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Re: Phylogeny and Taxonomy of Marine Mussels: Comments on the paper by Distel (2000)
Molecular Phylogenetics and Evolution Vol. 22, No. 2, February, pp. 330 –332, 2002 doi:10.1006/mpev.2001.1066, available online at http://www.idealibrary.com on
LETTER TO THE EDITOR Re: Phylogeny and Taxonomy of Marine Mussels: Comments on the paper by Distel (2000) To the Editor: Distel (2000) has recently studied the phylogenetic relationships between 12 recent marine mussels (Mytiloidea Rafinesque, 1815) belonging to six genera, and several taxa from related bivalve families, using the 18S rRNA gene sequence. In this paper, the author used the scheme for Mytilidae classification accepted by Newell (1969) and found evidence that Newell’s subfamily, Mytilinae Rafinesque, 1815 is polyphyletic. The author found that the rates of divergence between the studied Mytilidae genera 18S rRNA genes are nearly equal to those between other bivalve families. Distel also discussed the idea of polyphyletic convergent origin of modioliform and/or mytiliform body plans. I believe that there are three areas of Distel’s paper that require comment. First, the classification system based on paleontological data, which is usually known as Soot-Ryen’s (1969) and which has been used subsequently by both Newell and Distel, is not the only proposed classification scheme for mytilids. Following the first review by Soot-Ryen (1969), it became the usual practice to subdivide Mytilidae (Mytiloidea) into four subfamilies: Mytilinae; Crenellinae Gray, 1840; Lithophaginae H. Adams et A. Adams; 1857; and Modiolinae Keen, 1958. Subsequent schemes used by Bernard (1983) and Moore (1983) subdivided the family into the same subfamilies as Soot-Ryen (1969), but the composition of these subfamilies was quite different (see Kafanov, 1987). Habe (1977) later recognized a fifth subfamily, Musculinae Iredale, 1939; and Higo et al. (1999) supplemented the list of subfamilies by the Dacrydiinae Ockelmann, 1983 and Bathymodiolinae Kenk et Wilson, 1985. See Table 1. A very different system was proposed by Scarlato and Starobogatov (1979, 1984; Scarlato, 1981; Starobogatov, 1992), who subdivided the Myiloidea into four separate families: Mytilidae, Crenellidae, Septiferidae, and Lithophagidae. The latter is also considered a family in a recent review of northeast pacific bivalves (Coan et al., 2000). Furthermore, Scarlato and Starobogatov established an additional 13 subfamilies (see also Kafanov, 1987). Unfortunately, their diagnoses of taxa are extremely brief and they did not give arguments to support the proposed classification. Nevertheless, this scheme supports a polyphyletic origin of SootRyen’s Mytilinae. In Scarlato and Starobogatov (1979), 1055-7903/02 $35.00 © 2002 Elsevier Science (USA) All rights reserved.
an additional subfamily, Arcuatulinae has been established for the genera Arcuatula Lamy, 1919; Amygdalum Megerle von Muhlfeld, 1811; Geukensia Poel, 1959; Gregariella Monterosato, 1883; Mytella SootRyen, 1955; and Terua Dall, Bartch et Rehder, 1938. Thus, the situation of the species Hormomy: domingensis and Geukensia demissa in one cluster according to Distel’s study is not so surprising, and clearly supports the establishment of the Arcuatulinae. This study presents the facts that argue the interpretation of the Lithopaginae as a separate family (see above). Second, the relatively high divergence rate between the mytiloid taxa studied by Distel does not support the taxonomical level of the subfamilies Crenellinae Gray, 1840, Lithophaginae H. Adams et A. Adams, 1857, and Septiferinae Scarlato and Starobogatov, 1979. Recently, Kafanov and Drozdov (1998) studied sperm morphology of Mytiloidea. In terms of the presence or absence of an axial rod in the acrosome, they clearly classed the mytilids into two major groups: mussels possessing an axial rod belong to the more advanced (Popham, 1979) group around Mytilus, and those possessing no axial rod form the more primitive group around Modiolus (Linnaeus, 1758). Furthermore, they designated the path of mytilid spermatozoa evolution, based on DNA quantity and a mode of chromatin packing. Using these criteria, the Mytilus-type group consists of Mytilinae and more primitive Musculinae, while Septifer Nomura, 1936 would be the most advanced among the Modiolus-type group (which includes the other mytilids). The very similar Modiolus and Musculista Yamamoto et Habe, 1958 were found to be the most primitive. This study explains the origin of one joint cluster composed of Mytilinae and Musculinae (Crenellinae?), and the second cluster with the other taxa, as resulted in Distel’s paper. Based on both studies, it seems that the Mytiloidea consists of two major groups presumably at the family level. In this case, due to the resulting trade-off from the systems by Soot-Ryen (1969) and Scarlato and Starobogatov (1979), the family Mytilidae includes Mytilinae and Crenellinae (Musculinae), while the second family Lithophagidae H. et A. Adams, 1857 includes Lithophaginae, Modiolinae, Dacridiinae, Bathymodiolinae, and Septiferinae. In his paper, Distel preferred to reject the molecular clock assumption using marine mussel 18S rRNA, which is required to approve the taxonomical alternatives described above. Such a rejection requires support through additional and more representative investigations. The situation of Crenellinae
330
331
LETTER TO THE EDITOR
TABLE 1 Mytilid Genera Studied in Distel’s Paper: A Comparison of Classifications by Soot-Ryen (1969), Habe (1977), Bernard (1983), Moore (1983), Scarlato and Starobogatov (1979), and Higo et al. (1999) Soot-Ryen (1969), Bernard (1983), Moore (1983) Mytilus Linnaeus, 1758 Musculus Rosing, 1798 Modiolus Lamarck, 1799 Hormomya Morch, 1853 Geukensia Poel, 1959 Lithophaga Roding, 1798
a
Subfam. Mytilinae Rafinesque, 1825 Subfam. Crenellinae Gray, 1840
Scarlato and Starobogatov (1979)
Habe (1977), Higo et al. (1999)
Subfam. Mytilinae Rafinesque, 1825
Subfam. Mytilinae Rafinesque, 1825 Subfam. Musculinae Iredale, 1939
Subfam. Musculinae Iredale, 1939 Subfam. Modiolinae Keen, 1958
Subfam. Modiolinae Keen, 1958 Subfam. Lithophaginae H. et A. Adams, 1857
Fam. Arcuatulinae Scarlato et Starobogatov, 1979 Fam. Lithophagidae H. et A. Adams, 1857 Subfam. Adulianae H. et A. Adams, 1857
Subfam. Modiolinae Keen, 1958 Subfam. Lithophaginae H. et A. Adams, 1857
Partially after Kafanov (1987).
(as this subfamily is considered in the most recent reviews), as well as the validity of Musculinae subfamily name, remains obscure and also requires complementary studies. Third, the ancestry of Brachidontes to Modiolinae was proposed by Soot-Ryen (1969) while the later schemes by Bernard (1983), Moore (1983), Higo et al. (1999), and Coan et al. (2000) equivocally attribute this genus-to the Mytilinae. Distel had shown a polyphyletic origin of Mytilus and Brachidontes, i.e., the members of two distinct taxonomical groups (subfamilies). This leads to the idea of convergent evolution of a mytiliform body plan within the Mytiloidea. This thought may also be supported by the following. The Brachidontes lineage consists of both modioliform and mytiliform mussels, e.g., B. adamsianus and B.(H.) exustus, respectively. Further examination of phylogenetic relations within Brachidontes could clarify the evolution of the body plans within this lineage and relations to the other mytiliform taxa, e.g., Septifer, Perna, Stavelia, and Trichomya. All known fossil records of mytiliform mussels come from Jurassic or later periods, while the modioliforms were found in Devonian rocks (Newell, 1969). Several scholars had interpreted this fact as evidence for a relatively late origin of Mytilinae from Modiolinae or their closest relatives but not simultaneously from their common ancestors Modiolomorphidae in Devonian. Distel avoids unambiguous comments, probably because of incomplete paleontological records. Nevertheless, his molecular phylogeny leads to the hypothesis that Musculus-like mussels, which have a particular morphological resemblance to Modiolinae, may be considered the ancestors of Mytilinae; i.e., the mutual modioliform ancestor of both phyla descends from modiolomorphids.
ACKNOWLEDGMENTS I thank Dr. L. A. Beck and Dr. Ellen Kenchington for the review and valuable comments on the manuscript, and Dr. Alexander Kafanov and Eugenie Gladyshev for thoughtful discussion during the preparation of the manuscript.
REFERENCES Bernard, F. R. (1983). Catalogue of the living Bivalvia of the eastern Pacific Ocean: Bering Strait to Cape Horn. Can. Spes. Publ. Fish. Aquat. Sci. 61: 1–102. Coan, E. V., Scott P. V., and Bernard F. R. (2000). “Bivalve Seashells of Western North America: Marine Bivalve Mollusks from Arctic Alaska to Baja California,” Santa Barbara Museum of Natural History, Santa Barbara, CA. Distel, D. L. (2000). Phylogenetic relationships among Mytilidae (Bivalvia): 18S rRNA data suggest convergence in mytilid body plans. Mol. Phylogenet. Evol. 15: 25–33. Habe, T. (1977). “Systematics of Mollusca in Japan: Bivalvia and Scaphopoda,” Hokuryukan, Tokyo. Higo, S., Callomon, P., and Goto, Y. (1999). “Catalogue and Bibliography of the Marine Shell-Bearing Mollusca in Japan,” Elle Scientific Publications. p. 413– 421. Kafanov, A. I. (1987). Subfamily Mytilinae Rafinesque, 1815 (Bivalvia, Mytilidae) in the north Pacific Cenosoic. In “Fauna and Distribution of Mollusks: North Pacific and Polar Basin” (A. I. Kafanov, Ed.), pp. 65–103. Far East Science Center, Academy of Sciences of the USSR, Vladivostok. [in Russian]. Kafanov A. I., and Drozdov A. L. (1998). Comparative sperm morphology and phylogenetic classification of recent Mytiloidea (Bivalvia). Malacologia 39: 129 –139. Moore, E. J. (1983). “Tertiary Marine Pelecypods of California and Baja California: Nuculidae through Malleidae,” pp. 1–108. U. S. Geol. Surv. Prof. Paper 1228-A. Newell, N. D. (1969). Superfamily Mytilacea Rafinesque, 1815. In “Treatise on Invertebrate Paleontology” (P. C. Moore, Ed.), Part N, Vol. 1, Mollusca 6, Bivalvia, pp. 205–224. Geological Society of America and Univ. of Kansos.
332
LETTER TO THE EDITOR
Popham, J. D. (1979). Comparative spermatozoon morphology and bivalve phylogeny. Malacol. Rev. 12: 1–20. Scarlato, O. A. (1981). “Bivalve Mollusks from the west-Pacific Moderate Latitudes,” Nauka, Leningrad. [in Russian] Scarlato, O. A., and Starobogatov, A. I. (1979). A systematic position and distribution of the marine mussels. In “Commercial Bivalve Mollusks — Mussels and Their Role in the Ecosystems” pp. 106 – 111. Zool. Inst., Leningrad. [in Russian] Scarlato, O. A., and Starobogatov, A. I. (1984). A system of the suborder Mytileina (Bivalvia). Malacol. Rev. 13: 115–116. Soot-Ryen, T. (1969). Superfamily Mytilacea Rafinesque, 1815. In
“Treatise on Invertebrate Paleontology” (P. C. Moore, Ed.), Vol.1, Mollusca 6, Bivalvia, pp. 271–280. Geological Society of America and Univ. of Kansas. Starobogatov, A. I. (1992). Morphological basis for phylogeny and classification of Bivalvia. Ruthenica. Russ. Malacol. J. 2(1): 1–25.
Anton Y. Chichvarkhin Institute of Marine Biology Russian Academy of Sciences Vladivostok 690041, Russia E-mail: [email protected]
LETTER TO THE EDITOR Re: Phylogeny and Taxonomy of Marine Mussels: Comments on the paper by Distel (2000) To the Editor: Distel (2000) has recently studied the phylogenetic relationships between 12 recent marine mussels (Mytiloidea Rafinesque, 1815) belonging to six genera, and several taxa from related bivalve families, using the 18S rRNA gene sequence. In this paper, the author used the scheme for Mytilidae classification accepted by Newell (1969) and found evidence that Newell’s subfamily, Mytilinae Rafinesque, 1815 is polyphyletic. The author found that the rates of divergence between the studied Mytilidae genera 18S rRNA genes are nearly equal to those between other bivalve families. Distel also discussed the idea of polyphyletic convergent origin of modioliform and/or mytiliform body plans. I believe that there are three areas of Distel’s paper that require comment. First, the classification system based on paleontological data, which is usually known as Soot-Ryen’s (1969) and which has been used subsequently by both Newell and Distel, is not the only proposed classification scheme for mytilids. Following the first review by Soot-Ryen (1969), it became the usual practice to subdivide Mytilidae (Mytiloidea) into four subfamilies: Mytilinae; Crenellinae Gray, 1840; Lithophaginae H. Adams et A. Adams; 1857; and Modiolinae Keen, 1958. Subsequent schemes used by Bernard (1983) and Moore (1983) subdivided the family into the same subfamilies as Soot-Ryen (1969), but the composition of these subfamilies was quite different (see Kafanov, 1987). Habe (1977) later recognized a fifth subfamily, Musculinae Iredale, 1939; and Higo et al. (1999) supplemented the list of subfamilies by the Dacrydiinae Ockelmann, 1983 and Bathymodiolinae Kenk et Wilson, 1985. See Table 1. A very different system was proposed by Scarlato and Starobogatov (1979, 1984; Scarlato, 1981; Starobogatov, 1992), who subdivided the Myiloidea into four separate families: Mytilidae, Crenellidae, Septiferidae, and Lithophagidae. The latter is also considered a family in a recent review of northeast pacific bivalves (Coan et al., 2000). Furthermore, Scarlato and Starobogatov established an additional 13 subfamilies (see also Kafanov, 1987). Unfortunately, their diagnoses of taxa are extremely brief and they did not give arguments to support the proposed classification. Nevertheless, this scheme supports a polyphyletic origin of SootRyen’s Mytilinae. In Scarlato and Starobogatov (1979), 1055-7903/02 $35.00 © 2002 Elsevier Science (USA) All rights reserved.
an additional subfamily, Arcuatulinae has been established for the genera Arcuatula Lamy, 1919; Amygdalum Megerle von Muhlfeld, 1811; Geukensia Poel, 1959; Gregariella Monterosato, 1883; Mytella SootRyen, 1955; and Terua Dall, Bartch et Rehder, 1938. Thus, the situation of the species Hormomy: domingensis and Geukensia demissa in one cluster according to Distel’s study is not so surprising, and clearly supports the establishment of the Arcuatulinae. This study presents the facts that argue the interpretation of the Lithopaginae as a separate family (see above). Second, the relatively high divergence rate between the mytiloid taxa studied by Distel does not support the taxonomical level of the subfamilies Crenellinae Gray, 1840, Lithophaginae H. Adams et A. Adams, 1857, and Septiferinae Scarlato and Starobogatov, 1979. Recently, Kafanov and Drozdov (1998) studied sperm morphology of Mytiloidea. In terms of the presence or absence of an axial rod in the acrosome, they clearly classed the mytilids into two major groups: mussels possessing an axial rod belong to the more advanced (Popham, 1979) group around Mytilus, and those possessing no axial rod form the more primitive group around Modiolus (Linnaeus, 1758). Furthermore, they designated the path of mytilid spermatozoa evolution, based on DNA quantity and a mode of chromatin packing. Using these criteria, the Mytilus-type group consists of Mytilinae and more primitive Musculinae, while Septifer Nomura, 1936 would be the most advanced among the Modiolus-type group (which includes the other mytilids). The very similar Modiolus and Musculista Yamamoto et Habe, 1958 were found to be the most primitive. This study explains the origin of one joint cluster composed of Mytilinae and Musculinae (Crenellinae?), and the second cluster with the other taxa, as resulted in Distel’s paper. Based on both studies, it seems that the Mytiloidea consists of two major groups presumably at the family level. In this case, due to the resulting trade-off from the systems by Soot-Ryen (1969) and Scarlato and Starobogatov (1979), the family Mytilidae includes Mytilinae and Crenellinae (Musculinae), while the second family Lithophagidae H. et A. Adams, 1857 includes Lithophaginae, Modiolinae, Dacridiinae, Bathymodiolinae, and Septiferinae. In his paper, Distel preferred to reject the molecular clock assumption using marine mussel 18S rRNA, which is required to approve the taxonomical alternatives described above. Such a rejection requires support through additional and more representative investigations. The situation of Crenellinae
330
331
LETTER TO THE EDITOR
TABLE 1 Mytilid Genera Studied in Distel’s Paper: A Comparison of Classifications by Soot-Ryen (1969), Habe (1977), Bernard (1983), Moore (1983), Scarlato and Starobogatov (1979), and Higo et al. (1999) Soot-Ryen (1969), Bernard (1983), Moore (1983) Mytilus Linnaeus, 1758 Musculus Rosing, 1798 Modiolus Lamarck, 1799 Hormomya Morch, 1853 Geukensia Poel, 1959 Lithophaga Roding, 1798
a
Subfam. Mytilinae Rafinesque, 1825 Subfam. Crenellinae Gray, 1840
Scarlato and Starobogatov (1979)
Habe (1977), Higo et al. (1999)
Subfam. Mytilinae Rafinesque, 1825
Subfam. Mytilinae Rafinesque, 1825 Subfam. Musculinae Iredale, 1939
Subfam. Musculinae Iredale, 1939 Subfam. Modiolinae Keen, 1958
Subfam. Modiolinae Keen, 1958 Subfam. Lithophaginae H. et A. Adams, 1857
Fam. Arcuatulinae Scarlato et Starobogatov, 1979 Fam. Lithophagidae H. et A. Adams, 1857 Subfam. Adulianae H. et A. Adams, 1857
Subfam. Modiolinae Keen, 1958 Subfam. Lithophaginae H. et A. Adams, 1857
Partially after Kafanov (1987).
(as this subfamily is considered in the most recent reviews), as well as the validity of Musculinae subfamily name, remains obscure and also requires complementary studies. Third, the ancestry of Brachidontes to Modiolinae was proposed by Soot-Ryen (1969) while the later schemes by Bernard (1983), Moore (1983), Higo et al. (1999), and Coan et al. (2000) equivocally attribute this genus-to the Mytilinae. Distel had shown a polyphyletic origin of Mytilus and Brachidontes, i.e., the members of two distinct taxonomical groups (subfamilies). This leads to the idea of convergent evolution of a mytiliform body plan within the Mytiloidea. This thought may also be supported by the following. The Brachidontes lineage consists of both modioliform and mytiliform mussels, e.g., B. adamsianus and B.(H.) exustus, respectively. Further examination of phylogenetic relations within Brachidontes could clarify the evolution of the body plans within this lineage and relations to the other mytiliform taxa, e.g., Septifer, Perna, Stavelia, and Trichomya. All known fossil records of mytiliform mussels come from Jurassic or later periods, while the modioliforms were found in Devonian rocks (Newell, 1969). Several scholars had interpreted this fact as evidence for a relatively late origin of Mytilinae from Modiolinae or their closest relatives but not simultaneously from their common ancestors Modiolomorphidae in Devonian. Distel avoids unambiguous comments, probably because of incomplete paleontological records. Nevertheless, his molecular phylogeny leads to the hypothesis that Musculus-like mussels, which have a particular morphological resemblance to Modiolinae, may be considered the ancestors of Mytilinae; i.e., the mutual modioliform ancestor of both phyla descends from modiolomorphids.
ACKNOWLEDGMENTS I thank Dr. L. A. Beck and Dr. Ellen Kenchington for the review and valuable comments on the manuscript, and Dr. Alexander Kafanov and Eugenie Gladyshev for thoughtful discussion during the preparation of the manuscript.
REFERENCES Bernard, F. R. (1983). Catalogue of the living Bivalvia of the eastern Pacific Ocean: Bering Strait to Cape Horn. Can. Spes. Publ. Fish. Aquat. Sci. 61: 1–102. Coan, E. V., Scott P. V., and Bernard F. R. (2000). “Bivalve Seashells of Western North America: Marine Bivalve Mollusks from Arctic Alaska to Baja California,” Santa Barbara Museum of Natural History, Santa Barbara, CA. Distel, D. L. (2000). Phylogenetic relationships among Mytilidae (Bivalvia): 18S rRNA data suggest convergence in mytilid body plans. Mol. Phylogenet. Evol. 15: 25–33. Habe, T. (1977). “Systematics of Mollusca in Japan: Bivalvia and Scaphopoda,” Hokuryukan, Tokyo. Higo, S., Callomon, P., and Goto, Y. (1999). “Catalogue and Bibliography of the Marine Shell-Bearing Mollusca in Japan,” Elle Scientific Publications. p. 413– 421. Kafanov, A. I. (1987). Subfamily Mytilinae Rafinesque, 1815 (Bivalvia, Mytilidae) in the north Pacific Cenosoic. In “Fauna and Distribution of Mollusks: North Pacific and Polar Basin” (A. I. Kafanov, Ed.), pp. 65–103. Far East Science Center, Academy of Sciences of the USSR, Vladivostok. [in Russian]. Kafanov A. I., and Drozdov A. L. (1998). Comparative sperm morphology and phylogenetic classification of recent Mytiloidea (Bivalvia). Malacologia 39: 129 –139. Moore, E. J. (1983). “Tertiary Marine Pelecypods of California and Baja California: Nuculidae through Malleidae,” pp. 1–108. U. S. Geol. Surv. Prof. Paper 1228-A. Newell, N. D. (1969). Superfamily Mytilacea Rafinesque, 1815. In “Treatise on Invertebrate Paleontology” (P. C. Moore, Ed.), Part N, Vol. 1, Mollusca 6, Bivalvia, pp. 205–224. Geological Society of America and Univ. of Kansos.
332
LETTER TO THE EDITOR
Popham, J. D. (1979). Comparative spermatozoon morphology and bivalve phylogeny. Malacol. Rev. 12: 1–20. Scarlato, O. A. (1981). “Bivalve Mollusks from the west-Pacific Moderate Latitudes,” Nauka, Leningrad. [in Russian] Scarlato, O. A., and Starobogatov, A. I. (1979). A systematic position and distribution of the marine mussels. In “Commercial Bivalve Mollusks — Mussels and Their Role in the Ecosystems” pp. 106 – 111. Zool. Inst., Leningrad. [in Russian] Scarlato, O. A., and Starobogatov, A. I. (1984). A system of the suborder Mytileina (Bivalvia). Malacol. Rev. 13: 115–116. Soot-Ryen, T. (1969). Superfamily Mytilacea Rafinesque, 1815. In
“Treatise on Invertebrate Paleontology” (P. C. Moore, Ed.), Vol.1, Mollusca 6, Bivalvia, pp. 271–280. Geological Society of America and Univ. of Kansas. Starobogatov, A. I. (1992). Morphological basis for phylogeny and classification of Bivalvia. Ruthenica. Russ. Malacol. J. 2(1): 1–25.
Anton Y. Chichvarkhin Institute of Marine Biology Russian Academy of Sciences Vladivostok 690041, Russia E-mail: [email protected]