Revisiting metazoan phylogeny with genomic sampling of all phyla

Abstract

Proper biological interpretation of a phylogeny can sometimes hinge on the placement of key taxa—or fail when such key taxa are not sampled. In this light, we here present the first attempt to investigate (though not conclusively resolve) animal relationships using genome-scale data from all phyla. Results from the site-heterogeneous CAT + GTR model recapitulate many established major clades, and strongly confirm some recent discoveries, such as a monophyletic Lophophorata, and a sister group relationship between Gnathifera and Chaetognatha, raising continued questions on the nature of the spiralian ancestor. We also explore matrix construction with an eye towards testing specific relationships; this approach uniquely recovers support for Panarthropoda, and shows that Lophotrochozoa (a subclade of Spiralia) can be constructed in strongly conflicting ways using different taxon- and/or orthologue sets. Dayhoff-6 recoding sacrifices information, but can also reveal surprising outcomes, e.g. full support for a clade of Lophophorata and Entoprocta + Cycliophora, a clade of Placozoa + Cnidaria, and raising support for Ctenophora as sister group to the remaining Metazoa, in a manner dependent on the gene and/or taxon sampling of the matrix in question. Future work should test the hypothesis that the few remaining uncertainties in animal phylogeny might reflect violations of the various stationarity assumptions used in contemporary inference methods.

Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses

“…Organismal scope or featured taxon Cunha & Giribet (2019) yes Gastropods Laumer et al (2019) yes Animals Lemer et al (2019) yes Bivalves Lozano-Fernandez et al (2019) yes Chelicerates Marlétaz et al (2019) yes Spiralia Philippe et al (2019) yes Bilateria Narayanan Kutty et al (2019) no Calyptratae Uribe et al (2019) no Gastropods Wolfe et al (2019) no Decapod crustaceans Zverkov et al (2019) no Dicyemida and Orthonectida Aouad et al (2018) yes Archaea Laumer et al (2018) yes Placozoa Otero-Bravo et al (2018) yes Pantoea Puttick et al (2018) yes Land plants Schwentner et al (2018) yes Pancrustacea Sousa et al (2018) yes Land plants Bennett & Mao (2018) no Fulgoroidea symbionts Eitel et al (2018) no Placozoa Manzano-Marín et al (2018) no Cinara strobi symbionts Feuda et al (2017) yes Animals Szabó et al (2017) yes Pseudococcidae symbionts Williams et al (2017) yes Archaea Schwentner et al (2017) no Pancrustacea Shin et al (2017) no Curculionoidea Simion et al (2017) no Animals Yoshida et al (2017) no Tardigrades Leliaert et al (2016) yes Viridiplantae Zhang et al (2016) yes Roseobacter CHAB-I-5 lineage He et al (2016) no Rhizaria Song et al (2016) no Holometabola Domman et al (2015) yes Plastids Luo (2015) yes SAR11 Petitjean et al (2015) yes Archaea Borowiec et al (2015) no Animals Derelle et al (2015) no Eukaryotes Wang & Wu (2015) no Mitochondria…”

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…This indicates that lox2 evolved only after split of the common ancestor of those clades from remaining Spiralia and does not belong to the ancestral hox complement of all Spiralia (16). Whether absence of lox2 in lophophorates is plesiomorphic or represents evolutionary reversal depends on the position of Lophophorata within Spiralia, which is still debatable and not fully resolved (52)(53)(54)(55)94).…”

“…Brachiopoda -into the group called Lophophorata (50,51), which recently gained support as a valid clade from several transcriptomic and phylogenomic studies (52)(53)(54)(55). Although originally the Lophophorata were considered as deuterostomes (50,51), molecular data showed their protostome affinity (56) and currently the lophophorates occupy a wellsupported position within the clade of Spiralia (52)(53)(54)(55)57). Phoronids develop through a distinctive planktotrophic larval stage, called actinotrocha (58)(59)(60)(61).…”

“…ancestor of all phoronids. Recent studies are favoring a sister group relationship between phoronids and ectoprocts(52)(53)(54)(55)94), the latter of which possesses a mineralized external shell similarly as brachiopods. However, the Hox gene survey using degenerate polymerase chain reaction primers in ectoproct Crisularia (Bugula) turrita did not retrieve neither scr nor post1 sequences(95), which questions the possible correlation between loss of scr and post1 and the reduction of shell secreting tissues in phoronid lineage.…”

Hox gene expression during development of the phoronid Phoronopsis harmeri

“…1a). Due to the presence of lophophore, Phoronida have been traditionally united with two other clades-Ectoprocta (Bryozoa) and Brachiopoda-into the group called Lophophorata [50,51], which recently gained support as a valid clade from several transcriptomic and phylogenomic studies [52][53][54][55]. Although originally the Lophophorata were considered as deuterostomes [50,51], molecular data showed their protostome affinity [56] and currently the lophophorates Fig.…”