Social cues elicit sexual behavior in subordinate Damaraland mole-rats independent of gonadal status

Hormones and Behavior

Volumn 65, Issue 1, 2014, Pages 14-21

  Carter, Sara N ^a   Goldman, Bruce D ^b   Goldman, Sharry L ^b   Freeman, David A ^a  

^a University of Memphis   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Cooperative breeding; Eusociality; Fossorial mammal; Gonadal steroids; Inbreeding avoidance; Mating systems

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GONAD; INBREEDING; INCEST; LORDOSIS QUOTIENT; MALE; MATING SYSTEM; MOUNTING BEHAVIOR; NONHUMAN; PRIORITY JOURNAL; RAT; REPRODUCTIVE BEHAVIOR; SEXUAL BEHAVIOR; SIBLING; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SOLICITATION BEHAVIOR; THRUSTING BEHAVIOR;

COOPERATIVE BREEDING; EUSOCIALITY; FOSSORIAL MAMMAL; GONADAL STEROIDS; INBREEDING AVOIDANCE; MATING SYSTEMS;

ANIMALS; CASTRATION; CUES; FEMALE; GONADS; INBREEDING; INCEST; MALE; MOLE RATS; RECOGNITION (PSYCHOLOGY); SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT;

EID: 84890209430     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.11.001     Document Type: Article

References (54)

1. Aoki S. Evolution of sterile soldiers in aphids. Animal Societies: Theories and Facts 1987, 53-65. Japan Science Society Press, Tokyo. Y. Ito, J.L. Brown, J. Kikkawa (Eds.).
2. Asa C.S., Goldfoot D.A., Garcia M.C., Ginther O.J. Sexual behavior in ovariectomized and seasonally anovulatory pony mares (Equus caballus). Horm. Behav. 1980, 14(1):46-54.
3. Baum M.J., Koos Slob A., de Jong F.H., Westbroek D.L. Persistence of sexual behavior in ovariectomized stumptail macaques following dexamethasone treatment or adrenalectomy. Horm. Behav. 1978, 11:323-347.
4. Beach F.A. Coital behavior in dogs: VI. Long-term effects of castration upon mating in the male. J. Comp. Physiol. Psychol. 1970, 70(3):1-32.
5. Beach F.A. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav. 1976, 7:105-138.
6. Bennett N.C., Faulkes C.G. African Mole-rats: Ecology and Eusociality 2000, Cambridge University Press, Cambridge UK.
7. Bennett N.C., Jarvis J.U.M., Faulkes C.G., Millar R.P. LH responses to single doses of exogenous GnRH by freshly captured Damaraland mole-rats, Cryptomys damarensis. J. Reprod. Fertil. 1993, 99:81-86.
8. Bennett N.C., Faulkes C.G., Molteno A.J. Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility. Proc. Biol. Sci. 1996, 263(1376):1599-1603.
9. Berthold A.A. Transplantation of testes. 1944. English translation by D.P. Quiring. Bull. Hist. Med. 1849, 16:399-401.
10. Beyer C., Cruz M.L., Rivaud N. Persistence of sexual behavior in ovariectomized-adrenalectomized rabbits treated with cortisol. Endocrinology 1969, 85:790-793.
11. Beyer C., Hoffman K., Gonzales-Flores O. Neuroendocrine regulation of estrous behavior in the rabbit: similarities and differences with the rat. Horm. Behav. 2007, 52:2-11.
12. Blaustein J.D. Minireview: neuronal steroid hormone receptors. Endocrinology 2004, 145(3):1075-1081.
13. Blaustein J.D. Neuroendocrine regulation of feminine sexual behavior: lessons from rodent models and thoughts about humans. Annu. Rev. Psychol. 2008, 59:93-118.
14. Clarke F.M., Miethe G.H., Bennett N.C. Reproductive suppression in female Damaraland mole-rats Cryptomys damarensis: dominant control or self-restraint?. Proc. Biol. Sci. 2001, 268:899-909.
15. Cooke B., Hegstrom C.D., Villeneuve L.S., Breedlove S.M. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol. 1998, 19:323-362.
16. Cooney R., Bennett N.C. Inbreeding avoidance and reproductive skew in a cooperative mammal. Proc. Biol. Sci. 2000, 267:801-806.
17. Costantini R.M., Park J.H., Beery A.K., Paul M.J., Ko J.J., Zucker I. Post-castration retention of reproductive behavior and olfactory preferences in male Siberian hamsters: role of prior experience. Horm. Behav. 2007, 51:149-155.
18. Crespi B.J. Eusociality in Australian gall thrips. Nature 1992, 359:724-726.
19. Duffy J.E. Eusociality in a coral-reef shrimp. Nature 1996, 381:512-514.
20. Everitt B.J., Herbert J. Adrenal glands and sexual receptivity in female rhesus monkeys. Nature 1969, 222:1065-1066.
21. Feder H.H. Hormones and sexual behavior. Annu. Rev. Psychol. 1984, 35:165-200.
22. Frye C.A., Bayon L.E., Pursnani N.K., Purdy R.H. The neurosteroids, progesterone and 3α, 5α-THP, enhance sexual motivation, receptivity, and proceptivity in female rats. Brain Res. 1998, 808:72-83.
23. Goldfoot D.A., Wiegand S.J., Scheffler G. Continued copulation of ovariectomized adrenal-suppressed stumptail macaques (Macaca arctoides). Horm. Behav. 1978, 11:89-99.
24. Gray D.S., Gorzalka B.B. Adrenal steroid interactions in female sexual behavior: a review. Psychoneuroendocrinology 1980, 5(2):157-175.
25. Hazell R.W.A., Bennett N.C., Jarvis J.U.M., Griffin M. Adult dispersal in the co-operatively breeding Damaraland mole-rat (Cryptomys damarensis): a case study from the Waterberg region of Namibia. J. Zool. 2000, 252:19-25.
26. Heth G., Todrank J., Begall S., Wegner R.E., Burda H. Genetic relatedness discrimination in eusocial Cryptomys anselli mole-rats, Bathyergidae, Rodentia. Folia Zool. Brno 2004, 53(3):269-278.
27. Holmes M.M., Goldman B.D., Goldman S.L., Seney M.L., Forger N.G. Neuroendocrinology and sexual differentiation in eusocial mammals. Front. Neuroendocrinol. 2009, 30:519-533.
28. Jacobs D.S., Reid S., Kuiper S. Out-breeding behaviour and xenophobia in the Damaraland mole-rat, Cryptomys damarensis. Afr. Zool. 1998, 33:189-194.
29. Jarvis J.U.M., Bennett N.C. Eusociality has evolved independently in two genera of bathyergid mole-rats - but occurs in no other subterranean mammal. Behav. Ecol. Sociobiol. 1993, 33:253-260.
30. Kendrick K.M., Dixson A.F. Ovariectomy does not abolish proceptive behaviour cyclicity in the common marmoset (Callithrix jacchus). J. Endocrinol. 1984, 101:155-162.
31. Kent D.S., Simpson J.A. Eusociality in the beetle Austroplatypus incomperus (Coleoptera: Curculiodae). Naturwissenschaften 1992, 79:86-87.
32. Mani S.K., Allen J.M., Clark J.H., Blaustein J.D., O'Malley B.W. Convergent pathways for steroid hormone- and neurotransmitter-induced rat sexual behavior. Science 1994, 265(5176):1246-1249.
33. 1 mouse: the role of experience. Anim. Behav. 1976, 24(3):523-533.
34. Maswanganye K.A., Bennett N.C., Brinders J., Cooney R. Oligospermia and azoospermia in non-reproductive male Damaraland mole-rats Cryptomys damarensis (Rodentia: Bathyergidae). J. Zool. 1999, 248:411-418.
35. Mateo J. Kin recognition in ground squirrels and other rodents. J. Mammal. 2003, 84(4):1163-1181.
36. McGill T.E., Haynes C.M. Heterozygosity and retention of ejaculatory reflex after castration in male mice. J. Comp. Physiol. Psychol. 1973, 84(2):423-429.
37. Mellon S.H., Griffin L.D., Compagnone N.A. Biosynthesis and action of neurosteroids. Brain Res. Rev. 2001, 37:3-12.
38. Mendonça M., Chernetsky S., Nester K., Gardner G. Effects of gonadal sex steroids on sexual behavior in the big brown bat, Eptesicus fuscus, upon arousal from hibernation. Horm. Behav. 1996, 30:153-161.
39. Molteno A.J., Bennett N.C. Anovulation in non-reproductive female Damaraland mole-rats (Cryptomys damarensis). J. Reprod. Fertil. 2000, 119:35-41.
40. Nelson R.J. An Introduction to Behavioral Endocrinology 2005, Sinauer, Sunderland, MA. third ed.
41. Nice P.A., Fleming P.A., Bennett N.C., Bateman P.W., Miller D.W. Exposure to non-kin females rapidly affects testicular morphology in non-reproductive male Damaraland mole-rats. J. Zool. 2010, 2010:1-7.
42. Pfaff D. Estrogens and Brain Function 1980, Springer-Verlag, New York.
43. Pfaff D.W., Schwartz-Giblin S. Cellular mechanisms of female reproductive behaviors. The Physiology of Reproduction 1988, 1487-1568. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
44. Pfaff D.W., Sakuma Y., Kow L.M., Lee A.W.L., Easton A. Hormonal, neural and genomic mechanism for female reproductive behaviors: motivational arousal. Physiology of Reproduction 2006, 1825-1920. Elsevier Academic Press, New York. E.K. Knobil, J.D. Neills (Eds.).
45. Phoenix C.H., Goy R.W., Arnold A.A., Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959, 65(3):369-382.
46. Rickard C.A., Bennett N.C. Recrudescence of sexual activity in a reproductively quiescent colony of the Damaraland mole-rat (Cryptomys damarensis), by the introduction of an unfamiliar and genetically unrelated male-a case of incest avoidance in 'queenless' colonies. J. Zool. 1997, 241(1):185-202.
47. Rissman E.F., Bronson F.H. Role of the ovary and adrenal gland in the sexual behavior of the musk shrew, Suncus murinus. Biol. Reprod. 1987, 36:664-668.
48. Rosenblatt J.S., Aronson L.R. The decline of male sexual behavior in male cats after castration with special reference to the role of prior sexual experience. Behaviour 1958, 12(4):285-338.
49. Sachs B.D., Meisel R.L. The physiology of male sexual behavior. The Physiology of Reproduction 1988, 1393-1485. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
50. Snyman P.C., Jackson C.R., Bennett N.C. Do dispersing non-reproductive female Damaraland mole-rats, Cryptomys damarensis (Rodentia: Bathyergidae) exhibit spontaneous or induced ovulation?. Physiol. Behav. 2006, 87(1):88-94.
51. Wallen K., Zehr J.L. Hormones and history: the evolution and development of primate female sexuality. J. Sex Res. 2004, 41(1):101-112.
52. Whalen R. Sexual behavior of cats. Behaviour 1963, 20(3/4):321-342.
53. Young W.C. The hormones and mating behavior. Sex and Internal Secretions 1961, volume II:1173-1239. Williams & Wilkins, Baltimore, MD. W.C. Young (Ed.).
54. Zhou S., Holmes M.M., Forger N.G., Goldman B.D., Lovern M.B., Caraty A., Kallo I., Faulkes C.G., Cohen C.W. Socially regulated reproductive development: analysis of GnRH-1 and kisspeptin neuronal systems in cooperatively breeding naked mole-rats (Heterocephalus glaber). J. Comp. Neurol. 2013, 521(13):3003-3029.