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The Phylogenomic Forest of Bird Trees Contains a Hard Polytomy at the Root of Neoaves

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The Phylogenomic Forest of Bird Trees Contains a Hard Polytomy at the Root of Neoaves Zoologica Scripta Invited Review The phylogenomic forest of bird trees contains a hard polytomy at the root of Neoaves ALEXANDER SUH Submitted: 11 April 2016 Suh, A. (2016). The phylogenomic forest of bird trees contains a hard polytomy at the root Accepted: 11 August 2016 of Neoaves. — Zoologica Scripta, 45,50–62. doi:10.1111/zsc.12213 Birds have arguably been the most intensely studied animal group for their phylogenetic relationships. However, the recent advent of genome-scale phylogenomics has made the for- est of bird phylogenies even more complex and confusing. Here, in this perspective piece, I show that most parts of the avian Tree of Life are now firmly established as reproducible phylogenetic hypotheses. This is to the exception of the deepest relationships among Neoaves. Using phylogenetic networks and simulations, I argue that the very onset of the super-rapid neoavian radiation is irresolvable because of eight near-simultaneous speciation events. Such a hard polytomy of nine taxa translates into 2 027 025 possible rooted bifurcat- ing trees. Accordingly, recent genome-scale phylogenies show extremely complex conflicts in this (and only this) part of the avian Tree of Life. I predict that the upcoming years of avian phylogenomics will witness many more, highly conflicting tree topologies regarding the early neoavian polytomy. I further caution against bootstrapping in the era of genomics and suggest to instead use reproducibility (e.g. independent methods or data types) as sup- port for phylogenetic hypotheses. The early neoavian polytomy coincides with the Creta- ceous–Paleogene (K-Pg) mass extinction and is, to my knowledge, the first empirical example of a hard polytomy. Corresponding author: Alexander Suh, Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, SE - 752 36, Uppsala, Sweden. E-mail: alexander.suh@ ebc.uu.se Alexander Suh, Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, SE - 752 36, Uppsala, Sweden. E-mail: [email protected] Introduction publicly available trees/data sets (Jarvis et al. 2014, 2015; The last few years have produced so many different phylo- Prum et al. 2015; Suh et al. 2015). This was complemented genetic trees of birds that it has become almost impossible with networks based on simulated nine-taxon gene trees to see the forest for the trees. It is thus about time to revisit from a random tree generator (Boc et al. 2012) and simu- recent contradictory claims from genome-scale studies and lated nine-taxon retroposon presence/absence patterns (i.e. to disentangle the degrees of conflict present in different all 512 possible strings of nine binary digits). parts of the avian Tree of Life. Nearly all of these conflicts involve the super-rapid radiation of Neoaves, the taxon The emerging consensus of a largely resolved comprising all extant birds but the lineages leading to chick- neoavian Tree of Life ens, ducks, ostriches, cassowaries and tinamous. The There have been numerous attempts to solve the Neoaves Neoaves problem has been intensely debated for decades. In problem. Each of these has seen extensive disagreement the following, I show that genome-scale phylogenomics has between and among studies, irrespective of whether the resolved most of these disputes, and I argue that the data type was morphology (e.g. Livezey & Zusi 2007), presence of a hard polytomy explains all of the remaining DNA–DNA hybridization (e.g. Sibley & Ahlquist 1990), irresolvable branches of the neoavian Tree of Life. mitochondrial genes (e.g. Pratt et al. 2009; Pacheco et al. To test for a hard polytomy, I generated phylogenetic 2011) or single nuclear genes (e.g. Fain & Houde 2004; networks in Splitstree4 (Huson & Bryant 2006) using Poe & Chubb 2004). If one were to draw a strict consensus 50 ª 2016 The Authors. Zoologica Scripta published by John Wiley & Sons Ltd on behalf of Royal Swedish Academy of Sciences, 45, s1, October 2016, pp 50–62 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. A. Suh A hard polytomy at the root of Neoaves of all these analyses, it would be an entirely unresolved studies (McCormack et al. 2013; Jarvis et al. 2014; Prum neoavian ‘Bush of Life’. et al. 2015; Suh et al. 2015), for example Otidimorphae Over the last ten years, this picture has changed dramati- (bustards + turacos + cuckoos), Columbimorphae (mesites cally with analyses of more and more nuclear loci. While + sandgrouse + doves), the Aequornithes/Phaethontimor- exons have been shown to be problematic for resolving the phae clade and Afroaves (core landbirds excluding Aus- neoavian radiation (Chojnowski et al. 2008; Jarvis et al. tralaves) (Fig. 1). 2014), other nuclear data types such as introns, ultracon- served elements (UCEs) and retroposon presence/absence Some neoavian relationships are more complex than patterns have become increasingly important. Analysing a bifurcating tree even just a few handfuls of unlinked nuclear loci has It is relieving that there are now robust and reproducible revealed some surprising relationships that since then have phylogenetic hypotheses for most aspects of the Neoaves been recovered relatively consistently, such as Psittaco- problem (Fig. 1). But genome-scale phylogenomics passerae (passerines + parrots), Mirandornithes (flamingos notwithstanding, why do there continue to be controversial + grebes), Telluraves (core landbirds) and Aequornithes branches at the base of core landbirds and unresolved (core waterbirds) (van Tuinen et al. 2001; Ericson et al. branches at the onset of the neoavian radiation? As so often 2006; Hackett et al. 2008; Suh et al. 2011, 2012; Wang in biology, things are a bit more complex than they seem. et al. 2012). Other, equally surprising relationships have First of all, the current mainstream approach of measur- only been discovered through analysis of hundreds or thou- ing and comparing ‘support’ in genome-scale phyloge- sands of unlinked nuclear loci, such as Phaethontimorphae nomics may be flawed, as nicely illustrated by the recent (sunbittern + tropicbirds), the turaco/bustard clade and the example of the enigmatic hoatzin. In their Nature paper, sandgrouse/mesite clade (McCormack et al. 2013; Jarvis Prum et al. (2015) stated that their ‘[...] concatenated Baye- et al. 2014; Prum et al. 2015; Suh et al. 2015). sian analyses resulted in a completely resolved, well supported Since the end of 2015, it has been safe to say that there phylogeny. [...] Almost all clades in the maximum likelihood is now a new and robust consensus for the neoavian Tree tree were maximally supported with bootstrap scores (BS) of of Life (Fig. 1). With the exception of the eight deepest 1.00’. They used this ‘support’ to group the hoatzin with speciation events of the neoavian radiation, there appear to core landbirds and name the ‘novel’ clade ‘Inopinaves’ be reproducible phylogenetic hypotheses for all other long- (Fig. S1B). However, the same argument was used in the standing aspects of the Neoaves problem. I emphasize that Science paper by Jarvis et al. (2014) to group the hoatzin this reproducibility lies not in high values for bootstrap or with cranes + shorebirds and name the ‘novel’ clade Bayesian posterior probabilities, the reasons for which will ‘Gruae’ (Fig. S1A). How can we trust bootstrap or Baye- be discussed below. Instead, the new neoavian Tree of Life sian posterior probabilities if different trees exhibit discor- is largely robust and reproducible because most relation- dant topologies that all have maximum ‘support’? Salichos ships have been recovered in at least two phylogenetic trees & Rokas (2013) foresaw this problem a few years ago based on independent methods or data types (Fig. 1). when they stated that ‘[...] relying on bootstrap to analyse These are four genome-scale phylogenies, namely the Jar- phylogenomic data sets is misleading, [...] because its application vis et al. (2014) TENT tree (48 taxa, 14 536 nuclear loci), will, even in the presence of notable conflict or systematic error, the McCormack et al. (2013) tree (32 taxa, 1541 UCE loci), almost always result in 100% values’. Genome-scale phyloge- the Prum et al. (2015) tree (198 taxa, 259 nuclear loci) and nomics thus urgently needs a paradigm shift, away from the Suh et al. (2015) tree (48 taxa, 2118 retroposon loci). overselling ‘novel’ clades and instead defining support as For comparison in Fig. 1, I also included the Jarvis et al. reproducibility of a phylogenetic hypothesis – that is, the (2014) UCE tree (48 taxa, 3769 UCE loci) and the histori- emergence of the same bifurcation in independent data cally important and widely known Hackett et al. (2008) tree sets analysed by independent research groups using inde- (169 taxa, 19 intron loci). pendent methods. Additionally, I hope that measures such What is the lesson to be learnt from all this? It is not as internode certainty (Salichos & Rokas 2013), now simply the addition of more data, but the replication of implemented in RAxML (Salichos et al. 2014), will soon such analyses via independent data types, independent replace bootstrap and conventional Bayesian posterior taxon samplings and different teams of researchers, that probabilities in genome-scale phylogenomics. A recent lends credibility to the new consensus of the avian Tree of study on complex speciation in tomatoes shows that this is Life. Not only does this apply to the aforementioned rela- feasible (Pease et al. 2016). Furthermore, Bayesian analyses tionships that have now been recovered consistently in using a reversible-jump Markov chain Monte Carlo phylogenomic analyses, but also to some clades that were approach yield more reliable Bayesian posterior probabili- newly found in at least two of the four genome-scale ties than conventional Bayesian analyses under uniform ª 2016 Royal Swedish Academy of Sciences, 45, s1, October 2016, pp 50–62 51 A hard polytomy at the root of Neoaves A.
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