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Set­tle­ment of con­tro­versy on fam­ily tree of pla­cen­tal mammals

pub­lished 20 Feb­ru­ary 2016 | mod­i­fied 20 Feb­ru­ary 2016

African elephant Atlanta ZooThe roots of the mam­malian fam­ily tree have long been shrouded in mys­tery — when did the pla­cen­tal mam­mals go their sep­a­rate ways? Now, researchers at the Uni­ver­sity of Bris­tol say they’ve found where the fam­ily tree of pla­cen­tal mam­mals first branched apart — and when it hap­pened. Their find­ings were first pub­lished online on 5 Jan­u­ary in the jour­nal Genome Biol­ogy and Evo­lu­tion.

The con­tro­versy
Pla­cen­tal mam­mals con­sist of three main groups that diverged rapidly, evolv­ing in wildly dif­fer­ent direc­tions: Afrothe­ria (for exam­ple, ele­phants and ten­recs), Xenarthra (such as armadil­los and sloths) and Bore­oeuthe­ria (all other pla­cen­tal mam­mals). Placental mammals relationship hypothesisThe rela­tion­ships between them have been a sub­ject of fierce con­tro­versy with mul­ti­ple stud­ies com­ing to incom­pat­i­ble con­clu­sions over the last decade lead­ing some researchers to sug­gest that these rela­tion­ships might be impos­si­ble to resolve.

There are thus many out­stand­ing ques­tions such as which is the old­est sib­ling of the three? Did the mam­mals go their sep­a­rate ways due to South Amer­ica and Africa break­ing apart? And if not, when did pla­cen­tals split up?

This has been one of the areas of great­est debate in evo­lu­tion­ary biol­ogy, with many researchers con­sid­er­ing it impos­si­ble to resolve
Dr James E. Tarver, lead author, School of Earth Sci­ences, Uni­ver­sity of Bris­tol, UK »

Now we’ve proven these prob­lems can be solved — you just need to analyse genome-​scale datasets using mod­els that accu­rately reflect genomic evo­lu­tion,” added Tarver.

The study
The researchers assem­bled the largest mam­malian phy­loge­nomic dataset ever col­lected before test­ing it with a vari­ety of mod­els of mol­e­c­u­lar evo­lu­tion, choos­ing the most robust model and then analysing the data using sev­eral super­com­puter clus­ters at the Uni­ver­sity of Bris­tol and the Uni­ver­sity of Texas Advanced Com­put­ing Centre.

We tested it to destruc­tion,” said Dr Tarver. “We threw the kitchen sink at it.”

A com­pli­ca­tion in recon­struct­ing evo­lu­tion­ary his­to­ries from genomic data is that dif­fer­ent parts of genomes can and often do give con­flict­ing accounts of the his­tory,” said Dr Siavash Mirarab at the Uni­ver­sity of Cal­i­for­nia San Diego, USA. “Indi­vid­ual genes within the same species can have dif­fer­ent his­to­ries. This is one rea­son why the con­tro­versy has stood so long — many thought the rela­tion­ships couldn’t be resolved.”

To address the com­plex­i­ties of analysing large num­bers of genes shared among many species, the researchers paired two fun­da­men­tally dif­fer­ent approaches — con­cate­nated and coalescent-​based analy­ses — to con­firm the findings.

The find­ings
When the dust set­tled, the team had a spe­cific fam­ily tree show­ing that Atlanto­genata (con­tain­ing the sib­ling groups of African Afrothe­ria and the South Amer­i­can Xenarthra) is the sis­ter group to all other placentals.

Because many con­flict­ing fam­ily trees have already been pub­lished, the team then gath­ered three of the most influ­en­tial rivals and tested them against each other with the same model. All of the pre­vi­ous stud­ies sud­denly fell into line, their data agree­ing with Tarver and colleagues.

Phylogenetric tree placental mammalsResults from four of the phy­lo­ge­netic analy­ses with each one pro­vid­ing sup­port for Atlanto­genata as the sis­ter taxon to all other euthe­ri­ans. (a) The 21.4 mil­lion whole-​genome nucleotide align­ment ana­lyzed using Phy­lobayes (CAT-GTR+G), RAxML and ASTRAL with sup­port val­ues for almost all nodes being either 1 or 100. (b) The sin­gle con­cate­nated nucleotide align­ment for the pre-​mir sequences ana­lyzed under GTR+G in Phy­lobayes. Laurasiathe­ria is shown col­lapsed as the inter­re­la­tion­ships among the con­stituent taxa vary between data sets.
James E Tarver, et al. The Inter­re­la­tion­ships of Pla­cen­tal Mam­mals and the Lim­its of Phy­lo­ge­netic Infer­ence. (2016) 8 (2): 330344. doi: 10.1093/gbe/evv261; Cre­ative Com­mons Attri­bu­tion License

With the ori­gins of the fam­ily tree resolved, what does this mean for pla­cen­tal mam­mals? The researchers folded in another layer — a mol­e­c­u­lar clock analy­sis. “The mol­e­c­u­lar clock analy­sis uses a com­bi­na­tion of fos­sils and genomic data to esti­mate when these lin­eages diverged from each other,” said author Dr Mario Dos-​Reis of Queen Mary Lon­don, UK. “The results show that the afrothe­ri­ans and xenarthrens diverged from one another around 90 mil­lion years ago.”

The con­clu­sions
Pre­vi­ously, sci­en­tists thought that when Africa and South Amer­ica sep­a­rated from each other over 100 mil­lion years ago, they broke up the fam­ily of pla­cen­tal mam­mals, who went their sep­a­rate evo­lu­tion­ary ways divided by geog­ra­phy. But the researchers found that pla­cen­tal mam­mals didn’t split up until after Africa and South Amer­ica had already separated.

Placental mammal lineages divergenceResults from the mol­e­c­u­lar clock analy­sis show­ing the diver­gence times for pla­cen­tal lin­eages with all pos­te­rior prob­a­bil­i­ties shown in “green” and over­laid on the joint prior shown in “red,” with both shaded to show val­ues of high­est like­li­hood (see table 6 for the 95% HPD val­ues). Cur­rent bio­geo­graphic recon­struc­tions for the breakup of Pangea at 180, 120, and 90 Ma, from “left to right,” respec­tively, with hot­ter col­ors (“red”) indi­cat­ing faster rates of sea floor for­ma­tion than colder col­ors (“blue”) based on Seton et al. (2012) and down­load­able from http://​www​.earth​byte​.org/​R​e​s​o​u​r​c​e​s​/​g​l​o​b​a​l​_​p​l​a​t​e​_​m​o​d​e​l​_​E​S​R​12​.​h​t​m​l. Both the North­ern and South­ern hemi­sphere con­ti­nents have sep­a­rated by 90 Ma, high­light­ing the role of dis­per­sal, rather than vic­ari­ance, for the bio­geo­graphic dis­tri­b­u­tion of crown pla­cen­tals as the breakup of Pan­gaea pre­dates cur­rent mol­e­c­u­lar clock esti­mates for the diver­gence of crown pla­cen­tals.
James E Tarver, et al. The Inter­re­la­tion­ships of Pla­cen­tal Mam­mals and the Lim­its of Phy­lo­ge­netic Infer­ence. (2016) 8 (2): 330344. doi: 10.1093/gbe/evv261; Cre­ative Com­mons Attri­bu­tion License

We pro­pose that South America’s liv­ing endemic Xenarthra (for exam­ple, sloths, anteaters, and armadil­los) col­o­nized the island-​continent via over­wa­ter dis­per­sal,” said study author Dr Rob Asher of the Uni­ver­sity of Cam­bridge, UK.

Dr Asher sug­gests that this isn’t as dif­fi­cult as you might think. Mam­mals are among the great adven­tur­ers of the ani­mal king­dom, and at the time the proto-​Atlantic was only a few hun­dred miles wide. We already know that New World mon­keys crossed the Atlantic later, when it was much big­ger, prob­a­bly on rafts formed from storm debris. And, of course, mam­mals repeat­edly colonised remote islands like Madagascar.

Even sloths can swim smile :

You don’t always need to over­turn the sta­tus quo to make a big impact,” said Dr Tarver. “All of the com­pet­ing hypothe­ses had some evi­dence to sup­port them — that’s pre­cisely why it was the source of such con­tro­versy. Prov­ing the roots of the pla­cen­tal fam­ily tree with hard empir­i­cal evi­dence is a mas­sive accomplishment.”

(Source: Uni­ver­sity of Bris­tol press release, 15.02.2016)

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