Intersexuality and behavior in crayfish: The de-masculinization effects of androgenic gland ablation

Hormones and Behavior

Volumn 50, Issue 2, 2006, Pages 322-331

  Barki, Assaf ^a   Karplus, Ilan ^a   Manor, Rivka ^b   Sagi, Amir ^b  

^a VOLCANI CENTER   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Agonistic behavior; Androgenic gland; Androgenic hormone; Cherax quadricarinatus; Crayfish; Crustacea; Decapoda; Fighting; Intersexuality; Mating behavior; Vitellogenesis; Vitellogenin gene

Indexed keywords

VITELLOGENIN;

ADOLESCENT; ANDROGENIC GLAND ABLATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; COPULATION; CRAYFISH; ENDOCRINE SURGERY; FEMALE; FEMININITY; FIGHTING; GENETIC TRANSCRIPTION; GENOTYPE; HERMAPHRODITISM; JUVENILE; MALE; MATING; MORPHOLOGY; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; VITELLOGENESIS;

AGONISTIC BEHAVIOR; ANDROGENS; ANIMALS; ASTACOIDEA; COPULATION; FEMALE; FERTILIZATION; GENE EXPRESSION; MALE; OVARY; OVUM; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; TESTIS; VITELLOGENESIS;

EID: 33745912514     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2006.03.017     Document Type: Article

References (68)

1. Abdu U., Davis C., Khalaila I., and Sagi A. The vitellogenin cDNA of Cherax quadricarinatus encodes a lipoprotein with calcium binding ability, and its expression is induced following the removal of the androgenic gland in a sexually plastic system. Gen. Comp. Endocrinol. 127 (2002) 263-272
2. Azzauna A., Greve P., and Martin G. Sexual differentiation traits in functional males with female genital apertures (♂fga) in the woodlice Armadillidium vulgare Latr. (Isopoda, Crustacea). Gen. Comp. Endocrinol. 138 (2004) 42-49
3. Barki A., and Karplus I. Mating behavior and a behavioral assay for female receptivity in the red claw crayfish, Cherax quadricarinatus (von Martens). J. Crustac. Biol. 19 (1999) 493-497
4. Barki A., Karplus I., and Goren M. Effects of size and morphotype on dominance hierarchies and resource competition in the freshwater prawn Macrobrachium rosenbergii. Anim. Behav. 44 (1992) 547-555
5. Barki A., Harpaz S., and Karplus I. Contradictory asymmetries in body and weapon size, and assessment in fighting male prawns, Macrobrachium rosenbergii. Aggress. Behav. 23 (1997) 81-91
6. Barki A., Levi T., Hulata G., and Karplus I. Annual cycle of spawning and molting in the red-claw crayfish, Cherax quadricarinatus, under laboratory conditions. Aquaculture 157 (1997) 239-249
7. Barki A., Karplus I., Khalaila R., Manor, and Sagi A. Male-like behavioral patterns and physiological alterations induced by androgenic gland implantation in female crayfish. J. Exp. Biol. 206 (2003) 1791-1797
8. Berreur-Bonnenfant J., and Lawrence F. Comparative effect of farnesylacetone on macromolecular synthesis in gonads of crustaceans. Gen. Comp. Endocrinol. 54 (1984) 462-468
9. Bruski C.A., and Dunham D.W. The importance of vision in agonistic communication of the crayfish Orconectes rusticus: I. An analysis of bout dynamics. Behaviour 63 (1987) 83-107
10. Bulnheim H.-P. Sex transformation in Gammarus duebeni under the influence of hormonal and parasitic factors. Biol. Zentralbl. 96 (1977) 61-78
11. Chang E.S. Crustacean hyperglycemic hormone family: old paradigms and new perspectives. Am. Zool. 41 (2001) 380-388
12. Charniaux-Cotton H. Sex determination. In: Waterman T.H. (Ed). The Physiology of Crustacea vol. 1 (1960), Academic Press, New York 411-447
13. Charniaux-Cotton H., and Payen G. Sexual differentiation. In: Bliss D.E., and Mantel L.H. (Eds). The Biology of Crustacea (1985), Academic Press, New York 217-299
14. Charniaux-Cotton H., and Payen G. Crustacean reproduction. In: Laufer H., and Downer R.G.H. (Eds). Endocrinology of Selected Invertebrate Type (1988), Alan R. Liss, New York 279-303
15. Curtis M.C., and Jones C.M. Observation on monosex culture of redclaw crayfish Cherax quadricarinatus von Martens (Decapoda: Parastcidae) in earthen ponds. J. World Aquac. Soc. 26 (1995) 154-159
16. Darwin C. The Descent of Man and Selection in Relation to Sex (1871), Murray, London
17. Dunn O.J. Multiple comparisons using rank sums. Technometrics 6 (1964) 241-252
18. Dunn A.M., Adams J., and Smith J.E. Intersexes in a shrimp: a possible disadvantage of environmental sex determination. Evolution 44 (1990) 1875-1878
19. Dunn A.M., Adams J., and Smith J.E. Intersexuality in the crustacean Gammarus duebeni. Invertebr. Reprod. Dev. 25 (1994) 139-142
20. Fingerman M. Endocrine mechanisms in crayfish, with special emphasis on reproduction and neurotransmitter regulation of hormone release. Am. Zool. 33 (1995) 403-411
21. Fingerman M. Roles of neurotransmitters in regulating reproductive hormone release and gonadal maturation in decapod crustaceans. Invertebr. Reprod. Dev. 31 (1997) 47-54
22. Ford A.T., and Fernandes T.F. Notes on the occurrence of intersex in amphipods. Hydrobiologia 548 (2005) 313-318
23. Ford A.T., Fernandes T.F., Rider S.A., Read P.A., Robinson C.D., and Davies I.M. Reproduction in the amphipod, Echinogammarus marinus: a comparison between normal and intersex specimens. J. Mar. Biol. Assoc. UK 83 (2003) 937-940
24. Ford A.T., Fernandes T.F., Read P.A., Robinson C.D., and Davies I.M. The cost of intersexuality: a crustacean perspective. Mar. Biol. 145 (2004) 951-957
25. Ford A.T., Fernandes T.F., Rider S.A., Read P.A., Robinson C.D., and Davies I.M. Endocrine disruption in a marine amphipod? Field observations of intersexuality and de-masculinisation. Mar. Environ. Res. 58 (2004) 169-173
26. Ford A.T., Rodgers-Gray T.P., Davies I.M., Dunn A.M., Read P.A., Robinson C.D., Smith J.E., and Fernandes T.F. Abnormal gonadal morphology in intersex, Echinogammarus marinus (Amphipoda): a possible cause of reduced fecundity?. Mar. Biol. 147 (2005) 913-918
27. Gleeson R.A., Adams M.A., and Smith III A.B. Hormonal modulation of pheromone-mediated behavior in a crustacean. Biol. Bull. 172 (1987) 1-9
28. Huber R. Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena. J. Comp. Physiol., A Sens. Neural Behav. Physiol. 191 (2005) 231-239
29. Huber R., Daws A.G., Tuttle S.A., and Panksepp J.B. Quantitative behavioral techniques for the study of crustacean aggression. In: Wiese K. (Ed). The Crustacean Nerve System (2002), Springer-Verlag, Berlin 186-201
30. Hull E.M., Meisel R.L., and Sachs B.D. Male sexual behavior. In: Pfaff D.W. (Ed). Hormones, Brain and Behavior vol. 1 (2002), Academic Press, San Diego 3-137
31. Karplus I., Khalaila I., Sagi A., and Barki A. The influence of androgenic gland implantation on the agonistic behavior of female crayfish (Cherax quadricarinatus) in interactions with males. Behaviour 140 (2003) 649-663
32. Katakura Y. Endocrine and genetic control of sex differentiation in the Malacostracan Crustacea. Invertebr. Reprod. Dev. 16 (1989) 177-182
33. Kelley D.B. Sexually dimorphic behaviors. Annu. Rev. Neurosci. 11 (1988) 225-251
34. Kelly A., Hatcher M.J., and Dunn A.M. Intersexuality in the amphipod, Gammarus duebeni results from incomplete feminisation by the vertically transmitted parasitic sex ratio distorter Nosema granulosis. Evol. Ecol. 18 (2004) 121-132
35. Khalaila I., Weil S., and Sagi A. Endocrine balance between male and female components of the reproductive system in intersex Cherax quadricarinatus (Decapoda: Parastacidae). J. Exp. Zool. 283 (1999) 286-294
36. Khalaila I., Katz T., Abdu U., Yehezkel G., and Sagi A. Effects of implantation of hypertrophied androgenic glands on sexual characters and physiology of the reproductive system in the female red claw crayfish, Cherax quadricarinatus. Gen. Comp. Endocrinol. 121 (2001) 242-249
37. Khalaila I., Manor R., Weil S., Granot Y., Keller R., and Sagi A. The eyestalk-androgenic gland-testis axis in the crayfish Cherax quadricarinatus. Gen. Comp. Endocrinol. 127 (2002) 147-156
38. King D.S. Fine structure of the androgenic gland of the crab, Pachygrapsus crassipes. Gen. Comp. Endocrinol. 4 (1964) 533-544
39. Kravitz E.A. King Solomon Lecture, serotonin and aggression: insights gained from a lobster system and speculations on the role of amine neurons in a complex behavior. J. Comp. Physiol., A Sens. Neural Behav. Physiol. 186 (2000) 221-238
40. Manor R., Aflalo E.D., Segall C., Weil S., Azulay D., Ventura T., and Sagi A. Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebr. Reprod. Dev. 45 (2004) 151-159
41. Martin G., Sorokine O., Moniatte M., and Van Dorsselaer A. The androgenic hormone of the crustacean isopod Armadillidium vulgare. Ann. N. Y. Acad. Sci. 839 (1998) 111-117
42. Martin G., Sorokine O., Moniatte M., Bulet P., Hetru C., and Van Dorsselaer A. The structure of a glycosylated protein hormone responsible for sex determination in the isopod, Armadillidium vulgare. Eur. J. Biochem. 262 (1999) 727-736
43. McCurdy D.G., Forbes M.R., Logan S.P., Kopec M.T., and Mautner S.I. The functional significance of intersexes in the intertidal amphipod Corophium volutator. J. Crustac. Biol. 24 (2004) 261-265
44. Miyawaki M., and Taketomi Y. The occurrence of an extended perinuclear space in androgenic gland cells of the crayfish, Procambarus clarkii. Cytologia 43 (1978) 351-355
45. Ohira T., Hasegawa Y., Tominaga S., Okuno A., and Nagasawa H. Molecular cloning and expression analysis of cDNAs encoding androgenic gland hormone precursors from two porcellionidae species, Porcellio scaber and P. dilatatus. Zool. Sci. 20 (2003) 75-81
46. Okuno A., Hasegawa Y., Ohira T., Katakura Y., and Nagasawa H. Characterization and cDNA cloning of androgenic gland hormone of the terrestrial isopod Armadillidium vulgare. Biochem. Biophys. Res. Commun. 264 (1999) 419-423
47. Parnes S., Khalaila I., Hulata G., and Sagi A. Sex determination in crayfish: are intersex Cherax quadricarinatus (Decapoda, Crustacea) genetically females?. Genet. Res. 82 (2003) 107-116
48. Pavey C.R., and Fielder D.R. The influence of size differential on agonistic behaviour in the freshwater crayfish, Cherax cuspidatus (Decapoda: Parastacidae). J. Zool. Lond. 238 (1996) 445-457
49. Payen G.G. Roles of androgenic gland hormone in determining the sexual characters in crustacea. In: Gupta A.P. (Ed). Morphogenetic Hormones of Arthropods. Roles in Histogenesis, Organogenesis, and Morphogenesis (1990), Rutgers University Press, New Jersey 431-452
50. Rigaud T., and Juchault P. Sterile intersexuality in an isopod induced by the interaction between a bacterium (Wolbachia) and the environment. Can. J. Zool. 76 (1998) 493-499
51. Rodgers-Gray T.P., Smith J.E., Ashcroft A.E., Isaac R.E., and Dunn A.M. Mechanisms of parasite-induced sex reversal in Gammarus duebeni. Int. J. Parasitol. 34 (2004) 747-753
52. Rudolph E. New records of intersexuality in the freshwater crayfish Samastacus spinifrons (Decapoda, Parastacidae). J. Crustac. Biol. 22 (2002) 377-389
53. Rudolph E., Verdi A., and Tapia J. Intersexuality in the burrowing crayfish Parastacus varicosus Faxon, 1898 (Decapoda, Parastacidae). Crustaceana 74 (2001) 27-37
54. Rutherford P.L., Dunham D.W., and Allison V. Winning agonistic encounters by male crayfish Orconectes rusticus (Girard) (Decapoda, Cambaridae): chela size matters but chela symmetry does not. Crustaceana 68 (1995) 526-529
55. Sagi A., and Khalaila I. The crustacean androgen: a hormone in an isopod and androgenic activity in decapods. Am. Zool. 41 (2001) 477-484
56. Sagi A., Khalaila I., Barki A., Hulata G., and Karplus I. Intersex red claw crayfish, Cherax quadricarinatus (von Martens): functional males with pre-vitellogenic ovaries. Biol. Bull. 190 (1996) 16-23
57. Sagi A., Snir E., and Khalaila I. Sexual differentiation in decapod crustaceans: role of the androgenic gland. Invertebr. Reprod. Dev. 31 (1997) 55-61
58. Sagi A., Khalaila I., Abdu U., Shoukrun R., and Weil S. A newly established ELISA showing the effect of the androgenic gland on secondary-vitellogenic-specific protein in the hemolymph of the crayfish Cherax quadricarinatus. Gen. Comp. Endocrinol. 115 (1999) 37-45
59. Sagi A., Manor R., Segall C., Davis C., and Khalaila I. On intersexuality in the crayfish Cherax quadricarinatus: an inducible sexual plasticity model. Invertebr. Reprod. Dev. 41 (2002) 27-33
60. In: Schulkin J. (Ed). The Neuroendocrine Regulation of Behavior (1999), Cambridge University Press, Cambridge, UK
61. Shechter A., Aflalo E.D., Davis C., and Sagi A. Expression of the reproductive female-specific vitellogenin gene in endocrinologically induced male and intersex Cherax quadricarinatus crayfish. Biol. Reprod. 73 (2005) 72-79
62. Shuster C.M. Female sexual receptivity associated with molting and differences in copulatory behavior among three male morphs in Paracerceis sculpta (Crustacea: Isopoda). Biol. Bull. 177 (1989) 331-337
63. Sneddon L.U., Huntingford F.A., and Taylor A.C. Weapon size versus body size as a predictor of winning in fights between shore crabs, Carcinus maenas (L.). Behav. Ecol. Sociobiol. 41 (1997) 237-242
64. Taketomi Y. Ultrastructure of the androgenic gland of the crayfish, Procambarus clarkii. Cell Biol.Int. Rep. 10 (1986) 131-136
65. Telecky T.M. Alternative male reproductive strategies in the giant Malaysian prawn Macrobrachium rosenbergii. Pac. Sci. 38 (1984) 372-373
66. Thiel M., and Correa C. Female rock shrimp Rhynchocinetes typus mate in rapid succession up a male dominance hierarchy. Behav. Ecol. Sociobiol. 57 (2004) 62-68
67. Tierney A.J., Godleski M.S., and Massanari J.R. Comparative analysis of agonistic behavior in four crayfish species. J. Crustac. Biol. 20 (2000) 54-66
68. Zou E., and Fingerman M. External features of an intersex fiddler crab, Uca pugilator (Bosc, 1802) (Decapoda, Brachyura). Crustaceana 73 (2000) 417-423