigree network), I mentioned several well-known people who were involved in a consanguineous marriage, which is defined as the union of two people who are related as closer than second cousins. In that post I discussed in detail Charles Darwin (who married his first cousin); and in this post I discuss the artist Henri Toulouse-Lautrec, who was the offspring of a marriage between first cousins.

I thought that this would be a simple post, because there must be people who have studied the Toulouse-Lautrec-Montfa genealogy, given Henri's fame as a Post-Impressionist artist, along with the widespread knowledge that his phyiscal disabilities were genetic. But it turned out not to be so — there is no broad family tree that I could find, and no detailed discussion of inbreeding. The main information easily available is the direct lineage of inheritance of the various noble titles to which Henri would have been heir (had he survived his father, the Comte de Toulouse-Lautrec-Montfa), which can be traced back for more than 1000 years (see Vizegrafschaft Lautrec). However, the main interest for biology lies in his genetic relationship with his cousins, as we shall see below.

So, I sat down for a day to compile the family history for myself. The resulting genealogy is incomplete, but all of the relevant people are in it. I could not find all of the details about some of these people, either, which are apparently not available on the web; and some of the actual dates are inconsistent across different sources. In general, I have followed Dupic (2012).

When genealogical trees become networks

The point of this post is that marriages within a family turn the family tree into a network. So, a pedigree can be tree-like or not. In the latter case it is an example of a hybridization network.

This first genealogy shows a standard family tree for a single individual, looking backward in time from the bottom. So, this person is #1, the parents are #2 (father) and #3 (mother), and so on back through the generations, always with the male parent on the left (as is the convention). This example covers six generations, showing that without inbreeding everyone has 32 great-great-great grand-parents. These 32 people's genes are mixed more-or-less randomly (depending on recombination and assortment) to produce person #1. This is a good thing, evolutionarily, because there is then genetic diversity within #1.

However, with inbreeding some part of the ancestry disappears (when looking backward in time), because another part of the ancestry is duplicated in its place (this is called "pedigree collapse").

The second genealogy shows what happens when person #7 is the daughter of someone else in the same pedigree. If she is the daughter of #10 and #11, for example, then #5 and #7 would be sisters, and #2 and #3 would be first cousins. Now, person #1 has only 24 great-great-great grand-parents, and some of them are contributing to their descendants twice, rather than once (ie. #40–#47). This means that the genetic diversity in person #1 is less than it would be without the inbreeding. More to the point, any recessive alleles that exist in the ancestry have an increased probability of being homozygous in #1, and thus being expressed in the phenotype.

Toulouse-Lautrec's ancestry

This is, unfortunately, exactly what happened to Henri Toulouse-Lautrec, whose pedigree network is shown in the next figure. It is complete for six generations, plus an important part of the seventh. It is difficult to be complete beyond this generation, as the information becomes sparse, particularly about the female family members.

As shown, Henri's parents were first cousins, because their mothers were sisters. In addition, his maternal grandfather (#6) also had recent inbreeding in his history, because his mother (#13) was the daughter of a first-cousin marriage. This is not nearly as much inbreeding as has been implied by most commentators about Henri's life, but it is enough to potentially create genetic problems.

Note that it was Henri's mother's side of the family that was involved in the recent inbreeding, but the de Toulouse-Lautrec Montfa side was prone to the same thing, as are most titled families. As noted above, Henri died before inheriting his title. The title Comte de Toulouse-Lautrec-Monfa passed to Alphonse' next brother, Charles (1840-1917), who had no children, and thence to the next brother, Odon (1842-1937), and finally to Odon's son, Robert (1887-1972), who also had no children. The Internet seems to be silent about what happened to it after that.

Consequences of inbreeding

For Henri, life was tragic because he ended up with two copies of one particular recessive allele. The medical profession has been interested in this ever since his death, and much information is therefore now available about his condition (eg. Albury & Weisz 2013; Leigh 2013).

Albury & Weisz (2013) note:

The condition from which he probably suffered was first described in 1954 by the French physician Robert Weissman-Netter. It was named pycnodysostosis in 1962 by Marateaux and Lamy and was soon attributed to this artist as the "Toulouse-Lautrec Syndrome" ... Pycnodysostosis is a hereditary autosomal recessive dysplasia caused by an enzyme deficiency, namely of cathepsin K (cysteine protease deficiency in osteoclasts), reducing the normal bone resorption and leaving an incomplete matrix decomposition ... Toulouse Lautrec had a short stature with shortened legs, a large head due to a lack of closure of the fontanellae (which he usually covered with a hat), a shortened mandible with an obtuse angle (covered with a thick beard), dental deformities that required several surgical interventions, a large tongue, thick lips, profuse salivation, and a sinus obstruction with post-nasal drip. With fractures of the long bones during childhood, later on of the clavicle, with progressive hearing problems and cranio-facial deformities, Lautrec’s condition would complete the diagnosis of pycnodysostosis.

It seems to be widely recognized that Henri threw himself into his art at least partly to compensate for the psychological damage produced by his physical condition (he also became an alcoholic). As Leigh (2013) notes, his mother's side of the family had money (his father's side had a title but little money), and so Henri was financially free to do what he liked. He worked at a prodigious rate, and produced a life-time's worth of art in just 15 years — perhaps most famously his flamboyant lithograph posters (still as popular today as they were in his own time), but also oil paintings, watercolours, sculptures, ceramics and stained glass. He died at his mother's Château Malromé at age 36, after a stroke, but ultimately probably from tuberculosis (Albury & Weisz 2013).

Further inbreeding in the family

I noted in my previous post about Charles Darwin that, not only did he marry his cousin, his own sister married his wife's brother, thus literally keeping things in the family. In Henri Toulouse-Lautrec's case, the same thing happened: his paternal aunt married his maternal uncle, as shown in the next figure. This pedigree shows some more information about Henri's closest relatives, emphasizing the pair of consanguineous marriages.

There are 14 people shown in Henri's generation, all born to first-cousin marriages. (There may have been two more children in the Alix–Amédée marriage, but I have been unable to find any direct reference to them.) Of these people, six seem to have had disabilities similar to Henri's: Henri himself; his brother, who died the day before his first birthday; Madeleine, who died as a teenager; Geneviève; Béatrix; and Fides. The latter was so small that apparently she lived her entire life in a baby carriage (Rosenhek 2009). The photo below shows Henri with most of the Tapié de Céleyran family. It was taken in the summer of 1896 at Château du Bosc, where Henri had been born.

The two elderly women in the middle are Gabrielle (left) and Louise (right), the maternal and paternal grandmothers (they were sisters, remember). The father, Amédée, is at the rear centre (sticking his tongue out at the photographer), and the mother, Alix, is standing at the far right. Standing next to her is the oldest son, Raoul; and his wife, Elisabeth, is seated at the far left. The next two sons, Gabriel and Odon, are absent, along with their wives. The next son, Emmanuel, is standing at the back left; and his wife, Marie-Thérèse, is seated next to the pram (middle right). The youngest sons are sitting on the ground at the front centre, with Alexis on the left and Olivier on the right. The first-born daughter, Madeleine, was already dead when the photo was taken. The next three daughters are sitting at the middle left, with Germaine sitting on Elisabeth's lap, Geneviève in front of her, and then Marie seated on the ground. Béatrix is at the middle right, sitting next to Marie-Thérèse, and Fides is in her pram. Henri himself is seated on the ground at the far left. His brother, Richard, had also died before the photo was taken. The remaining four people (standing either side of Amédée) are other relatives.

Nevertheless, this large family did manage to survive the effects of inbreeding, unlike Henri's own family. At least seven of the children survived to have children of their own (~19 grand-children):

Person Raoul Gabriel Odon Emmanuel Germaine Marie Alexis

Spouse Elisabeth DAUDÉ de LAVALETTE (1870-1956) Anne de TOULOUSE-LAUTREC (1873-1944) Marguerite TAILLEFER de LAPORTALIÈRE (1878-1958) Marie-Thérèse des CORDES Alexandre d'ANSELME (1876-1912) Adrien de RODAT d'OLEMPS (1806-1884) Anne Marie de MALVIN de MONTAZET (1885-1974)

4 children 3 children 1 child 2 children 2 children 3 children 4 children

Note that Gabriel and Anne were third cousins, since they had great-grand-fathers who were brothers; nevertheless, they had 3 female children, at least one of whom also had 3 children. One of Alexis' sons (ie. Henri's second cousin once removed) was well-known art critic Michel Tapié de Céleyran (1909-1987), who married and had seven children, two of whom died in infancy.

Inbreeding increases the probability that recessive alleles will be expressed, but it does not make this inevitable. In Henri's case, two disabled children in succession seems to have dissuaded his parents, and they separated, whereas his aunt and uncle had a healthy child the second time, and so they continued producing a family. However, these days it is not recommended that you marry any of your first cousins.

Conclusion

Evolution is about biodiversity at all hierarchical levels, not just between or within species, but within individuals as well. Average intra-individual genetic diversity reaches a maximum when the ancestry is tree-like, and reduces with each instance of inbreeding, which turns the tree into a network of increasingly greater complexity.

I have discussed an even more extreme example of consanguinity in a previous post (Family trees, pedigrees and hybridization networks), in which the inbreeding became so severe that the royal family lineage actually came to an end.

References

Albury WR, Weisz GM (2013) Toulouse-Lautrec and medicine: a triumph over infirmity. Hektoen International 5: 3.

Dupic S. (2012) Toulouse-Lautrec - Généalogie 87 le site de référence de la généalogie de la haute-vienne.

Leigh FW (2013) Henri Marie Raymond de Toulouse-Lautrec-Montfa (1864-1901): artistic genius and medical curiosity. Journal of Medical Biography 21: 19-25.

Rosenhek J (2009) Picture imperfect: tiny Henri de Toulouse-Lautrec’s talent – and troubles – were larger than life. Doctor's Review Oct 2009.

Phylogenetics with SpongeBob

Some time ago I published a blog post on Faux phylogenies in which I included a phylogeny of cartoon animals by Mike Keesey. In this phylogeny, SpongeBob SquarePants was the outgroup. However, SpongeBob goes much further than this.

Importantly, the main characters in the cartoon have representative members of several phyla (notably, except the Cnidaria). Indeed, the List of SpongeBob SquarePants characters at Wikipedia makes this very clear. This opens up the possibility that they could be a means of using modern culture to introduce phylogenetics. This idea has been independently discovered at least twice.

Perhaps the best known usage is by Paul Arriola, produced for his freshman biology students, as shown in the first figure.

This has been reproduced in several places on the web, including Pinterest (e.g. here and here), Facebook (e.g. here and here), and academia (here).

Another, apparently independent, usage is by Rita Chen of the sister artists known as The Hurricanes.

Note that a few "extra" characters have been added (the planarian, ragworm and roundworm), and that the names are not all quite correct.

By the way, did you know that there is a species of sponge-like fungus (in the Boletaceae) called Spongiforma squarepantsii, and named after the character? If not, then see Wikipedia.

What are evolutionary networks currently used for?

These days, there are many unrooted affinity-type networks used to display conflicting phylogenetic signals. There are many different methods available, although the various forms of splits graphs seem to dominate, especially NeighborNet and Consensus Networks (for species-level data), and Reduced Median Networks and Median Joining Networks (for population-level data). However, phylogeneticists are interested in genealogies, not just data displays.

Unfortunately, rooted evolutionary networks are not so well off. There is a great need for such networks in phylogenetics, but there are very few automated methods available for constructing them. These networks are needed whenever a genealogy involves reticulation processes rather than solely divergence. The latter produces a tree-like evolutionary history but the former do not, and these thus require network methods.

Due to the lack of obvious methods, most current research papers still do not illustrate reticulate evolution with a genealogy. A collection of ad hoc methods is usually applied to the data, and the evolutionary processes are then inferred from this. However, the use of a network to illustrate the inferred genealogy is rather rare.

Indeed, for species-level studies most papers simply present a set of incongruent gene trees, although some of them also illustrate either (i) the tree derived from the combined data, or (ii) a consensus tree with or without the conflicting relationships, or (iii) a pair of cophylogeny trees. Occasionally, the hybrid origin of some of the species, for example, is illustrated, but the putative parents are not connected in a phylogeny.

Population-level studies often present unrooted haplotype networks, illustrating processes such as hybridization and introgression between closely related species, or the evolution of domesticated species.

However, these ad hoc methods do not mean that evolutionary networks do not appear in the literature. In this blog post I include a representative sample of rooted networks that are intended to illustrate inferred genealogies. They are grouped according to the evolutionary processes being studied (see Reticulation patterns and processes in phylogenetic networks). I have also briefly indicated how the networks were constructed.

Homoploid Hybridization

Hybridization is commonly studied in the literature, and phylogenetic networks appear not infrequently. This first example was constructed by the unreleased program HyperPars.

Dickerman AW (1998) Generalizing phylogenetic parsimony from the tree to the forest. Systematic Biology 47: 414-426.

This next example was constructed by program SplitsTree. Note that the root of the network is not clearly indicated.

Pirie MD, Humphreys AM, Barker NP, Linder HP (2009) Reticulation, data combination, and inferring evolutionary history: an example from Danthonioideae (Poaceae). Systematic Biology 58: 612-628.

This example was constructed manually from a set of gene trees. Note that it is drawn in a rather unusual style for indicating hybridization.

Sang T, Crawford D, Stuessy T (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84: 1120-1136.

Polyploid Hybridization

Polyploid hybridization is probably the most likely type of study to have a phylogenetic network. This is at least partly because there is a computer program, Padre, to automate much of the work. This program was used to construct this first network.

Marcussen T, Jakobsen KS, Danihelka J, Ballard HE, Blaxland K, Brysting AK, Oxelman B (2012) Inferring species networks from gene trees in high-polyploid North American and Hawaiian violets (Viola, Violaceae). Systematic Biology 61: 107-126.

This next example was also constructed by program Padre.

Sessa EB, Zimmer EA, Givnish TJ (2012) Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae). BMC Evolutionary Biology 12: 104.

This example constructed manually from a gene tree.

Marhold K, Lihová J (2006) Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Systematics and Evolution 259: 143-174.

Introgressive Hybridization

Introgression is a widely studied phenomenon. However, rooted evolutionary networks are rarely presented. This first one was constructed manually from a set of gene trees.

Koblmüller S, Duftner N, Sefc KM, Aibara M, Stipacek M, Blanc M, Egger B, Sturmbauer C (2007) Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika — the result of repeated introgressive hybridization. BMC Evolutionary Biology 7: 7.

The next example was also constructed manually from a set of gene trees.

Morgan DR (2003) nrDNA external transcribed spacer (ETS) sequence data, reticulate evolution, and the systematics of Machaeranthera (Asteraceae). Systematic Botany 28: 179-190.

This example was constructed by program SplitsTree.

Labate JA, Robertson LD (2012) Evidence of cryptic introgression in tomato (Solanum lycopersicum L.) based on wild tomato species alleles. BMC Plant Biology 12: 133.

Horizontal Gene Transfer

HGT is a hot topic these days, both among prokaryotes and among eukaryotes, although most papers do not present a phylogenetic network. The first example was constructed by program Sprit from the species tree and a gene tree.

Walsh AM, Kortschak RD, Gardner MG, Bertozzi T, Adelson DL (2013) Widespread horizontal transfer of retrotransposons. Proceedings of the National Academy of Sciences USA 110: 1012-1016.

This next example was constructed manually from a gene tree.

Delwiche CF, Palmer JD (1996) Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Molecular Biology and Evolution 13: 873-882.

This example was constructed manually from incongruence among a series of gene trees.

Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ (2009) Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. The Plant Cell 21: 1897-1911.

Homologous Recombination

Intra-genic recombination is often studied without reference to a network. Nevertheless, several programs exist, and this particular network was constructed by program Kwarg.

Jenkins PA, Song YS, Brem RB (2012) Genealogy-based methods for inference of historical recombination and gene flow and their application in Saccharomyces cerevisiae. PLoS One 7: e46947.

Chromosomal rearrangements are studied rather rarely. This network was constructed manually from a phylogenetic tree. Note that the root of the network is not clearly indicated.

Rumpler Y, Hauwy M, Fausser JL, Roos C, Zaramody A, Andriaholinirina N, Zinner D (2011) Comparing chromosomal and mitochondrial phylogenies of the Indriidae (Primates, Lemuriformes). Chromosome Research 19: 209-224.

Viral Reassortment

Reassortment of segmented viruses produces very complex networks. This one is a partial network, constructed manually from a series of phylogenetic analyses.

Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459(7250): 1122-1125.

Genome Fusion

This is a difficult topic to study. As is almost always done, this network was constructed manually from a phylogenetic tree.

Thiergart T, Landan G, Schenk M, Dagan T, Martin WF (2012) An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biology and Evolution 4: 466-485.

Apomixis

This topic rarely involves networks. This network was constructed manually from the output of program SplitsTree.

Dyer RJ, Savolainen V, Schneider H (2012) Apomixis and reticulate evolution in the Asplenium monanthes fern complex. Annals of Botany 110: 1515-1529.

Removing Convergence

This is an unusual use of a network, but the author notes that "the use of reticulations clarifies the phylogeny by factoring out apparent convergence, even though there is no reason to think that actual hybridization or introgression has occurred." The network was constructed by an unreleased program.

Alroy J (1995) Continuous track analysis: a new phylogenetic and biogeographic method. Systematic Biology 44: 152-178.

Phylogenetic networks 1900-1990

In earlier blog posts I have pointed out that the first phylogenetic network explicitly representing a genealogy was published in 1755 (The first phylogenetic network, 1755) and the second in 1766 (The second phylogenetic network, 1766), but the third one that I know of did not appear until 1888 (Networks of genealogy). Up until 1900 there were, however, many networks published that represented affinity rather than genealogy (Networks of affinity rather than genealogy).

In this post I consider the subsequent history of phylogenetic networks, as far as I have been able to determine it, up until 1990. Networks remained relatively rare up to that time; and indeed even the name "phylogenetic network" usually referred to an unrooted tree rather than to a reticulating network (Who first used the term "phylogenetic network"?). From 1990 onwards networks have become quite common, and many scores of them have now been published.

Below, I present all of the networks that I am aware of from 1900-1990. I doubt very much that this includes all of the published networks. Indeed, I do not know even what proportion of them are presented here. However, I do believe that this is a representative selection of the uses of phylogenetic networks between 1900 and 1990.

Note: Last updated 16 November 2014.

Background

This was an era in which trees dominated phylogenetic thinking, presumably in response to Charles Darwin's 1859 book (Who published the first phylogenetic tree?). Reticulation was talked about by a number of authors when discussing affinity, notably in botany (Stevens P.F. 1994. The Development of Biological Systematics: Antoine-Laurent de Jussieu, Nature, and the Natural System. Columbia Uni. Press, New York), but it was rarely illustrated, especially empirically. Indeed, the most popular time for affinity networks was up to the mid-late 1800s, at which time genealogical trees took over.

Most of the networks shown below are rooted, and thus represent genealogy, but a few unrooted affinity networks still appeared. However, in general few people used phylogenies to display their results, even when discussing hybridization or horizontal gene transfer. The people investigating these phenomena appeared to not be thinking in terms of phylogenetics, but instead were investigating mechanisms among a small group of species. The phylogenetic context that is so prevalent in biology today was rare before 1990.

There is an obvious peak during the 1950s, and there is an interesting gap after 1970 when cladistics rose to prominence, with its focus on dichotomous trees (Who first used the term "phylogenetic network"?). Nevertheless, the existence of such a diverse collection of networks shows that biologists were still able to "think outside of the box" when they felt it was necessary.

The networks

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Available from the Biodiversity Heritage Library.

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Available from JStor.

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Figure copy available in JStor.

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Available from JStor.

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The figure is taken from Alston & Turner (1963) Biochemical Systematics, available from the Biodiversity Heritage Library.

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Available from the Biodiversity Heritage Library.

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The figure is taken from Alston & Turner (1963) Biochemical Systematics, available from the Biodiversity Heritage Library.

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Available from JStor.

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Available from Springer.