Female genital system of the folding-trapdoor spider Antrodiaetus unicolor (Hentz, 1842) (Antrodiaetidae, Araneae): Ultrastructural study of form and function with notes on reproductive biology of spiders

Journal of Morphology

Volumn 263, Issue 3, 2005, Pages 284-309

  Michalik, Peter ^a   Reiher, Wencke ^a   Tintelnot Suhm, Marika ^b   Coyle, Frederick A ^c   Alberti, Gerd ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b Western Carolina University ^*  (Germany)

^c WESTERN CAROLINA UNIVERSITY   (United States)

Author keywords

Cryptic female choice; Gland; Mygalomorphae; Secretion; Sperm selection; Sperm storage; Spermatheca

Indexed keywords

ANIMAL; ARTICLE; FEMALE; FEMALE GENITAL SYSTEM; PHYSIOLOGY; REPRODUCTION; SCANNING ELECTRON MICROSCOPY; SPIDER; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; FEMALE; GENITALIA, FEMALE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; REPRODUCTION; SPIDERS;

ANTRODIAETIDAE; ANTRODIAETUS UNICOLOR; ARANEAE; MYGALOMORPHAE; NEMESIIDAE;

EID: 16244365230     PISSN: 03622525     EISSN: None     Source Type: Journal    
DOI: 10.1002/jmor.10309     Document Type: Article

References (79)

1. Afzelius BA, Alberti G, Dallai R, Godula J, Witalinski W. 1989. Virus- and Rickettsia-infected sperm cells in arthropods. J Invertebr Pathol 53:365-377.
2. Alberti G. 1974. Fortpflanzungsverhalten und Fortpflanzungsorgane der Schnabelmilben (Acarina: Bdellidae, Trombidiformes). Z Morphol Tiere 78:111-157.
3. Alberti G. 1995. Comparative spermatology of Chelicerata: review and perspective. In: Jamieson BGM, Ausio J, Justine J, editors. Advances in spermatozoal phylogeny and taxonomy, vol. 166. Mem Mus natn Hist nat, Paris. p 203-230.
4. Alberti G. 2000. Chelicerata. In: Jamieson BGM, editor. Progress in male gamete ultrastructure and phylogeny, vol. 8. Oxford: IBH. p 311-388.
5. Alberti G. 2002. Ultrastructural investigations of sperm and genital systems in Gamasida (Acari: Anactinotrichida) current state and perspectives for future research. Acarologia 42:107-126.
6. Alberti G, Coons LB. 1999. Acari: mites. In: Harrison FW, Foelix RF, editors. Microscopic anatomy of invertebrates, vol. 8C. New York: Wiley-Liss. p 515-1215.
7. Alberti G, Hänel H. 1986. Fine structure of the genital system in the bee parasite, Varroa jacobsoni (Gamasida: Dermanyssina) with remarks on spermiogenesis, spermatozoa, and capacitation. Exp Appl Acarol 2:63-104.
8. Alberti G, Krantz GW. Some ultrastructural observations on a species of Arctacaridae (Arctacarina; Gamasida), with remarks on their phylogenetic significance. Proc 11th Int Congr Acarol, Merida (Mexico), 2002 (in press).
9. Alberti G, Michalik P. 2004. Feinstrukturelle Aspekte der Fortpflanzungssysteme von Spinnentieren (Arachnida). Denisia 12:1-62.
10. Alberti G, Afzelius BA, Lucas SM. 1986. Ultrastructure of spermatozoa and spermatogenesis in bird spiders (Theraphosidae, Mygalomorphae, Araneae). J Submicrosc Cytol 18:739-753.
11. Alberti G, Gegner A, Witalinski W. 2000. Fine structure of the spermatophore and spermatozoa in inseminated females of Pergamasus mites (Acari: Gamasida: Pergamasidae). J Morphol 245:1-18.
12. Andrade, MCB. 1996. Sexual selection for male sacrifice in the Australian redback spider. Science 271:70-72.
13. Austad SN. 1984. Evolution of sperm priority patterns in spiders. In: Smith RL, editor. Sperm competition and the evolution of animal mating systems, vol. 7. New York: Academic Press. p 223-249.
14. Berendonck B, Greven H. 2002. Morphology of female and male genitalia of Latrodectus revivensis Shulov, 1948 (Araneae, Theridiidae) with regard to sperm priority patterns. In: Toft S, Scharff N, editors. European arachnology 2000. Aarhus: Aarhus University Press. p 157-167.
15. Berendonck B, Greven H. 2005. Genital structures in the entelegyne widow spider Latrodectus revivensis (Arachnida; Araneae; Theridiidae) indicate a low ability for cryptic female choice by sperm manipulation. J Morphol 263:118-132.
16. Bertani R, Silva Junior PI. 2002. The first mygalomorph spider without spermathecae: Sickius longibulbi, with a revalidation of Sickius (Araneae, Theraphosidae, Ischnocolinae). J Arachnol 30:519-526.
17. Bitsch J, Bitsch C. 1991. Glandes épidermiques des aptérygotes. Ultrastructure et modifications lors de la mue. Ann Soc Ent Fr 27:129-142.
18. Briceño, RD. 1987. How spiders determine clutch size. Rev Biol Trop 35:25-29.
19. Brown SG. 1985. Mating behavior of the golden orb-weaving spider, Nephila clavipes. II. Sperm capacitation, sperm competition, and fecundity. J Comp Psychol 99:167-175.
20. Burger M, Nentwig W, Kropf C. 2003. Complex genital structures indicate cryptic female choice in a haplogyne spider (Arachnida, Araneae, Oonopidae, Gamasomorphinae). J Morphol 255:80-93.
21. Cooke JA. 1966. Synopsis of the structure and function of the genitalia in Dysdera crocata. Senckenberg Biol 47:35-43.
22. Coons LB, Alberti G. 1999. Acari: ticks. In: Harrison FW, Foelix RF, editors. Microscopic anatomy of invertebrates, vol. 8C. New York: Wiley-Liss. p 267-514.
23. Coyle FA. 1968. The mygalomorph spider genus Atypoides (Araneae, Antrodiaetidae). Psyche 75:157-194.
24. Coyle FA. 1971. Systematics and natural history of the mygalomorph spider genus Antrodiaetus and related genera (Araneae, Antrodiaetidae). Bull Mus Comp Zool 141:269-402.
25. Coyle FA, Harrison FW, McGimsey WC, Palmer JM. 1983. Observation on the structure and function of spermathecae in haplogyne spiders. Trans Am Microsc Soc 102:272-280.
26. De Carlo JM. 1973. Anatomia microscopia de las espermatecas de los generos Grammostola y Acanthoscurria. Physis 32:343-350.
27. Di Palma A, Alberti G. 2001. Fine structure of the female genital system in phytoseiid mites with remarks on egg nutrimentary development, sperm-access system, sperm transfer, and capacitation (Acari, Gamasida, Phytoseiidae). Exp Appl Acarol 25:525-591.
28. Eberhard WG. 1996. Female control: sexual selection by cryptic female choice. Monographs in behavior and ecology. Princeton, NJ: Princeton University Press.
29. Eberhard WG. 2004. Why study spider sex: special traits of spiders facilitate studies of sperm competition and cryptic female choice. J Arachnol 32:545-556.
30. Eberhard WG, Huber BA. 1998. Courtship, copulation, and sperm transfer in Leucauge mariana (Araneae, Tetragnathidae) with implications for the higher classification. J Arachnol 26:342-368.
31. Elgar MA, Schneider JM, Herberstein ME. 2000. Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc R Soc Lond B 267:2439-2443.
32. Elgar MA, Champion de Crespigny FE, Ramamurthy S. 2003. Male copulation behaviour and the risk of sperm competition. Anim Behav 66:211-216.
33. Fahrenbach WH. 1999. Merostomata. In: Harrison FW, Foelix RF, editors. Microscopic anatomy of invertebrates, vol. 8A. New York: Wiley-Liss. p 21-115.
34. Farley RD. 1999. Scorpiones. In: Harrison FW, Foelix RF, editors. Microscopic anatomy of invertebrates, vol. 8A. New York: Wiley-Liss. p 117-222.
35. Fritz AH, Turner FR. 2002. A light and electron microscopical study of the spermathecae and ventral receptacle of Anastrepha suspensa (Diptera: Tephritidae) and implications in female influence of sperm storage. Arthropod Struct Dev 30:293-313.
36. Gerhardt U. 1923. Weitere sexualbiologische Untersuchung an Spinnen. Arch Naturgesch A10:1-225.
37. Happ GM, Happ CM. 1977. Cytodifferentiation in the accessory glands of Tenebrio molitor. III. Fine structure of the spermathecal accessory gland in the pupa. Tissue Cell 9:711-732.
38. Haupt J. 2003. The Mesothelae - a monograph of an exceptional group of spiders (Araneae: Mesothelae). Zoologica 154:1-102.
39. Hellriegel B, Ward PI. 1998. Complex female reproductive tract morphology: Its possible use in postcopulatory female choice. J Theor Biol 190:179-186.
40. Huber BA. 1993. Genital mechanics and sexual selection in the spider Nesticus cellulanus (Araneae: Nesticidae). Can J Zool 71:2437-2447.
41. Huber BA. 1997. On American Micromerys and Metagonia (Araneae, Pholcidae), with notes on behavior and natural history. Zool Scr 25:341-363.
42. Huber BA. 2002. Functional morphology of the genitalia in the spider Spermophora senoculata (Pholcidae, Araneae). Zool Anz 241:105-116.
43. Huber BA. 2004. Evidence for functional segregation in the directionally asymmetric male genitalia of the spider Metagonia mariguitarensis (Gonzáles-Sponga) (Pholcidae: Araneae). J Zool Lond 262:317-326.
44. Jacquemin G, Bareth C. 1981. Ultrastructure des soies glandulaires et sensorielles du premier sternite abdominal des males de Campodea chardardi Condé (Insecta: Diplura): modifications liées à la mue. Int J Insect Morphol Embryol 10:463-481.
45. Knoflach B, van Harten A. 2002. The genus Latrodectus from mainland Yemen, the Socotra archipelago and adjacent countries (Araneae, Theridiidae). Fauna Arabia 19:321-361.
46. Kovoor J. 1981. Une source probable de phéromones sexuelles: les glandes tégumentaires de la région génitale des femelles d'Araignées. Atti Soc Tosc Sci Nat Mem ser B 88:1-15.
47. Lopez A. 1987. Glandular aspects of sexual biology. In: Nentwig W, editor. Ecophysiology of spiders. Berlin: Springer. p 121-132.
48. Lopez A, Juberthie-Jupeau L. 1983. Structure et ultrastructure de la spermathéque chez Telema tenella Simon (Araneae, Telemidae). Mem Biospeol 10:413-418.
49. Marchini D, Bernini LF, Marri L, Giordano PC, Dallai R. 1991. The female reproductive accessory glands of the medfly Ceratitis capitata: antibacterial activity of the secretion fluid. Insect Biochem 21:597-605.
50. Margaritis LH, Mazzini M. 1998. Structure of the egg. In: Harrison FW, Locke M, editors. Microscopic anatomy of invertebrates, vol. 11C. New York: Wiley-Liss. p 995-1037.
51. Michalik P, Haupt J, Alberti G. 2004a. On the occurrence of coenospermia in mesothelid spiders (Araneae, Heptathelidae). Arthropod Struct Dev 33:173-181.
52. Michalik P, Dallai R, Giusti F, Alberti G. 2004b. The ultrastructure of the peculiar synspermia of some Dysderidae (Araneae, Arachnida). Tissue Cell 36:447-460.
53. Michalik P, Sacher P, Alberti G. 2004c. Ultrastructural observations of spermatozoa of several tetragnathid spiders and their phylogenetic implications (Araneae, Tetragnathidae). J Morphol Published in Wiley InterScience (www.interscience.wiley-.com) DOI: 10.1002/jmor.10226.
54. Morishita R, Ferreira SA, Filha AS, Faraco CD. 2003. Studies on oogenesis and oviposition in the brown spider Loxosceles intermedia (Araneae: Sicariidae). Anat Rec 273A:575-582.
55. Noirot C, Quennedey A. 1974. Fine structure of insect epidermal glands. A Rev Ent 19:61-80.
56. Noirot C, Quennedey A. 1991. Glands, gland cells, glandular units: some comments on terminology and classification. Ann Soc Entomol Fr 27:123-128.
57. Ōsaki H. 1969. Electron microscope study on the spermatozoon of the liphistiid spider Heptathela kimurai. Acta Arachnol Tokyo 22:1-12.
58. Parker JR. 1999. The sites of fertilisation and ovulation in entelegyne spiders. Newsl Br Arachnol Soc 84:6-7.
59. Quennedey A. 1991. The moulting process of perennial class 3 gland cells during the postembryonic development of two heterometabolous insects: Blaberus (Dictyoptera) and Dysdercus (Heteroptera). Ann Soc Ent Fr 27:143-161.
60. Quennedey A. 1998. Insect epidermal gland cells: ultrastructure and morphogenesis. In: Harrison FW, Locke M, editors. Microscopic anatomy of invertebrates, vol. 11A. New York: Wiley-Liss. p 177-207.
61. Reynolds ES. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208.
62. Richardson KC, Jarett L, Finke EH. 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313-325.
63. Schäfer MA, Uhl G. 2002. Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour. Behav Ecol Sociobiol 51:368-377.
64. Schneider JM, Elgar MA. 2001. Sexual cannibalism and sperm competition in the golden orb-spider Nephila plumipes (Araneoida): female and male perspective. Behav Ecol 12:547-552.
65. Schneider JM, Herberstein ME, De Crespigny FC, Ramamurthy S, Elgar MA. 2000. Sperm competition and small size advantage for males of the golden orb-web spider Nephila edulis. J Evol Biol 13:939-946.
66. Suhm M, Alberti G. 1993. The fine structure of the spermatheca of Amaurobius fenestralis (Stroem, 1768) (Amaurobiidae, Araneae). Boll Acc Gioenia Sci Nat 26:343-353.
67. Suhm M, Alberti G. 1996. The fine structure of the spermatheca of Pardosa lugubris (Walckenaer, 1802). Rev Suisse Zool hors serie:635-642.
68. Suzuki H. 1995. Fertilization occurs internally in the spider Achaearanea tepidariorum (C. Koch). Invertebr Reprod Dev 28:211-214.
69. Uhl G. 1994a. Genital morphology and sperm storage in Pholcus phalangioides (Fuesslin, 1775) (Pholcidae; Araneae). Acta Zool Stockh 75:1-12.
70. Uhl G. 1994b. Ultrastructure of the accessory glands in female genitalia of Pholcus phalangioides (Fuesslin, 1771) (Pholcidae; Araneae). Acta Zool Stockh 75:13-25.
71. Uhl G. 1996. Sperm storage secretion of female cellar spiders (Pholcus phalangioides: Araneae): a gel-electrophoretic analysis. J Zool 240:153-161.
72. Uhl G. 1998. Mating behavior in the cellar spider, Pholcus phalangioides, indicates sperm mixing. Anim Behav 56:1155-1159.
73. Uhl G. 2000. Two distinctly different sperm storage organs in female Dysdera erythrina (Araneae: Dysderidae). Arthropod Struct Dev 29:163-169.
74. Uhl G. 2002. Female genital morphology and sperm priority patterns in spiders (Araneae). In: Toft S, Scharff N, editors. European arachnology 2000. Aarhus: Aarhus University Press. p 145-156.
75. Uhl G, Gunnarsson B. 2001. Female genitalia in Pityohyphantes phrygianus, a spider with a skewed sex ratio. J Zool 255:367-376.
76. Uhl G, Vollrath F. 1998. Genital morphology of Nephila edulis: Implications for sperm competition in spiders. Can J Zool 76:39-47.
77. Watson PJ. 1993. Foraging advantage of polyandry for male sierra dome spiders (Linyphia litigiosa: Linyphiidae) and assessment of alternative direct benefit hypotheses. Am Nat 141:440-465.
78. Wiehle H. 1961. Der Embolus des männlichen Spinnentasters. Zool Anz Suppl 24:457-480.
79. Wiehle H. 1967. Steckengebliebene Emboli in den Vulven von Spinnen (Arachnida, Araneae). Senckenberg Biol 48:197-202.