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Phylogeny of birds (19 Viewers)

Massive family-level global bird tree based on whole-genome analyses


BOOM! Today, our new bird phylogeny was published in Nature (soon also at Complexity of avian evolution revealed by family-level genomes - Nature). Or, well, an ugly preview version that should soon be prettified was made available. This is the main result of the family phase of the Bird 10,000 Genomes Project (B10K), and thus is “the new Jarvis et al. (2014) tree”. The work has been incredibly intensive and demanding, and the 52-headed crew of co-authors has been led by Josefin Stiller (University of Copenhagen), Siavash Mirarab (UCSD) and Guojie Zhang (Zhejiang University). I should stress already here that my contributions have been rather minor, but I’m probably the only one on BirdForum, so I figured it falls on me to report our study here.

This is the most detailed, highly resolved, and precise phylogeny of birds to date. It is based on 363 species, representing 92% of all bird families (as per Howard & Moore 4; the last 8% representing taxa we have so far been unable to get usable samples from), whose whole genomes have been sequenced, assembled, and annotated. They have then put into a whole-genome alignment and, in total, these analyses cover nearly 100 BILLION basepairs. With quite some margin, this makes up the most extensive phylogenetic analyses of birds to date. There’s long been a debate about whether increased taxon sampling is better to increase precision and reliability or increased genetic sequencing (more loci; more base pairs). Here, we’ve been able to test this. More about that below, but first some of the taxonomic news. Let’s start with something that makes some intuitive sense.

Strigformes and Accipitriformes are sister orders (but it’s complicated…)
In the main two previous genome-scale phylogenies by Jarvis et al. 2014 (based on 48 taxa and 48,000,000 bp of genes and ultra-conserved elements (UCEs)) and Prum et al. 2015 (based on 198 species and 395,000 bp from protein-coding genes), Strigiformes (owls) have been recovered as a sister lineage to a clade within Afroaves comprising Coliiformes, Leptosomatiformes, Trogoniformes, Bucerotiformes, Coraciiformes, and Piciformes, i.e. the bulk of clade Afroaves. Accipitriformes, however, was recovered as having branched off earlier from that clade (Jarvis et al. 2014) or even earlier, from the branch leading to the ancestor of Afroaves and the Australaves orders Cariamiformes, Falconiformes, Psittaciformes, and Passeriformes (Prum et al. 2015).

In our main tree, which was produced with coalescent-based analyses of a 63,430,000-bp matrix of spaced intergenic sequence (63,430 loci of 1,000 bp each), diurnal birds of prey and their nocturnal counterparts come out as sister lineages, placed basally within Afroaves. Having said that, these orders are particularly problematic to place and ancient hybridization may have played a role. More details in the paper. Now for a newly recovered grouping that none of you would have seen coming!

View attachment 1569508

Elementaves is an exceedingly diverse neoavian clade of surprising relatives
As expected, at the base of our tree sits infraclass Palaeognathae (ratites), sister to all other extant birds, which sort under infraclass Neognathae. Neognathae diverges into parvclasses Galloanseres (fowl and ducks) and Neoaves, the latter comprising all remaining birds. The arrangement within parvclass Neoaves has been subject to many changes, since the very rapid diversification at its base has been near-impossible to sort out with any confidence. Our analyses recover four basal clades within Neoaves. The first one to branch out is Mirandornithes (Phoenicopteriformes, Podicipediformes); next comes Columbaves (Mesitornithiformes, Pterocliformes, Columbiformes, Musophagiformes, Otidiformes, Cuculiformes)—although there is a whole interesting story about Columbaves, that shows that Columbimorphae may in fact be sister to Mirandornthes instead, forming Columbea (see separate paper by Mirarab et al. released today in PNAS). Left is a two-way split between Telluraves, which comprises Afroaves and Australaves as above, and our novel cool gang/unruly bunch.

Included here is a clade with Opisthocomiformes as probable sister to the sister pair Gruiformes and Charadriiformes; another clade where Caprimulgiformes (sensu lato, i.e. = Strisores) likely sits at the base as sister to a clade which bifurcates into Phaetontimorphae (Eurypygiformes, Phaetontiformes) and Aequornithes (Gaviformes, Pelecaniformes, Procellariformes, Sphenisciformes). This means that our very smallest (hummers) and largest (one way to measure at least; albatrosses) are part of the same clade. I see lots of shaking heads and furrowed brows right now, and expect several of you to think that “this just cannot be right”. While no phylogeny can claim to be the truth, I will say, however, that this is not a random grouping that has just been accepted without challenge (and loads of additional analyses). It does nicely illustrate, however, how the amount of data affects both support and topology – and that different methods of analyses recover different topologies. There’s lots more to read about this in the paper.

As for the name, we name it Elementaves because the clade’s lineages have diversified into terrestrial, aquatic, and aerial niches (holding several of our most impressive specialists like penguins, albatrosses, and swifts), corresponding to the classical elements of earth, water, and air. So, what about fire? Well, several species within Phaethontimorphae have names derived from the sun, a big ball of fire.

What are the differences in topology and which tree should you believe in?
We argue overall that our extensive taxon sampling combined with extensive genomic sampling (i.e. not taxa vs loci, but preferably both) of regions that are not under direct or indirect selection (unlike previous trees), analysed in a coalescence-based framework, produces a stronger and more reliable bird phylogeny. There’s lots more to read about this in the paper. But what are the differences from the two previous main panavian phylogenies, Jarvis et al. (2014) and Prum et al. (2015)? This is made easy to assess as it is summarised in this figure:

View attachment 1569509

Should you trust this new tree over Jarvis or Prum? We argue yes, but we also offer a fun analyses that lends some support to this claim. If one explores the phylogenetic signal (based on the tree) in how morphological trait (co-)vary, it turns out that in morphometric variables (bill measurements, body mass, tail length, wing length and shape, and tarsus length), the distribution of measurements across species “make more sense” with the new tree. That is, there is less sudden variation (evolutionary shifts) along the tree branching toward the present with our new topology, than compared with the tree of Prum et al. (2015) [too few species in Jarvis et al. 2014].

Precision of age estimation and timing relative the
The final cool thing I’d like to bring up about this new phylogeny is that the precision is vastly higher for node age estimation than has ever been achieved before (including Jarvis et al. 2014 and Prum et al. 2015). This has much to do with the extensive work to classify avian fossils and empirically generate ‘calibration densities’ for no less than 34 nodes. Many node age estimates differ from previous studies, but most fall within the latter’s large 95% confidence intervals. Our new dating offers much narrower confidence intervals (and some surprises in terms of actual age, like very much older Tinamidae, older Apodidae, younger Pipridae and Accipitridae). This offers more insight to the timing around the Cretaceous–Paleogene boundary, which coincides with the rapid and extensive diversification of Neoaves. Some folks have proposed a scenario in which the main lineages of Neoaves would have evolved prior to the asteroid impact and survived through it. More favoured and more well-supported by fossils, though so far not supported with any precision by molecular data, is the ‘big bang’ scenario. This means that the main diversification of Neoaves would have happened after the asteroid impact, as a response to the vacation of whole ecological niches previously occupied by non-avian dinosaurs and other animals. Our tree lends support to this scenario.

That’s over and out from me at this point, but I promise you that there is much more to be gleaned from Stiller et al. (2024)! Not least, a lot of additional goodies are hiding in the supplemental extended data figures, so don’t miss out on them.
You should propose a clade bringing together Hoazin + Gruiformes and Charadriiformes. 😏
 
Me too, but luckily there's excel to count for me: Agostinho Antunes, Edward L. Braun, Erich D. Jarvis, Guangji Chen, Guojie Zhang, Iker Rivas-González, Josefin Stiller, Mikkel H. Schierup, Qi Fang, Shaohong Feng, Siavash Mirarab, Uyen Mai.
Recently there have been several large-scale studies with different results, notably on the position of the Hoazin and raptors (except Falcons). The latter two offer very identical results.
 
They describe the composition and reason for name.

The fourth major clade is new and phenotypically diverse, containing Aequornithes (pelicans, tubenoses, penguins, and loons), Phaethontimorphae (kagu, sunbittern, and tropicbirds), Strisores (nightbirds, swifts, and hummingbirds), Opisthocomiformes (hoatzin), and Cursorimorphae (shorebirds and cranes). This clade was supported in coalescent-based analyses of the intergenic regions, and UCEs, but not by the exons, introns, or in concatenated analysis of the intergenic regions (Fig. 3d, Extended Data Fig. 4). We name the clade Elementaves because its lineages have diversified into terrestrial, aquatic, and aerial niches, corresponding to the classical elements of earth, water, and air, and several Phaethontimorphae have names derived from the sun, representing fire.
 
A complete and dynamic tree of birds
Emily Jane McTavish, Jeff A. Gerbracht, Mark T. Holder, Marshall J. Iliff, Denis Lepage, Pam C. Rasmussen, Benjamin Redelings, Luna Luisa Sanchez-Reyes, Eliot T. Miller
bioRxiv 2024.05.20.595017; doi: A complete and dynamic tree of birds

Abstract
We present a complete, time-scaled, evolutionary tree of the world's bird species. This tree unites phylogenetic estimates for 9,239 species from 262 studies published between 1990 and 2024, using the Open Tree synthesis algorithm. The remaining species are placed in the tree based on curated taxonomic information. The tips of this complete tree are aligned to the species in the Clements Taxonomy used by eBird and other resources, and cross-mapped to other taxonomic systems including the Open Tree of Life (Open Tree), National Center for Biotechnology Information (NCBI), and Global Biodiversity Information Facility (GBIF). The total number of named bird species varies between 10,824 and 11,017 across the taxonomy versions we applied (v2021, v2022 and v2023). We share complete trees for each taxonomy version. The procedure, software and data-stores we used to generate this tree are public and reproducible. The tree presented here is Aves v1.2 and can be easily updated with new phylogenetic information as new estimates are published. We demonstrate the types of large scale analyses this data resource enables by linking geographic data with the phylogeny to calculate the regional phylogenetic diversity of birds across the world. We will release updated versions of the phylogenetic synthesis and taxonomic translation tables annually. The procedure we describe here can be applied to developing complete phylogenetic estimates for any taxonomic group of interest.


Curious to see their complete tree of birds
 
A complete and dynamic tree of birds
Emily Jane McTavish, Jeff A. Gerbracht, Mark T. Holder, Marshall J. Iliff, Denis Lepage, Pam C. Rasmussen, Benjamin Redelings, Luna Luisa Sanchez-Reyes, Eliot T. Miller
bioRxiv 2024.05.20.595017; doi: A complete and dynamic tree of birds

Abstract
We present a complete, time-scaled, evolutionary tree of the world's bird species. This tree unites phylogenetic estimates for 9,239 species from 262 studies published between 1990 and 2024, using the Open Tree synthesis algorithm. The remaining species are placed in the tree based on curated taxonomic information. The tips of this complete tree are aligned to the species in the Clements Taxonomy used by eBird and other resources, and cross-mapped to other taxonomic systems including the Open Tree of Life (Open Tree), National Center for Biotechnology Information (NCBI), and Global Biodiversity Information Facility (GBIF). The total number of named bird species varies between 10,824 and 11,017 across the taxonomy versions we applied (v2021, v2022 and v2023). We share complete trees for each taxonomy version. The procedure, software and data-stores we used to generate this tree are public and reproducible. The tree presented here is Aves v1.2 and can be easily updated with new phylogenetic information as new estimates are published. We demonstrate the types of large scale analyses this data resource enables by linking geographic data with the phylogeny to calculate the regional phylogenetic diversity of birds across the world. We will release updated versions of the phylogenetic synthesis and taxonomic translation tables annually. The procedure we describe here can be applied to developing complete phylogenetic estimates for any taxonomic group of interest.


Curious to see their complete tree of birds
You doi link (again) does not work: https://www.biorxiv.org/content/10.1101/2024.05.20.595017v1.full.pdf
I assume the tree must be somewhere in here, but I don't understand how to find it: GitHub - McTavishLab/AvesData: Data deposit for Aves synthetic tree
 
Here is the direct link
 
I was able to get the tree to read in the program mesquite, although the tree is so big my computer is not happy. I used the tree_annot_summary.nex file.

But yes, the lack of a simple pdf with a set of trees is definitely an odd choice, since it kind of makes the tree invisible to anyone who isn't already a phylogenetics trained person
 
I was able to get the tree to read in the program mesquite, although the tree is so big my computer is not happy. I used the tree_annot_summary.nex file.

But yes, the lack of a simple pdf with a set of trees is definitely an odd choice, since it kind of makes the tree invisible to anyone who isn't already a phylogenetics trained person
The file cannot be converted to PDF?
 
I'm assuming you should be able to view the tree at Open Tree of Life, at least when the paper is published. Not sure if it's loaded yet or how to check the paper version versus the live OTT version. The current tree for Aves has Caprimulgimorphae as the first neoavian branch.

If you look at the curator page, you see both the Stiller et al (2024) and Wu et al (2024) studies (it also has Alstrom 2023 on Aluridae). Emily McTavish, first author on the study above, is the curator of these datasets. You can view the trees from these studies by following the links, e.g. Stiller study and Stiller tree.
 
yeah, but I don't think its based on anything new, right? they state that where data was absent they use "curated taxonomic opinions" which basically amounts to "well I think these two species are related based on x", not something backed up from a unambiguous phylogenetic analysis. I guess its still better than nothing?
 
Fig 2A shows the families with 25 or more members in the tree. It looks like the ordinal topology is the Stiller et al (2024) one. I can't tell for certain if it's exactly the same, but there seem to be small unlabelled branches in the right places. I'm assuming this is not entirely because recent papers get a higher weighting.
 

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