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Unistellate spermatozoa of decapods: comparative evaluation and evolution of the morphology

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Abstract

Decapod unistellate spermatozoa are primarily characterized by the presence of a single appendage (spike) extending from the acrosome. Among decapods, this type of spermatozoon is found only in shrimps of the families Sicyoniidae, Penaeidae, and Solenoceridae (suborder Dendrobranchiata) and of the infraorder Caridea (suborder Pleocyemata). This review comparatively discusses the morphological diversity of unistellate spermatozoal ultrastructure among these decapods, as well as the role of the primary structures involved in the fertilization and spermatozoal capacitation. Furthermore, the use of the unistellate spermatozoal ultrastructure to support phylogenetic relationships and of the current phylogenetic evidences to investigate the evolution of spermatozoa of decapods is discussed. Morphologically, the main differences between caridean and dendrobranchiate unistellate spermatozoa are the shape of the main body (inverted cup-shaped, and spherical, bulged or elongate, respectively) and complexity of the acrosomal region. The latter is directly related to the type of fertilization. For example, dendrobranchiates have more complex acrosomal regions than that carideans, and fertilization involves a visible acrosome reaction, which is not observed in carideans. Ultrastructural changes of spermatozoa throughout capacitation are unknown in carideans, but for dendrobranchiates generally occur in the acrosomal vesicle and subacrosomal region throughout attachment of the spermatophore to the thelycum, enabling fertilization by the spermatozoa. Comparative evaluation of spermatozoal morphology and current phylogenetic evidences corroborates the hypothesis that the spermatozoal spike of carideans and dendrobranchiates is the result of convergent evolution.

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References

  • Abele LG, Felgenhauer BE (1986) Phylogenetic and phonetic relationships among the lower Decapoda. J Crust Biol 6(3):385–400

    Article  Google Scholar 

  • Ahyong ST, O’Meally D (2004) Phylogeny of the decapoda reptantia: resolution using three molecular loci and morphology. Raffles B Zool 52(2):673–693

    Google Scholar 

  • Alfaro J, Lawrence AL, Lewis D (1993) Interaction of bacteria and male reproductive system blackening disease of captive Penaeus setiferus. Aquaculture 117:1–8

    Article  Google Scholar 

  • Alfaro J, Muñoz N, Vargas M, Komen J (2003) Induction of sperm activation in open and closed thelycum penaeoid shrimps. Aquaculture 216:371–381

    Article  Google Scholar 

  • Alfaro J, Ulate K, Vargas M (2007) Sperm maturation and capacitation in the open thelycum shrimp Litopenaeus (Crustacea: Decapoda: Penaeoidea). Aquaculture 270:436–442

    Article  Google Scholar 

  • Arsenault AL (1984) Changes in the nuclear envelope associated with spermatid differentiation in the shrimp, Crangon semtemspinosa. J Ultrastruct Res 86:294–308

    Article  Google Scholar 

  • Arsenault AL, Clattenburg RE, Odense PH (1979) Spermiogenesis in the shrimp, Crangon septemspinosa, Say. Can J Zool 57:486–498

    Article  Google Scholar 

  • Arsenault AL, Clattenburg RE, Odense PH (1980) Further observations on spermiogenesis in the shrimp, Crangon septemspinosa. A mechanism for cytoplasmic reduction. Can J Zool 58:497–506

    Article  Google Scholar 

  • Aungsuchawan S, Browdy CL, Withyachumnarnkul B (2011) Sperm capacitation of the shrimp Litopenaeus vannamei. Aquac Res 42:188–195

    Article  Google Scholar 

  • Baldwin JD, Griffin FJ, Clark WH (1998) Immunological characterization of the acrosomal filament in the marine shrimp Sicyonia ingentis. Zygote 6:329–339

    Article  PubMed  CAS  Google Scholar 

  • Barros C, Dupré E, Viveiros L (1986) Sperm-egg interactions in the shrimp Rhynchocinetes typus. Gamete Res 14:171–180

    Article  Google Scholar 

  • Bauer RT (1986) Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans. J Crust Biol 6(3):313–325

    Article  Google Scholar 

  • Bauer RT, Holt GJ (1998) Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea. Mar Biol 132:223–235

    Article  Google Scholar 

  • Bauer RT, Min LJ (1993) Spermatophores and plug substance of the marine shrimp Trachypenaeus similis (Crustacea: Decapoda: Penaeidae): formation in the male reproductive tract and disposition in the inseminated female. Biol Bull 185:174–185

    Article  Google Scholar 

  • Bauer RT, Thiel M (2011) First description of a pure-search mating system and protandry in the shrimp Rhynchocinetes uritai (Decapoda: Caridea). J Crust Biol 31(2):286–295

    Article  Google Scholar 

  • Bracken HD, De Grave S, Felder DL (2009a) Phylogeny of the infraorder Caridea based on mitochondrial and nuclear genes (Crustacea: Decapoda). In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean Issues 18. Taylor and Francis/CRC Press, Boca Raton, pp 282–305

    Google Scholar 

  • Bracken HD, Toon A, Felder DL, Martin JW, Finley M, Rasmussen J, Palero F, Crandall KA (2009b) The decapod tree of life: compiling the data and moving toward a consensus of decapod evolution. Arthropod Syst Phylogeny 67(1):99–116

    Google Scholar 

  • Bracken HD, De Grave S, Toon A, Felder DL, Crandall KA (2010) Phylogenetic position, systematic status, and divergence time of the Procarididea (Crustacea: Decapoda). Zool Scr 39(2):198–212

    Article  Google Scholar 

  • Braga AL, Nakayama CL, Suita de Castro LA, Wasielesky W (2013) Spermatozoa ultrastructure of the pink shrimp Farfantepenaeus paulensis (Decapoda: Dendrobranchiata). Acta Zool 94:119–214

    Article  Google Scholar 

  • Bray WA, Lawrence AL (1992) Reproduction of Penaeus species in captivity. In: Fast A, Lester LJ (eds) Marine shrimp culture: principles and practices. Elsevier Science Publishers BV, Amsterdam, pp 93–169

    Google Scholar 

  • Burkenroad MD (1981) The higher taxonomy and evolution of Decapoda (Crustacea). Trans San Diego Soc Nat Hist 19:251–268

    Google Scholar 

  • Butcher AR, Fielder DR (1994) The reproductive anatomy of male freshwater prawns Macrobrachium australiense (Holthuis, 1890) in southeast Queensland. Invertebr Reprod Dev 26(3):205–212

    Article  Google Scholar 

  • Chan T-Y, Tong J, Tam YK, Chu KH (2008) Phylogenetic relationships among genera of the Penaeidae (Crustacea: Decapoda) revealed by mitochondrial 16S rRNA gene sequences. Zootaxa 1694:38–50

    Google Scholar 

  • Chen TI, Green JD, Clark WH (1994) Sperm penetration of the vitelline envelope of Sicyonia ingentis eggs is mediated by a trypsin-like lysin of acrosomal vesicle origin. Dev Growth Differ 36(3):259–273

    Article  CAS  Google Scholar 

  • Chow S, Sandifer P (2001) Sperm-egg interaction in the palaemonid shrimp Palaemonetes vulgaris. Fisheries Sci 67:370–372

    Article  CAS  Google Scholar 

  • Chow S, Ogasawara Y, Taki Y (1982) Male reproductive system and fertilization of the palaemonid shrimp Macrobrachium rosenbergii. B Jpn Soc Sci Fish 48(2):177–183

    Article  Google Scholar 

  • Christoffersen ML (1988) Phylogenetic systematics of the Eucarida (Crustacea: Malacostraca). Revta Bras Zool 5(2):325–351

    Article  Google Scholar 

  • Chu KH, Tsang LM, Ma KY, Chan T-Y, Ng PKL (2009) Decapod phylogeny: what can protein-coding genes tell us? In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean issues 18. Taylor and Francis/CRC Press, Boca Raton, pp 90–99

  • Clark WH, Griffin FJ (1988) The morphology and physiology of the acrosome reaction in the sperm of the decapod, Sicyonia ingentis. Dev Growth Differ 30(5):451–462

    Article  Google Scholar 

  • Clark WH, Kleve MC, Yudin AI (1981) An acrosome reaction in natantian sperm. J Exp Zool 218:279–291

    Article  CAS  Google Scholar 

  • Cobos V, Díaz V, Raso JEG, Manjón-Cabeza ME (2011) The male reproductive system of Hippolyte inermis Leach 1815 (Decapoda, Caridea). Helgol Mar Res 65:17–24

    Article  Google Scholar 

  • Correa C, Baeza JA, Dupré E, Hinojosa IA, Thiel M (2000) Mating behavior and fertilization success of three ontogenetic stages of male rock shrimp Rhynchocinetes typus (Decapoda: Caridea). J Crust Biol 20(4):628–640

    Article  Google Scholar 

  • Cross NL (1998) Role of cholesterol in sperm capacitation. Biol Reprod 59:7–11

    Article  PubMed  CAS  Google Scholar 

  • Cuartas EI, Sousa LG (2007) Ultrastructural study of the spermatophores and spermatozoa in Uca uruguayensis (Decapoda, Brachyura, Ocypodidae). Biociências 15:21–28

    Google Scholar 

  • Dall W, Hill BJ, Rothlisberg OC, Staples DJ (1990) The biology of the Penaeidae. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology. Academic Press, London, pp 1–384

    Google Scholar 

  • Davis BK (1981) Timing of fertilization in mammals: sperm cholesterol/phospholipid ratio as a determinant of the capacitation interval. Proc Natl Acad Sci 78(12):7560–7564

    Article  PubMed  CAS  Google Scholar 

  • De Grave S, Pentcheff ND, Ahyong ST, Chan T-Y, Crandall KA, Dworschak PC, Felder DL, Feldmann RM, Fransen CHJM, Goulding LYD, Lemitre R, Low MEY, Martin JW, Ng PKL, Schweitzer CE, Tan SH, Tshudy D, Wetzer R (2009) A classification of living and fossil genera of decapod crustaceans. Raffles B Zool 21:1–109

    Google Scholar 

  • Demestre M, Fortuño JM (1992) Reproduction of the deep-water shrimp Aristeus antennatus (Decapoda: Dendrobranchiata). Mar Ecol Prog Ser 88:41–51

    Article  Google Scholar 

  • Dixon CJ, Ahyong ST, Schram FR (2003) A new hypothesis of decapod phylogeny. Crustaceana 76(8):935–975

    Article  Google Scholar 

  • Dougherty WJ (1987) Oriented spermatozoa in the spermatophore of the palaemonid shrimp. Macrobrachium rosenbergii. Tissue Cell 19(1):145–152

    Article  PubMed  CAS  Google Scholar 

  • Dupré E, Barros C (1983) Fine structure of the mature spermatozoon of Rhynchocinetes typus, Crustacea Decapoda. Gamete Res 7:1–18

    Article  Google Scholar 

  • Dupré EM, Barros C (2011) In vitro fertilization of the rock shrimp, Rhynchocinetes typus (Decapoda, Caridea): a review. Biol Res 44:125–133

    Article  PubMed  Google Scholar 

  • Dupré E, Schaaf G (1996) Influence of ions on the unfolding of the spermatozoa of the rock shrimp, Rhynchocinetes typus. J Exp Zool 274:358–364

    Article  Google Scholar 

  • Felgenhauer BE (1992) Internal anatomy of the Decapoda: an overview. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates. Decapod Crustacea, vol 10. Wiley-Liss, New York, pp 45–75

  • Felgenhauer BE, Abele LG (1991) Morphological diversity of decapod spermatozoa. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 322–341

    Google Scholar 

  • Felgenhauer BE, Abele LG, Kim W (1988) Reproductive morphology of the anchialine shrimp Procaris ascensionis (Decapoda: Procarididae). J Crust Biol 8(3):333–339

    Article  Google Scholar 

  • Fransen CHJM, De Grave S (2009) Evolution and radiation of shrimp-like decapods: an overview. In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean issues 18. Taylor and Francis/CRC Press, Boca Raton, pp 245–259

    Chapter  Google Scholar 

  • Garda AA, Colli GR, Aguiar-Júnior O, Recco-Pimentel SM, Báo SN (2002) The ultrastrucutre of the spermatozoa of Epipedobates flavopictus (Amphibia, Anura, Dendrobatidae), with comments on its evolutionary significance. Tissue Cell 34(5):356–364

    Article  PubMed  Google Scholar 

  • Griffin FJ, Clark WH, Crowe JH, Crowe LM (1987) Intracelular pH decreases during the in vitro induction of the acrosome reaction in the sperm of Sicyonia ingestis. Biol Bull 173:311–323

    Article  Google Scholar 

  • Griffin FJ, Shigekawa K, Clark WH (1988) Formation and structure of the acrosomal filament in the sperm of Sicyonia ingentis. J Exp Zool 246:94–102

    Article  Google Scholar 

  • Guinot D, Jamieson BGM, Richer de Forges B (1994) Relationship of Homolidae and Dromiidae: evidence from spermatozoa ultrastructure (Crustacea, Decapoda). Acta Zool 75(3):255–267

    Article  Google Scholar 

  • Gwo JC (2000) Cryopreservation of aquatic invertebrate semen: a review. Aquac Res 31:259–271

    Article  Google Scholar 

  • Hendelberg J (1986) The phylogenetic significance of sperm morphology in the Platyhelminthes. Hydrobiology 132:53–58

    Article  Google Scholar 

  • Jamieson BGM (1984) A phonetic and cladistics study of spermatozoal ultrastructure in the Oligochaeta (Annelida). Hydrobiologia 115:3–13

    Article  Google Scholar 

  • Jamieson BGM (1991) Ultrastructure and phylogeny of crustacean spermatozoa. Mem Queensl Mus 31:109–142

    Google Scholar 

  • Jamieson BGM (1994) Phylogeny of the Brachyura with particular reference to the Podotremata: evidence from a review of spermatozoal ultrastructure (Crustacea, Decapoda). Phil Trans R Soc Lond B 345:373–393

    Article  Google Scholar 

  • Jamieson BGM, Healy JM (1992) The phylogenetic position of the Tuatara, Sphenodon (Sphenodintida, Amniota), as indicates by cladistics analysis of the ultrastructure of spermatozoa. Phil Trans R Soc Lond B 335:207–219

    Article  Google Scholar 

  • Jamieson BGM, Tudge CC (1990) Dorippids are Heterotremata: evidence from ultrastructure of the spermatozoa of Neodorippe astute (Dorippidae) and Portunus pelagicus (Portunidae) Brachyura: Decapoda. Mar Biol 106:347–354

    Article  Google Scholar 

  • Jamieson BGM, Tudge CC (2000) Crustacea-Decapoda. In: Adiyodi KG, Adiyodi RG, Jamieson BGM (eds) Reproductive biology of invertebrates. Progress in male gamete ultrastructure and phylogeny, vol 9C. Wiley, Chichester, pp 1–95

    Google Scholar 

  • Jamieson BGM, Guinot D, Richer de Forges B (1995) Phylogeny of the Brachyura (Crustacea, Decapoda): evidence from spermatozoal ultrastructure. In: Jamieson BGM, Ausio J, Justine J-L (eds) Advances in spermatozoa phylogeny and taxonomy. Mémoires du Muséum National d’Histoire Naturalle, Paris, pp 265–283

    Google Scholar 

  • Jarman SN, Nicol S, Elliott NG, McMinn A (2000) 28S rDNA evolution in the Eumalacostraca and the phylogenetic position of krill. Mol Phylogenet Evol 17(1):26–36

    Article  PubMed  CAS  Google Scholar 

  • Kang X, Ge Shaoqin, Guo M, Liu G, Mu S (2008) A transmission electron microscopy investigation: the membrane complex in spermatogenesis of Fenneropenaeus chinensis. Cytotechnology 56:113–121

    Article  PubMed  Google Scholar 

  • Kim DH, Jo Q, Choi JH, Yun SJ, Oh TY, Kim BK, Han C (2003) Sperm structure of the pandalid shrimp Pandalopsis japonica (Decapoda, Pandalidae). J Crust Biol 23(1):23–32

    Article  CAS  Google Scholar 

  • Klann AE, Bird T, Peretti AV, Gromov AV, Alberti G (2009) Ultrastructure of spermatozoa of solifuges (Arachnida, Solifugae): possible characters for their phylogeny? Tissue Cell 41:91–103

    Article  PubMed  CAS  Google Scholar 

  • Klaus S, Brandis D (2011) Evolution of sperm morphology in potamid freshwater crabs (Crustacea: Brachyura: Potamoidea). Zool J Linn Soc 161:53–63

    Article  Google Scholar 

  • Klaus S, Schubart CD, Brandis D (2009) Ultrastructure of spermatozoa and spermatophores of old world freshwater crabs (Brachyura: Potamoidea: Gecarcinucidae, Potamidae, and Potamonautidae). J Morphol 270:175–193

    Article  PubMed  Google Scholar 

  • Kleve MG, Clark WH (1980) Association of actin with sperm centrioles: isolation of centriolar complexes and immunofluorescent localization of actin. J Cell Biol 86:87–95

    Article  PubMed  CAS  Google Scholar 

  • Kleve MG, Yudin AL, Clark WH (1980) Fine structure of the unistellate sperm of the shrimp, Sicyonia ingentis (Natantia). Tissue Cell 12:29–45

    Article  PubMed  CAS  Google Scholar 

  • Koehler LD (1979) A unique case of cytodifferentiation: spermiogenesis of the prawn, Palaemonetes paludosus. J Ultrastruct Res 69:109–120

    Article  PubMed  CAS  Google Scholar 

  • Kruevaisayawan H, Vanichviriyakit R, Weerachatyanukul W, Iamsaard S, Withyachumnarnkul B, Basak A, Tanphaichitr N, Sobhon P (2008) Induction of the acrosome reaction in black tiger shrimp (Penaeus monodon) requires sperm trypsin-like enzyme activity. Biol Reprod 79:134–141

    Article  PubMed  CAS  Google Scholar 

  • Leung-Trujillo JR, Lawrence AL (1987) Spermatophore generation times in Penaeus setiferus, P. vannamei, and P. stylirostris. J World Aquacult 22(4): 244–251

  • Levine AE, Walsh KA (1980) Purification of an acrosin-like enzyme from sea urchin sperm. J Biol Chem 255(10):4814–4820

    PubMed  CAS  Google Scholar 

  • Li CP, De Grave S, Chan T-Y, Lei HC, Chu KH (2011) Molecular systematics of caridean shrimps based on five nuclear genes: implications for superfamily classification. Zool Anz 250:270–279

    Article  Google Scholar 

  • Lindsay LL, Clark WH (1992) Preloading of micromolar intracellular Ca+2 during capacitation of Sicyonia ingentis sperm, and the role of the pHi decrease during the acrosome reaction. J Exp Zool 262(2):219–229

    Article  PubMed  CAS  Google Scholar 

  • Lino-Neto J, Dolder H (2001) Ultrastructural characteristics of the spermatozoa of Scelionidae (Hymenoptera, Platygastroidea) with phylogenetic considerations. Zool Scr 30:89–96

    Article  Google Scholar 

  • Lynn JW, Clark WH (1983a) A morphological examination of sperm-egg interaction in the freshwater prawn, Macrobrachium rosenbergii. Biol Bull 164:446–458

    Article  Google Scholar 

  • Lynn JW, Clark WH (1983b) The fine structure of the mature sperm of the freshwater prawn, Macrobrachium rosenbergii. Biol Bull 164:459–470

    Article  Google Scholar 

  • Ma KY, Chan TY, Chu KH (2009) Phylogeny of penaeoid shrimps (Decapoda: Penaeoidea) inferred from nuclear protein-coding genes. Mol Phylogenet Evol 53:45–55

    Article  PubMed  CAS  Google Scholar 

  • Manjón-Cabeza ME, Cobos V, Raso JEG (2011) The reproductive system of Hippolyte niezabitowskii. Zoology 114:140–149

    Article  PubMed  Google Scholar 

  • Martin JW, Davis GE (2001) An updated classification of the Recent Crustacea. Natur Hist Mus Los Angeles County 39:1–124

    Google Scholar 

  • Medina A (1994) Spermiogenesis and sperm structure in the shrimp Parapenaeus longirostris (Crustacea: Dendrobranchiata): comparative aspects among decapods. Mar Biol 119:449–460

    Article  Google Scholar 

  • Medina A (1995a) Spermatozoal ultrastructure in Dendrobranchiata (Crustacea, Decapoda): taxonomic and phylogeny considerations. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoa phylogeny and taxonomy. Mémoires du Muséum National d’Histoire Naturalle, Paris, pp 231–242

    Google Scholar 

  • Medina A (1995b) The atypical sperm morphologies of Aristeus antennatus and Aristaeomorpha foliacea (Crustacea, Dendrobranchiata, Aristeidae) and their phylogenetic significance. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoa phylogeny and taxonomy. Mémoires du Muséum National d’Histoire Naturalle, Paris, pp 243–250

    Google Scholar 

  • Medina A, Rodriguez A (1992) Spermiogenesis and sperm structure in the crab Uca tangeri (Crustacea, Brachyura) with special reference to the acrosome differentiation. Zoomorphology 111:161–165

    Article  Google Scholar 

  • Medina A, López de la Rosa I, Santos A (1994a) Ultrastructural comparison of the spermatozoa of Sicyonia carinata (Sicyoniidae) and Penaeopsis serrata (Penaeidae) shrimp (Crustacea, Dendrobranchiata), with particular emphasis on the acrosomal structure. J Submicrosc Cytol Pathol 26(3):395–403

    Google Scholar 

  • Medina A, Mourente G, López de la Rosa I, Santos A, Rodríguez A (1994b) Spermatozoal ultrastructure of Penaeus kerathurus and Penaeus japonicus (Crustacea, Dendrobranchiata). Zoomorphology 114:161–167

    Article  Google Scholar 

  • Medina A, Megina C, Abascal FJ, Calzada A (2003) The sperm ultrastructure of Merluccius merluccius (Teleostei, Gadiformes): phylogenetic considerations. Acta Zool 84:131–137

    Article  Google Scholar 

  • Medina A, García-Isarch E, Sobrino I, Abascal FJ (2006a) Ultrastructure of the spermatozoa of Aristeopsis edwardsiana and Aristeus varidens (Crustacea, Dendrobranchiata, Aristeidae). Zoomorphology 125:39–46

    Article  Google Scholar 

  • Medina A, Scelzo MA, Tudge CC (2006b) Spermatozoal ultrastructure in three Atlantic solenocerid shrimps (Decapoda, Dendrobranchiata). J Morphol 267:300–307

    Article  PubMed  Google Scholar 

  • Mohamed KS, Diwan AD (1993) Spermatogenesis and spermatophore formation in the indian white prawn Penaeus indicus H. Milne Edwards. J Mar Biol Ass India 35:180–192

    Google Scholar 

  • Musco L, Giangrande A, Gherardi M, Lepore E, Mercurio M, Sciscioli M (2008) Sperm ultra-structure of Odontosyllis ctenostoma (Polychaeta:Syllidae) with inferences on syllid phylogeny and reproductive biology. Sci Mar 72(2): 421–427

    Google Scholar 

  • Nunes ET, Braga AA, Santos DC, Camargo-Mathias MI (2010) Cytodifferentiation during the spermatogenesis of the hermaphrodite Caridea Exhippolysmata oplophoroides. Micron 41:585–591

    Article  PubMed  Google Scholar 

  • Papathanassiou E, King PE (1984) Ultrastructural studies on gametogenesis of the prawn Palaemon serratus (Pennant). II. Spermiogenesis. Acta Zool 65:33–40

    Article  Google Scholar 

  • Pereira G (1997) A cladistics analysis of the freshwater shrimps of the family Palaemonidae (Crustacea, Decapoda, Caridea). Acta Biol Venez 17:1–69

    Google Scholar 

  • Perez C, Roco M, Castro A, Dupré E, Schatten G, Barros C (1991) Localization of microfilaments and a tubulin-like protein in crustacean (Rhynchocinetes typus) spermatozoon. Mol Reprod Dev 28:373–379

    Article  PubMed  CAS  Google Scholar 

  • Pochon-Masson J (1969) Infrastructure du spermatozoide de Palaemon elegans (De Man) (Crustacé, Decápode). Arch Zool Exp Gen 110:363–372

    Google Scholar 

  • Poljaroen J, Vanichviriyakit R, Tinikul Y, Phoungpetchara I, Linthong V, Weerachatyanukul W, Sobhon P (2010) Spermatogenesis and distinctive mature sperm in the giant freshwater prawn, Macrobrachuim rosenbergii (De Man, 1879). Zool Anz 249:81–94

    Article  Google Scholar 

  • Pongtippatee P, Vanichviriyakit R, Chavadej J, Plodpai P, Pratoomchart B, Sobhon P, Withyachumnarnkul B (2007) Acrosome reaction in the sperm of the black tiger shrimp Penaeus monodon (Decapoda, Penaeidae). Aquac Res 38:1635–1644

    Article  Google Scholar 

  • Porter ML, Pérez-Losada M, Crandall KA (2005) Model-based multi-locus estimation of decapod phylogeny and divergence times. Mol Phylogenet Evol 37:355–369

    Article  PubMed  CAS  Google Scholar 

  • Quan J, Zhuang Z, Deng J, Dai J, Zhang Y (2004) Phylogenetic relationships of 12 Penaeoidea shrimp species deduced from mitochondrial DNA sequences. Biochem Genet 42:331–345

    Article  PubMed  CAS  Google Scholar 

  • Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–136

    Article  Google Scholar 

  • Rios M, Barros C (1997) Trypsin-like enzymes during fertilization in the shrimp Rhynchocinetes typus. Mol Reprod Dev 46:581–586

    Article  PubMed  CAS  Google Scholar 

  • Sawada H, Pinto MR, Santis R (1998) Participation of sperm proteasome in fertilization of the phlebobranch ascidian Ciona intestinalis. Mol Reprod Dev 50:493–498

    Article  PubMed  CAS  Google Scholar 

  • Scelzo MA, Medina A (2003) Spermatozoal ultrastructure in Artemesia longinaris (Decapoda, Penaeidae). J Crust Biol 23(4):814–818

    Article  Google Scholar 

  • Scelzo MA, Medina A (2004) A dendrobranchiate, Peisos petrunkevitchi (Decapoda, Sergestidae), with reptant-like sperm: a spermiocladistic assessment. Acta Zool 85:81–89

    Article  Google Scholar 

  • Scholtz G, Richter S (1995) Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca). Zool J Linn Soc 113(3):289–328

    Google Scholar 

  • Schram FR (2001) Phylogeny of decapods: moving towards a consensus. Hydrobiologia 449:1–20

    Article  Google Scholar 

  • Selmi MG, Brizzi R, Bigliardi E (1997) Sperm morphology of salamandrids (Amphibia, Urodela): implications for phylogeny and fertilization biology. Tissue Cell 29(6):651–664

    Article  PubMed  CAS  Google Scholar 

  • Shen H, Braband A, Scholtz G (2013) Mitogenomic analysis of decapod crustacean phylogeny corroborates traditional views on their relationships. Mol Phylogenet Evol 66:776–789

    Google Scholar 

  • Shigekawa K, Clark WK (1986) Spermiogenesis in the Marine Shrimp, Sicyonia ingentis. Dev Growth Differ 28(2):95–112

    Article  Google Scholar 

  • Tavares C, Serejo C, Martin JW (2009) A preliminar phylogenetic analysis of the Dendrobranchiata based on morphological characters. In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean issues 18. Taylor and Francis/CRC Press, Boca Raton, pp 262–279

    Google Scholar 

  • Tavares-Bastos L, Colli GR, Báo SN (2008) The evolution of sperm ultrastructure among Boidae (Serpentes). Zoomorphology 127:189–202

    Article  Google Scholar 

  • Terossi M, Tudge CC, Greco LS, Mantelatto FL (2012) A novel spermatozoan ultrastructure in the shrimp Hippolyte obliquimanus Dana, 1852 (Decapoda: Caridea: Hippolytidae). Invertebr Reprod Dev 56(4):299–304

    Article  Google Scholar 

  • Tirelli T, Silvestro D, Pessani D, Tudge CC (2010) Description of the male reproductive system of Paguristes eremita (Anomura, Diogenidae) and its placement in a phylogeny of diogenid species based on spermatozoal and spermatophore ultrastructure. Zool Anz 248:299–312

    Article  Google Scholar 

  • Toon A, Finley M, Staples J, Crandall KA (2009) Decapod phylogenetics and molecular evolution. In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean issues 18. Taylor and Francis/CRC Press, Boca Raton, pp 16–29

    Google Scholar 

  • Tsang LM, Ma KY, Ahyong ST, Chan T-Y, Chu KH (2008) Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia. Mol Phylogenet Evol 48:359–368

    Article  PubMed  CAS  Google Scholar 

  • Tudge CC (1997) Phylogeny of the Anomura (Decapoda, Crustacea): spermatozoa and spermatophore morphological evidence. Contrib Zool 67(2):125–141

    Google Scholar 

  • Tudge CC (2009) Spermatozoal morphology and its bearing on decapod phylogeny. In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean issues 18. Taylor and Francis/CRC Press, Boca Raton, pp 101–119

    Chapter  Google Scholar 

  • Vanichviriyakit R, Kruevaisayawan H, Weerachatyanukul W, Tawipreeda P, Withyachumnarnkul B, Pratoomchat B, Chavadej J, Sobhon P (2004) Molecular modification of Penaeus monodon sperm in female thelycum and its consequent responses. Mol Reprod Dev 69:356–363

    Article  PubMed  CAS  Google Scholar 

  • Vázquez-Bader AR, Carrero JC, García-Varela M, Gracia A, Laclette JP (2004) Molecular phylogeny of superfamily Penaeoidea Rafinesque-Schmaltz, 1815, based on mitochondrial 16S partial sequence analysis. J Shrellfish Res 23:911–917

    Google Scholar 

  • Vieira GHC, Cunha LD, Scheltinga DM, Glaw F, Colli GR, Báo SN (2007) Sperm ultrastructure of hoplocercid and oplurid lizards (Sauropsida, Squamata, Iguania) and the phylogeny of Iguania. J Zool Syst Evol Res 45(2):230–241

    Article  Google Scholar 

  • Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS (1995) Capacitation of mouse spermatozoa: I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121:1129–1137

    PubMed  CAS  Google Scholar 

  • Visconti PE, Ning XP, Fornés MW, Alvarez JG, Stein P, Connors SA, Kopf GS (1999) Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals and increase in protein tyrosine phosphorylation during mouse sperm capacitation. Dev Biol 214:429–443

    Article  PubMed  CAS  Google Scholar 

  • Voloch CM, Freire PR, Russo CAM (2005) Molecular phylogeny of penaeid shrimps inferred from two mitochondrial markers. Genet Mol Res 4:668–674

    PubMed  CAS  Google Scholar 

  • Wikramanayake AH, Clark WH (1994) Two extracellular matrices from oocytes of the marine shrimp Sicyonia ingentis that independently mediate only primary or secondary sperm binding. Dev Growth Differ 36:89–101

    Article  Google Scholar 

  • Wikramanayake AH, Uhlinger KR, Griffin FJ, Clark WH (1992) Sperm of the shrimp Sicyonia ingentis undergo a bi-phasic capacitation accompanied by morphological changes. Dev Growth Differ 34(3):347–355

    Article  Google Scholar 

  • Yamada Y, Aketa K (1982) Purification and characterization of the trypsin-like enzyme of the sea urchin Hemicentrotus pulcherrimus. Dev Growth Differ 24:125–134

    Article  CAS  Google Scholar 

  • Yamasaki H, Takamune K, Katagiri C (1988) Classification, inhibition and specificity studies of the vitelline coat lysine from toad sperm. Gamete Res 30:287–300

    Article  Google Scholar 

  • Yeo DCJ, Ng PKL (2003) Recognition of two subfamilies in the Potamidae Ortmann, 1896 (Brachyura, Potamidae) with a note on the genus Potamon Savigny, 1816. Crustaceana 76(10):1219–1235

    Article  Google Scholar 

  • Yokota N, Sawada H (2007) Sperm proteasomes are responsible for the acrosome reaction and sperm penetration of the vitelline envelope during fertilization of the sea urchin Pseudocentrotus depressus. Dev Biol 308:222–231

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Biological Oceanography, Oceanography Institute, Federal University of Rio Grande, C.P. 474, Rio Grande, RS, 96 201-900, Brazil

    André Braga

  2. Marine Station of Aquaculture, Oceanography Institute, Federal University of Rio Grande, C.P. 474, Rio Grande, RS, 96201-900, Brazil

    Cintia L. Nakayama, Luis Poersch & Wilson Wasielesky Jr.

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  1. André Braga
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  2. Cintia L. Nakayama
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  3. Luis Poersch
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  4. Wilson Wasielesky Jr.
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Correspondence to Wilson Wasielesky Jr..

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Communicated by A. Schmidt-Rhaesa.

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Braga, A., Nakayama, C.L., Poersch, L. et al. Unistellate spermatozoa of decapods: comparative evaluation and evolution of the morphology. Zoomorphology 132, 261–284 (2013). https://doi.org/10.1007/s00435-013-0187-2

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  • DOI: https://doi.org/10.1007/s00435-013-0187-2

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