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Near2009chap42.Pdf Ray-fi nned fi shes (Actinopterygii) Thomas J. Neara,* and Masaki Miyab have been raised regarding the phylogenetic a1 nities aDepartment of Ecology and Evolutionary Biology & Peabody of polypteriforms within Actinopterygii with an alter- Museum of Natural History, Yale University, New Haven, CT 06520, native hypothesis that they are more closely related to b USA; Natural History Museum and Institute, Chiba, 955-2 Aoba- sarcopterygians (4–6). Phylogenetic analyses of morpho- cho, Chuo-ku, Chiba 260-8682, Japan logical characters have supported the hypothesis that *To whom correspondence should be addressed (thomas.near@ yale.edu) Polypteriformes is most closely related to all other extant actinopterygians (1, 7–15). 7 e phylogenetic position of Polypteriformes consistently inferred from morpho- Abstract logical data has also been supported in phylogenetic ana- lyses of nuclear encoded 28S rRNA gene sequences (16, Extant Actinopterygii, or ray-fi nned fi shes, comprise fi ve 17), DNA sequences from whole mitochondrial genomes major clades: Polypteriformes (bichirs), Acipenseriformes (18, 19), and a combined data analysis of seven single- (sturgeons and paddlefi shes), Lepisosteiformes (gars), copy nuclear genes (20). Amiiformes (bowfi n), and Teleostei, which contains more 7 ere is little doubt that the A ve major actinoptery- than 26,890 species. Phylogenetic analyses of morph- gian clades are each monophyletic (Amiiformes contains ology and DNA sequence data have typically supported only a single extant species, Fig. 1). However, the hypoth- Actinopterygii as an evolutionary group, but have disagreed eses of relationships among these clades have diB ered on the relationships among the major clades. Molecular dramatically among analyses of both morphological divergence time estimates indicate that Actinopterygii and molecular data sets. 7 ese discrepancies involve diversifi ed in the Lower Devonian (416–397 million years the relationships of Amiiformes and Lepisosteiformes, ago, Ma), and the major clades had diversifi ed by the end of and whether Amiiformes, Acipenseriformes, and the Carboniferous (~300 Ma). Lepisosteiformes form an “ancient A sh” clade. Perhaps the most problematic aspect of actinop- Actinopterygii, or ray-A nned A shes, are one of the two terygian phylogenetics involves the relationship of major lineages of osteichthyan vertebrates, the other Lepisosteiformes and Amiiformes. 7 ese two lineages being Sarcopterygii (1). 7 ere are more than 26,890 spe- were traditionally grouped together along with sev- cies of actinopterygian A shes and the group has diversi- eral extinct lineages in the Holostei (21, 22). Analyses A ed into a wide range of marine and freshwater habitats of morphological characters has resulted in an alterna- (2). Typically A ve major clades are recognized in Actin- tive hypothesis that Amiiformes is the closest relative of opterygii: Polypteriformes (bichirs), Acipenseriformes Teleostei and Lepisosteiformes is most closely related to (sturgeons and paddleA shes), Lepisosteiformes (gars), this clade (23–30). However, other morphological studies Amiiformes (BowA n), and Teleostei. In this account, (4, 31–33), and molecular phylogenetic analyses of both we review the evidence presented for the monophyly of nuclear and mtDNA gene sequences, have resulted in a Actinopterygii, the phylogenetic hypotheses of relation- monophyletic Holostei (16, 19, 20, 29, 34). ships among the major actinopterygian clades, and the inferences of divergence times resulting from analyses of DNA sequence data sampled from whole mitochondrial genomes and nuclear genes. 7 e only plausible skepticism regarding the mono- phyly of actinopterygians was directed speciA cally at the phylogenetic relationships of Polypteriformes. Since the early part of the twentieth century polypteriforms have Fig. 1 The only extant amiiform species (Amia calva), from been considered actinopterygians (3) however, doubts Texas, USA. Credit: B. H. Bauer. T.J. Near and M. Miya. Ray-A nned A shes (Actinopterygii). Pp. 328–331 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 332828 11/28/2009/28/2009 11:28:07:28:07 PPMM Eukaryota; Metazoa; Vertebrata; Actinopterygii 329 Lepisosteiformes 4 3 Acipenseriformes 2 Amiiformes 1 Teleostei Polypteriformes D C P Tr J K Pg Ng PALEOZOIC MESOZOIC CZ 400 300 200 100 0 Million years ago Fig. 2 A timetree of ray-fi nned fi shes (Actinopterygii). Divergence times are shown in Table 1. Abbreviations: C (Carboniferous), CZ (Cenozoic), D (Devonian), J (Jurassic), K (Cretaceous), Ng (Neogene), P (Permian), Pg (Paleogene), and Tr (Triassic). One of the more recent controversies in actinoptery- Sarcopterygii, and these studies attempted to estimate gian phylogenetics involves the phylogenetic analysis of divergence times among all major deuterostome or ver- whole mitochondrial genome sequences that A nds the tebrate lineages. Pairwise genetic distances of amino acid Amiiformes, Lepisosteiformes, and Acipenseriformes sequences sampled from 44 genes and calibrated with a form a clade that is most closely related to Teleostei. single amniote fossil resulted in an age estimate for the 7 is has been referred to as the “ancient A sh” clade (19). split of Actinopterygii and Sarcopterygii at 450 ± 35.5 Maximum likelihood Kishino-Hasegawa tree topology Ma (36). To account for heterogeneity of molecular evo- tests using the whole mitochondrial genome sequences lutionary rates among lineages, Kumar and Hedges (36) were unable to reject several more traditional hypotheses excluded genes that exhibited rate heterogeneity. A very of actinopterygian relationships, including Holostei as similar study that diB ered by using a combination of fos- being most closely related to Teleostei, Amiiformes most sil and molecular calibrations resulted in a nearly iden- closely related to Teleostei, and a polytomy involving tical age estimate for the Actinopterygii–Sarcopterygii Lepisosteiformes, Amiiformes, and Teleostei (19). Inoue split (37). A more recent study provided an age estimate et al. (19) cite support for the “ancient A sh” clade in a study of 476 Ma with a 95% credibility interval (CI) of (494– examining relationships among jawed vertebrates using 442) for the Actinopterygii–Sarcopterygii split using insertions and deletions of amino acid sites in nuclear amino acid sequences from 325 nuclear genes analyzed genes (35). 7 is study did not support the monophyly of with a Bayesian local clock method and calibrated with a clade containing Lepisosteiformes, Amiiformes, and 13 fossils (38). Acipenseriformes, but only provided apomorphic char- 7 e second group of studies speciA cally addressed the acter states to distinguish two clades, one containing divergence times among the major extant actinoptery- Amiiformes, Lepisosteiformes, Acipenseriformes, and gian clades, and provides age estimates for the common Teleostei (Actinopteri), and Teleostei as distinct from the ancestor of all living actinopterygians. Inoue et al. (39) Actinopteri (35). 7 e inability of data sets consisting of presented a time-calibrated phylogeny estimated using whole mitochondrial genomes or multiple nuclear genes amino acid sequences from 26 mitochondrial genomes to reject alternative phylogenetic relationships among sampled among Polypteriformes, Acipenseriformes, the major actinopterygian lineages indicates that much Lepisosteiformes, Amiiformes, and Teleostei. 7 e time- work remains to resolve these relationships (19, 33). tree is shown in Fig. 2, and the phylogeny depicts a slight Several studies have presented molecular divergence alteration of the “ancient A sh” clade presented in an earl- time estimates for the Actinopterygii. Yet, these investi- ier study (19). Divergence times were estimated with a gations diB er in the type of data sampled, the calibrations partitioned Bayesian strategy using the computer pro- used to convert estimated genetic divergence to absolute gram Multidivtime, and a set of 13 fossil calibrations. age estimates, and the methods used to account for rate Interestingly, the molecular age estimate for the com- heterogeneity among lineages. mon ancestor of all living Actinopterygii overlaps com- 7 e Arst set of studies discussed in this review pletely with the conA dence interval estimated for the address the age of the split between Actinopterygii and lower bound age of actinopterygians at 425.6 Ma using HHedges.indbedges.indb 332929 11/28/2009/28/2009 11:28:08:28:08 PPMM 330 THE TIMETREE OF LIFE Table 1. Divergence time estimates (Ma) and their confi dence/ 7 e molecular divergence times estimated for Actin- credibility intervals (CI) among ray-fi nned fi shes (Actinopterygii). opterygii support observations from the fossil record Timetree Estimates that the early diversiA cation of this clade occurred in the Paleozoic (10–12). 7 ese age estimates also indicate that Node Time Ref. (19) Ref. (33) the diversiA cation of the major extant actinopterygian Time CI Time CI clades also occurred in the Paleozoic, with subsequent 1 407.0 407 376–446 – – diversiA cation of major teleost clades occurring in the 2 343.0 343 310–381 372 347–391 late Paleozoic and Mesozoic. 7 e molecular age estimate 3327.0327295–366– – presented for the split of Teleostei from other actinop- 4 312.0 312 279–351 – – terygians (Table 1) is more than 100 Ma older than the earliest teleost fossils (e.g., Pholidophorus) that date to the Note: Node times in the timetree are from ref. (19). Middle Triassic (26, 41,
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