A novel transient structure with phylogenetic implications found in ratite spermatids

BMC Evolutionary Biology

John T Soley¹  Lizette du Plessis² 

[1] Department of Anatomy and Physiology, Faculty of Veterinary Science, University of Pretoria, Onderstepoort 0110, South Africa;Electron Microscope Unit, Department of Anatomy and Physiology, Faculty of Veterinary Science, University of Pretoria, Onderstepoort 0110, South Africa

关键词: Phylogenetics;    Spermiogenesis;    Ratites;   

Others  :  1087315
DOI  :  10.1186/1471-2148-13-104

 received in 2013-03-14, accepted in 2013-05-21,  发布年份 2013

【 摘 要 】

Background

A novel transient structure was observed in the spermatids of three ratite species using transmission electron microscopy.

Results

The structure first appeared at the circular manchette stage of sperm development, was most prominent during the longitudinal manchette phase and disappeared abruptly prior to spermiation. It was composed of regularly-spaced finger-like projections which were closely associated with the outer nuclear membrane, giving the nucleus a cogwheel-like appearance. The projections were approximately 30 nm long and 14 nm wide. Although a similar structure has been described in certain lizard and crocodile species, this is the first report of a similar structure in the developing spermatids of birds.

Conclusions

The potential value of non-traditional characters, such as spermiogenesis and sperm ultrastructure, as phylogenetic markers has recently been advocated. The morphologically unique structure found in ratite spermatids provides additional evidence of a possible phylogenetic link between the reptiles and birds. It also endorses the basal positioning of the ratites as a monophyletic group within the avian phylogenetic tree.

【 授权许可】

   
2013 du Plessis and Soley; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Ericson PGP: Current perspectives on the evolution of birds. Contrib Zool 2008, 77:109-116.
• [2]Hackett SJ, Kimbali RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T: A phylogenomic study of birds reveals their evolutionary history. Science 2008, 320:1763-1768.
• [3]Cracraft J: The major clades of birds. In The Phylogeny and Classification of Tetrapods. Edited by Benton MJ. Oxford: Clarendon Press; 1988:339-361.
• [4]Cracraft J, Mindell DP: The early history of modern birds: A comparison of molecular and morphological evidence. In The hierarchy of life. Edited by Fernholm B, Bremer K, Jörnvall H. Amsterdam: Elsevier Science Publishers; 1989:389-403.
• [5]Leonard L, Dyke GJ, van Tuinen M: A new specimen of the fossil palaeognath Lithornis from the lower Eocene of Denmark. Am Mus Novit 2005, 3491:1-11.
• [6]Sibley CG, Ahlquist JE: The phylogeny and relationships of the ratite birds as indicated by DNA-DNA hybridization. In Evolution Today. Edited by Scudder GCE, Reveal JL. Pittsburgh: Hunt Institute for Botanical Documentation, Carnegie-Mellon University; 1981:301-335.
• [7]Sibley CG, Ahlquist JE: Phylogeny and classification of birds. New Haven: Yale University Press; 1995.
• [8]Sibley CG, Ahlquist JE, Monroe BL: A classification of the living birds of the world based on DNA-DNA hybridization studies. Auk 1988, 105:409-423.
• [9]Paton T, Haddrath O, Baker AJ: Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds. Proc R Soc B 2002, 269:839-846.
• [10]García-Moreno J, Sorenson M, Mindell DP: Congruent avian phylogenies inferred from mitochondrial and nuclear DNA sequences. J Mol Evol 2003, 57:27-37.
• [11]Janke A, Arnason U: The complete mitochondrial genome of Alligator mississippiensis and the separation between recent Archosauria (birds and crocodiles). Mol Biol Evol 1997, 14:1266-1272.
• [12]Mindell DP, Sorenson MD, Dimcheff DE, Hasegawa M, Ast JC, Yuri T: Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. Syst Biol 1999, 48:138-152.
• [13]Van Tuinen M, Sibley CG, Hedges SB: The early history of modern birds inferred from DNA sequences of nuclear and mitochondrial ribosomal genes. Mol Biol Evol 2000, 17:451-457.
• [14]Braun EL, Kimball RT: Examining basal avian divergences with mitochondrial sequences: model complexity, taxon sampling, and sequence length. Syst Biol 2002, 51:614-625.
• [15]Haddrath O, Baker AJ: Multiple nuclear genes and retroposons support vicariance and dispersal of the paleaognaths, and an Early Cretaceous origin of modern birds. Proc R Soc Lond 2012, 279:4617-4625.
• [16]Koehler LD: Diversity of avian spermatozoa ultrastructure with emphasis on the members of the order Passeriformes. Memoir Mus Natl Hist 1995, 166:437-444.
• [17]Jamieson BMG: Avian spermatozoa: structure and phylogeny. In Reproductive Biology and Phylogeny of Birds Part A. Edited by Jamieson BMG. Jersey: Science Publishers; 2007:349-512.
• [18]Gribbins KM: Reptilian spermatogenesis: a histological and ultrastructural perspective. Spermatogenesis 2011, 1:250-269.
• [19]Aire TA: Spermatogenesis and testicular cycles. In Reproductive Biology and Phylogeny of Birds Part A. Edited by Jamieson BMG. Jersey: Science Publishers; 2007:279-348.
• [20]Phillips DM, Asa CS: Development of spermatozoa in the rhea. Anat Record 1989, 223:276-282.
• [21]Baccetti B, Burrini AG, Falchetti E: Spermatozoa and relationships in Palaeognath birds. Biol Cell 1991, 71:209-216.
• [22]Soley JT: Centriole development and formation of the flagellum during spermiogenesis in the ostrich (Struthio camelus). J Anat 1994, 185:301-313.
• [23]Soley JT: Differentiation of the acrosomal complex in ostrich (Struthio camelus) spermatids. J Morphol 1996, 227:101-111.
• [24]Soley JT: Nuclear morphogenesis and the role of the manchette during spermiogenesis in the ostrich (Struthio camelus). J Anat 1997, 190:563-576.
• [25]Du Plessis L, Soley JT: Abaxial tail implantation in the emu, Dromaius novaehollandiae: morphological characteristics and origin of a rare avian sperm defect. Theriogenology 2012, 77:1137-1143.
• [26]Nagano T: Observations on the fine structure of the developing spermatid in the domestic chicken. J Cell Biol 1962, 14:193-205.
• [27]McIntosh JR, Porter KR: Microtubules of the spermatids of the domestic fowl. J Cell Biol 1967, 35:153-173.
• [28]Tingari MD: Observations on the fine structure of spermatozoa in the testis and excurrent ducts of the male fowl, Gallus domesticus. J Reprod Fertil 1973, 34:255-265.
• [29]Okamura F, Nishiyama H: The early development of the tail and the transformation of the shape of the nucleus of the spermatid of the domestic fowl, Gallus gallus. Cell Tissue Res 1976, 169:345-359.
• [30]Gunawardana VK, Scott MGAD: Ultrastructural studies on the differentiation of spermatids in the domestic fowl. J Anat 1977, 124:741-755.
• [31]Sprando RL, Russell D: Spermiogenesis in the red-ear turtle (Pseudemys scripta) and the domestic fowl (Gallus domesticus): a study of cytoplasmic events including cell volume changes and cytoplasmic elimination. J Morphol 1988, 198:95-118.
• [32]Lin M, Jones RC: Spermiogenesis and spermiation in the Japanese quail (Coturnix coturnix japonica). J Anat 1993, 183:525-535.
• [33]Maretta M: Formation and role of the manchette microtubules in the poultry spermatids. Acta Vet Brno 1995, 64:23-29.
• [34]Aire TA: Ultrastructural study of spermiogenesis in the turkey, Meleagris gallopavo. Brit Poultry Sci 2003, 44:674-682.
• [35]Tripepi S, Jamieson BGM, Brunelli E: Ultrastructure of the spermatid of Caprimulgus europaeus Linnaeus 1758, the European nightjar (Aves; Caprimulgidae), with phylogenetic implications. J Morphol 2006, 267:1157-1164.
• [36]Lovas EM, Filippich LJ, Johnston SD: Spermiogenesis in the Australian cockatiel Nymphicus hollandicus. J Morphol 2012, 273:1291-1305.
• [37]Da Cruz-Landim C, Da Cruz-Höfling MA: Electron microscope study of lizard spermiogenesis in Tropidurus torquatus (Lacertilia). Caryologia 1977, 30:151-162.
• [38]Da Cruz-Höfling MA, Da Cruz-Landim C: The fine structure of nuclei during spermiogenesis in the lizard Tropidurus torquatus (Lacertilia). Cytologia 1978, 43:61-68.
• [39]Butler RD, Gabri MS: Structure and development of the sperm head in the lizard Podarcis (=Lacerata) taurica. J Ultrastruct Res 1984, 88:261-274.
• [40]Al-Hajj H, Janakat S, Mahmoud F: Electron microscopic study of sperm head differentiation in the lizard Agama stellio. Can J Zoolog 1987, 65:2959-2968.
• [41]Vieira GHC, Wiederhecker HC, Colli GR, Báo SN: Spermiogenesis and testicular cycle of the lizard Tropidurus torquatus (Squamata, Tropiduridae) in the Cerrado of central Brazil. Amphibia-Reptilia 2001, 22:217-233.
• [42]Ferreira A, Dolder H: Sperm ultrastructure and spermiogenesis in the lizard, Tropidurus itambere. Biol Cell 2003, 27:353-362.
• [43]Saita A, Comazzi M, Perrotta E: Electron microscope study of spermiogenesis in Caiman crocodylus L. Ital J Zool 1987, 4:307-318.
• [44]Clark AW: Some aspects of spermiogenesis in a lizard. Am J Anat 1967, 121:369-400.
• [45]Phillips DM: Development of spermatozoa in the woolly opossum with special reference to the shaping of the sperm head. J Ultrastruct Res 1970, 33:369-380.
• [46]Phillips DM: Spermiogenesis. New York: Academic Press; 1974.
• [47]Myles DG, Hepler PK: Shaping of the sperm nucleus in Marsilea: A distinction between factors responsible for shape generation and shape determination. Dev Biol 1982, 90:238-252.
• [48]Barth AD, Oko RJ: Abnormal morphology of bovine spermatozoa. Ames: Iowa State University Press; 1989.
• [49]Russell LD, Russell JA, MacGregor GR, Meistrich ML: Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am J Anat 1991, 192:97-120.
• [50]Hermo L, Pelletier R-M, Cyr DG, Smith CE: Surfing the wave, cycle, life history, and genes/protein expressed by testicular germ cells. Part 2: Changes in spermatid organelles associated with development of spermatozoa. Micros Res Techniq 2010, 73:279-319.
• [51]MacKinnon EA, Abraham PJ, Svatek A: Long link induction between the microtubules of the manchette in intermediate stages of spermiogenesis. Z Zellforsch Mik Ana 1973, 136:447-460.
• [52]Maretta M: The ultrastructure of the spermatozoon of the drake. Acta Vet Brno 1975, 25:47-52.
• [53]Cracraft J: Phylogeny and evolution of the Ratite birds. Ibis 1974, 116:494-521.
• [54]Cracraft J: Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event. Proc R Soc Lond B 2001, 268:459-469.
• [55]Haddrath O, Baker AJ: Complete mitochondrial DNA genome sequences of extinct birds: Ratite phylogenetics and the vicariance biogeography hypothesis. Proc R Soc Lond B 2001, 268:939-945.
• [56]Johnston P: New morphological evidence supports congruent phylogenies and Gondwana vicariance for palaeognathous birds. Zool J Linn Soc-Lond 2011, 163:959-982.
• [57]Simões K, Orsi AM, Viegas KAS: Ultrastructural characteristics of spermiogenesis in the domestic duck (Anas platyrhynchos). Anat Histol Embryol 2005, 34:307-311.
• [58]Harshman J, Braun EL, Braun MJ, Huddleston CJ, Bowie RCK, Chojnowski JL, Hackett SJ, Han K-L, Kimball RT, Marks BD, Miglia KJ, Moore WS, Reddy S, Sheldon FH, Steadman DW, Steppan SJ, Witt CC, Yuri T: Phylogenetic evidence for multiple losses of flight in ratite birds. PNAS 2008, 105:13462-13467.
• [59]Smith JV, Braun EL, Kimball RT: Ratite nonmonophyly: independent evidence from 50 novel loci. Syst Biol 2013, 62:35-49.
• [60]Stapel SO, Leunissen JAM, Versteeg M, Wattel J, de Jong WW: Ratites as oldest offshoot of avian stem – evidence from α-crystallin A sequences. Nature 1984, 311:257-259.
• [61]Walker AD: New light on the origin of birds and crocodiles. Nature 1972, 237:257-266.
• [62]Whetstone KN, Martin LD: New look at the origin of birds and crocodiles. Nature 1979, 279:234-235.
• [63]Rest JS, Ast JC, Austin CC, Waddell PJ, Tibbetts EA, Hay JM, Mindell DP: Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Mol Phylogenet Evol 2003, 29:289-297.
• [64]Fraser RDB, Parry DAD: The structural basis of the filament-matrix texture in the avian/reptilian group of hard β-keratins. J Struct Biol 2011, 173:391-405.
• [65]Gower DJ, Weber E: The braincase of Euparkeria, and the evolutionary relationships of birds and crocodilians. Biol Rev 1998, 73:367-411.
• [66]Schweitzer MH, Wittmeyer JL, Horner JR: Gender-specific reproductive tissue in ratites and Tyrannosaurus rex. Science 2005, 308:1456-1460.
• [67]Feduccia A: Explosive evolution in tertiary birds and mammals. Science 1995, 267:637-638.
• [68]Härlid A, Arnason U: Analyses of mitochondrial DNA nest ratite birds within the Neognathae: supporting a neotenous origin of ratite morphological characters. Proc R Soc Lond B 1999, 266:305-309.
• [69]Johnson KP: Taxon sampling and the phylogenetic position of Passeriformes: Evidence from 916 avian cytochrome b sequences. Syst Biol 2001, 50:128-136.