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Kuraku2009chap40.Pdf Jawless fi shes (Cyclostomata) Shigehiro Kurakua,b,*, Kinya G. Otaa, and genes (8–11), and protein-coding genes of the nuclear Shigeru Kuratania genomes (12–16). Here we review the phylogenetic rela- aLaboratory for Evolutionary Morphology, RIKEN Center for tionships and the divergence time of the two families of Developmental Biology, 2–2-3 Minatojima-minami, Chuo-ku, Kobe Cyclostomata. b 650–0047, Japan; Lehrstuhl für Zoologie und Evolutionsbiologie, Most molecular studies to date have concluded that Department of Biology, University of Konstanz, Universitätsstrasse Cyclostomata is a monophyletic group (see 17 and refer- 10, D-78457 Konstanz, Germany *To whom correspondence should be addressed (shigehiro.kuraku@ ences therein). 7 ese A ndings suggest that many primi- uni-konstanz.de) tive morphological traits found in hagA shes are just due to secondary losses in the hagA sh lineage, or that the pre- sumed primitive nature of the hagA sh morphology is due Abstract to the unavailability of detailed morphological descrip- tion, as recently exempliA ed by hagA sh embryonic Cyclostomata comprises two families of living jawless morphology (18). Rediscovery of cyclostome monophyly fi shes: hagfishes (Myxinidae, 44 species) and lampreys can be regarded as one of the most outstanding examples (Petromyzonidae, 41 species). Morphological analyses have in which molecular phylogenetics has resolved contro- favored the closer relationship of lampreys to jawed verte- versial phylogenetic relationships among major animal brates (gnathostomes) than to hagfi shes. However, most of groups (19). With this rediscovery, researchers can now the recent molecular phylogenetic analyses have supported estimate the timing of hagA sh–lamprey divergence using a hagfi sh–lamprey relationship. The estimated divergence molecular sequence information. time for hagfi shes and lampreys among several studies Phylogenetic studies have revealed that the hagA sh averages 482 million years ago (Ma), but varies (520–432 lineage exhibits a long branch, suggesting elevation of Ma) depending mostly on the assumed timing of the evolutionary rate at the molecular level in this lineage cyclostome–gnathostome divergence. Nonetheless, there (e.g., 17). For this reason, application of local clock ana- is agreement that hagfi sh and lamprey lineages diverged lysis is expected to improve the precision of divergence relatively shortly (within 100 million years) after the diver- time estimation, especially in this animal group. Using a gence of cyclostomes and gnathostomes. lineage-speciA c method, the hagA sh–lamprey divergence was estimated to be 499 (536–462) Ma in an analysis of Cyclostomata consists of two extant orders, Myxini- seven nuclear genes (20). A subsequent Bayesian analysis formes and Petromyzoniformes (1). Myxiniformes con- of 25 nuclear genes resulted in a slightly older estimate of tains a single family, Myxinidae that includes 44 species 520 (596–461) Ma (16). In this study, the minimum time in six genera (2) (hagA shes; Fig. 1). Petromyzoniformes constraint for hagA sh–lamprey divergence was incorpo- also consists of a single family, Petromyzonidae that rated based on fossil-based discoveries of extinct relatives includes 41 species in six genera (3) (lampreys, Fig. 1). Historically, hagA shes and lampreys have been classi- A ed as cyclostomes (“round mouth”) because both have a jawless mouth armed with retractable horny teeth (4). However, some morphological traits in hagA shes (e.g., lack of vertebrae, heart innervation, and eye lens) have been taken to suggest that lampreys are more closely related to jawed vertebrates (gnathostomes) than to hag- A shes (5). To settle this controversy, molecular phylo- Fig. 1 Two Japanese lampreys (Lethenteron japonicum) and an genetic studies have been conducted since the early inshore hagfi sh (Eptatretus burgeri, tangled). Credit: S. Kuraku 1990s using ribosomal DNA genes (6, 7), mitochondrial and K. G. Ota. S. Kuraku, K.G. Ota, and S. Kuratani. Jawless A shes (Cyclostomata). Pp. 317–319 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 331717 11/28/2009/28/2009 11:28:00:28:00 PPMM 318 THE TIMETREE OF LIFE Myxinidae 1 Petromyzonidae O S D C P Tr J K Pg PALEOZOIC MESOZOIC CZ 400 300 200 100 0 Million years ago Fig. 2 A timetree of jawless fi shes (Cyclostomata). Divergence times are shown in Table 1. Abbreviations: C (Carboniferous), CZ (Cenozoic), D (Devonian), J (Jurassic), K (Cretaceous), O (Ordovician), P (Permian), Pg (Paleogene), S (Silurian), and Tr (Triassic). Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) between jawless fi shes (Cyclostomata). Timetree Estimates Node Time Ref. (16) Ref. (17)(a) Ref. (17)(b) Ref. (20) Time CI Time CI Time CI Time CI 1 482.3 520.0 596–461 432.0 473–391 478.0 497–459 499.0 536–462 Note: Node times in the timetree represent the mean of time estimates from different studies. From ref. (17), estimates are presented from (a) nuclear and (b) mitochondrial data. of modern hagA shes and lampreys (325 Ma; 21 and ref- Acknowledgment erences therein). In a more recent study, the divergence Support was provided by Grants-in-Aid from the time of hagA shes and lampreys was estimated using dif- Ministry of Education, Science and Culture of Japan. ferent sets of genes (nuclear genes and mitochondrial genes) and calibration dates (molecules and fossils) (17). Application of molecular estimates (16, 22) as the max- References imum and minimum time constraints resulted in dates that are similar to the previous estimate (520 Ma; 16) or 1. M. W. Hardisty, Biology of the Cyclostomes (Chapman & Hall, London, 1979). much more ancient (612 Ma) (data not shown in Table 2. J. M. Jørgensen, e Biology of HagA shes, 1st ed. 1; see 17 for details). When the cyclostome– gnathostome (Chapman & Hall, London; New York, 1998). split is constrained at 500 Ma, however, the analysis 3. M. W. Hardisty, I. C. Potter, e Biology of Lampreys resulted in a 432 (473–391) Ma date based on 10 nuclear (Academic Press, London; New York, 1971). genes and 478 (497–459) Ma date based on 12 mitochon- 4. A. M. C. Duméril, Zoologie Analytique, ou Méthode drial genes for the hagA sh–lamprey divergence (17). Naturelle de ClassiA cation des Animaux, Rendue plus Since those studies were completed, the fossil record facile a l’Aide de Tableaux Synoptiques (Allais, Paris, of lampreys has been extended into the late Devonian 1806). (~360 Ma) (23), which is 11% older than the calibration 5. P. Janvier, Early Vertebrates (Clarendon Press; Oxford date that was used for the divergence of hagA shes and University Press, Oxford, England, New York, NY, 1996). lampreys (16). 6. J. Mallatt, J. Sullivan, Mol. Biol. Evol. 15, 1706 (1998). 7. D. W. Stock, G. S. Whitt, Science 257, 787 (1992). While the estimates of hagA sh–lamprey divergence 8. C. Delarbre et al., Mol. Biol. Evol. 17, 519 (2000). times are highly variable, depending on the calibrations 9. C. Delarbre, C. Gallut, V. Barriel, P. Janvier, G. Gachelin, used, all available studies unequivocally suggest that the Mol. Phylogenet. Evol. 22, 184 (2002). ancestors of Myxinidae (hagA shes) and Petromyzonidae 10. C. Delarbre, A. S. Rasmussen, U. Arnason, G. Gachelin, (lampreys) diverged relatively soon (less than 100 mil- J. Mol. Evol. 53, 634 (2001). lion years) aJ er the ancestors of cyclostomes split from 11. A. S. Rasmussen, A. Janke, U. Arnason, J. Mol. Evol. 46, the gnathostome lineage. 382 (1998). HHedges.indbedges.indb 331818 11/28/2009/28/2009 11:28:02:28:02 PPMM Eukaryota; Metazoa; Vertebrata; Cyclostomata 319 12. F. Delsuc, H. Brinkmann, D. Chourrout, H. Philippe, 19. A. Meyer, R. Zardoya, Annu. Rev. Ecol. Evol. Syst. 34, 311 Nature 439, 965 (2006). (2003). 13. N. Takezaki, F. Figueroa, Z. Zaleska-Rutczynska, J. Klein, 20. S. B. Hedges, in Major Events in Early Vertebrate Mol. Biol. Evol. 20, 287 (2003). Evolution, P. E. Ahlberg, Ed. (Taylor & Francis, London, 14. S. Kuraku, D. Hoshiyama, K. Katoh, H. Suga, T. Miyata, 2001), pp. 119–134. J. Mol. Evol. 49, 729 (1999). 21. P. C. J. Donoghue, M. P. Smith, I. J. Sansom, in Telling the 15. R. F. Furlong, P. W. H. Holland, Zool. Sci. 19, 593 (2002). Evolutionary Time, P. C. J. Donoghue, M. P. Smith, Eds. 16. J. E. Blair, S. B. Hedges, Mol. Biol. Evol. 22, 2275 (2005). (Taylor & Francis, London, 2003), pp. 190–223. 17. S. Kuraku, S. Kuratani, Zool. Sci. 23, 1053 (2006). 22. S. Kumar, S. B. Hedges, Nature 392, 917 (1998). 18. K. G. Ota, S. Kuraku, S. Kuratani, Nature 446, 672 23. R. W. Gess, M. I. Coates, B. S. Rubidge, Nature 443, 981 (2007). (2006). HHedges.indbedges.indb 331919 11/28/2009/28/2009 11:28:02:28:02 PPMM.
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