Female preference for males depends on reproductive physiology in the African cichlid fish Astatotilapia burtoni

General and Comparative Endocrinology

Volumn 180, Issue 1, 2013, Pages 56-63

  Kidd, Michael R ^a,b   O'Connell, Lauren A ^a   Kidd, Celeste E ^a   Chen, Christine W ^a   Fontenot, Miles R ^a   Williams, Sidney J ^a   Hofmann, Hans A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b TEXAS A AND M INTERNATIONAL UNIVERSITY   (United States)

Author keywords

Mate choice; Reproductive physiology; Sex steroid hormones; Sexual behavior; Sexual selection

Indexed keywords

ANDROGEN; GESTAGEN; PROSTAGLANDIN F2; PROSTAGLANDIN F2 ALPHA; SEX HORMONE; TESTOSTERONE;

AGGRESSION; ARTICLE; ASTATOTILAPIA BURTONI; BREEDING; CICHLID; CONTROLLED STUDY; COURTSHIP; FEMALE; MALE; MATE CHOICE; NONHUMAN; OOCYTE; OVULATION; PRIORITY JOURNAL; REPRODUCTION; SEXUAL BEHAVIOR; SPAWNING; STIMULUS RESPONSE; TESTOSTERONE RELEASE;

EID: 84870918724     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.10.014     Document Type: Article

References (60)

1. Adkins-Regan E. Hormonal mechanisms of mate choice. Am. Zool. 1998, 38:166-178.
2. Adkins-Regan E. Neuroendocrinology of social behavior. ILAR J. 2009, 50:5-14.
3. Asturiano J.F., Sorbera L.A., Ramos J., Kime D.E., Carrilo M., Zanuy S. Hormonal regulation of the European sea bass reproductive cycle: an individualized female approach. J. Fish Biol. 2000, 56:1155-1172.
4. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Methodol. 1995, 57:289-300.
5. Campbell C.M., Walsh J.M., Idler D.R. Steroids in the plasma of the winter flounder (Pseudopleuronectes americanus walbaum). A seasonal study and investigation of steroid involvement in oocyte maturation. Gen. Comp. Endocrinol. 1976, 29:14-20.
6. Chenoweth S.F., Blows M.W. Dissecting the complex genetic basis of mate choice. Nat. Rev. Genet. 2006, 7:681-692.
7. Clement T.S., Grens K.E., Fernald R.D. Female affiliative preference depends on reproductive state in the African cichlid fish, Astatotilapia burtoni. Behav. Ecol. 2005, 16:83-88.
8. Cole T.B., Stacey N.E. Olfactory responses to steroids in an African mouth-brooding cichlid, Haplochromis burtoni (Günther). J. Fish Biol. 2006, 68:661-680.
9. Cornish D.A. Seasonal steroid hormone profiles in plasma and gonads of the tilapia Oreochromis mossambicus. Water SA 1998, 24:257-263.
10. Cote I.M., Hunte W. Male and female mate choice in the redlip blenny: why bigger is better. Anim. Behav. 1989, 38:78-88.
11. Couldridge V.C.K., Alexander G.J. Does time spent near a male predict female mate choice in a Malawian cichlid?. J. Fish Biol. 2001, 59:667-672.
12. Coulter G.W. Lake Tanganyika and its Life Oxford 1991, Oxford University Press, Oxford, pp. 1-354.
13. Coward K., Bromage N.R. Histological classification of oocyte growth and the dynamics of ovarian recrudescence in Tilapia zillii. J. Fish Biol. 1998, 53:285-302.
14. Crews D. Evolution of neuroendocrine mechanisms that regulate sexual behavior. Trends Endocrinol. Metab. 2005, 16:354-361.
15. Desjardins J.K., Klausner J.Q., Fernald R.D. Female genomic response to mate information. Proc. Natl. Acad. Sci. USA 2010, 107:21176-21180.
16. Ferkin M.H., Zucker I. Seasonal control of odour preferences of meadow voles (Microtus pennsylvanicus) by photoperiod and ovarian hormones. J. Reprod. Fertil. 1991, 92:433-441.
17. Fernald R.D., Hirata N.R. Field study of Haplochromis burtoni: quantitative behavioural observations. Anim. Behav. 1977, 25:964-975.
18. Forlano P.M., Bass A.H. Neural and hormonal mechanisms of reproductive-related arousal in fishes. Horm. Behav. 2011, 59:616-629.
19. Forsgren E. Mate sampling in a population of sand gobies. Anim. Behav. 1997, 53:267-276.
20. Gabor C.R., Halliday T.R. Sequential mate choice by multiple mating smooth newts: females become more choosy. Behav. Ecol. 1997, 8:162-166.
21. Gavrilets S., Arnqvist G., Friberg U. The evolution of female mate choice by sexual conflict. Proc. R. Soc. Lond. B 2001, 268:531-539.
22. Hardin J., Hilbe J. Generalized Estimating Equations 2003, Chapman and Hall/CRC, London.
23. Harmin S.A., Crim L.W., Wiegand M.D. Plasma sex steroid profiles and the seasonal reproductive cycle in male and female winter flounder, Pleuronectes americanus. Mar. Biol. 1995, 121:601-610.
24. Hofmann H.A. Functional genomics of neural and behavioral plasticity. J. Neurobiol. 2003, 54:272-282.
25. Johnson K., Thomas P., Wilson R.R. Seasonal cycles of gonadal development and plasma sex steroid levels in Epinephelus morio, a protogynous grouper in the Eastern Gulf of Mexico. J. Fish Biol. 1998, 52:502-518.
26. Kidd C.E., Kidd M.R., Hofmann H.A. Measuring multiple hormones from a single water sample using enzyme immunoassays. Gen. Comp. Endocrinol. 2010, 165:277-285.
27. Kidd M.R., Danley P.D., Kocher T.D. A direct assay of female choice in cichlids: all the eggs in one basket. J. Fish. Biol. 2006, 68:373-384.
28. Kobayashi M., Aida K., Hanyu I. Hormone changes during ovulatory cycle in goldfish. Gen. Comp. Endocrinol. 1988, 69:301-307.
29. Kobayashi M., Aida K., Hanyu I. Involvement of steroid hormones in the preovulatory gonadotropin surge in female goldfish. Fish Physiol. Biochem. 1989, 7:141-146.
30. Kobayashi M., Sorensen P.W., Stacey N.E. Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol. Biochem. 2002, 26:71-84.
31. Kocher T.D. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 2004, 5:288-298.
32. Liley N.R., Stacey N.E. Hormones, pheromones and reproductive behavior. Fish Physiology 1983, vol. IXb:1-63. Academic Press, New York.
33. Lim H., Sorensen P.W. Polar metabolites synergize the activity of prostaglandin F2α in a species-specific hormonal sex pheromone released by ovulated common carp. J. Chem. Ecol. 2011, 37:695-704.
34. Macintosh D.J., Little D.C. Nile tilapia (Oreochromis niloticus). Broodstock Management and Egg and Larval Quality 2005, 277-320. Blackwell Science Ltda, London. N.R. Bromage, R.J. Roberts (Eds.).
35. Malison J.A., Procarion L.S., Barry T.P., Kapuscinski A.R., Kayes T.B. Endocrine and gonadal changes during the annual reproductive cycle of the freshwater teleost Stizostedion vitreum. Fish Physiol. Biochem. 1994, 13:473-484.
36. Maruska K.P., Fernald R.D. Steroid receptor expression in the fish inner ear varies with sex, social status, and reproductive state. BMC Neurosci. 2010, 11:58.
37. Maruska K.P., Ung U.S., Fernald R.D. The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance. PLoS One. 2012, 7:e37612.
38. McEwen B.S., Jones K.J., Pfaff D.W. Hormonal control of sexual behavior in the female rat: molecular, cellular and neurochemical studies. Biol. Reprod. 1987, 36:37-45.
39. Moore M.C., Crews D. Sex steroid hormones in natural populations of a sexual whiptail lizard Cnemidophorus inornatus, a direct evolutionary ancestor of a unisexual parthenogen. Gen. Comp. Endocrinol. 1986, 63:424-430.
40. Moore P.J., Moore A.J. Reproductive aging and mating: the ticking of the biological clock in female cockroaches. Proc. Natl. Acad. Sci. USA 2001, 98:9171-9176.
41. Munakata A., Kobayashi M. Endocrine control of sexual behavior in teleost fish. Gen. Comp. Endocrinol. 2010, 165:456-468.
42. Nadler R.D., Graham C.E., Gosselin R.E., Delwood C.C. Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycle of the chimpanzee (Pan troglodytes). Am. J. Primatol. 1985, 9:273-284.
43. Nagahama Y., Yamashita M. Regulation of oocyte maturation in fish. Dev. Growth Differ. 2008, 50:S195-S219.
44. Norberg B., Björnsson B.T., Brown C.L., Wichardt U.P., Deftos L.J., Haux C. Changes in plasma vitellogenin, sex steroids, calcitonin, and thyroid hormones related to sexual maturation in female brown trout (Salmo trutta). Gen. Comp. Endocrinol. 1989, 75:316-326.
45. Renn S.C.P., Aubin-Horth N., Hofmann H.A. Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 2004, 5:42.
46. Renn S.C.P., Fraser E.J., Aubin-Horth N., Trainor B.C., Hofmann H.A. Females of an African cichlid fish display male-typical social dominance behavior and elevated androgens in the absence of males. Horm. Behav. 2012, 61:496-503.
47. Rinchard J., Kestemont P., Kühn E.R., Fostier A. Seasonal changes in plasma levels of steroid hormones in an asynchronous fish the gudgeon Gobio gobio L. (Teleostei, Cyprinidae). Gen. Comp. Endocrinol. 1993, 92:168-178.
48. Robinson G.E., Fernald R.D., Clayton D.F. Genes and social behavior. Science 2008, 322:896-900.
49. Ryan M.J., Fox J.H., Wilczynski W., Rand A.S. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 1990, 343:66-67.
50. Salzburger W., Renn S.C., Steinke D., Braasch I., Hofmann H.A., Meyer A. Annotation of expressed sequence tags for the East African cichlid fish Astatotilapia burtoni and evolutionary analyses of cichlid ORFs. BMC Genomics 2008, 9:96.
51. Seehausen O., Witte F., Van Alphen J.J.M., Bouton N. Direct mate choice maintains diversity among sympatric cichlids in Lake Victoria. J. Fish Biol. 1998, 53:37-55.
52. Sisneros J.A., Forlano P.M., Knapp R., Bass A.H. Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen. Comp. Endocrinol. 2004, 136:101-116.
53. Sorensen P.W., Hara T.J., Stacey N.E., Goetz F.W. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 1988, 39:1039-1050.
54. Stacey N.E., Sorensen P.W. Reproductive pheromones. Fish Physiology 2006, 359-412. Elsevier Academic Press, San Diego. K.A. Sloman, R.W. Wilson, S. Balshine (Eds.).
55. Stelkens R.B., Pierotti M.E., Joyce D.A., Smith A.M., van der Sluijs I., Seehausen O. Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:2861-2870.
56. Suresh D.V., Baile V.V., Prasada Rao P.D. Annual reproductive phase-related profile of sex steroids and their carrier, SHBG, in the Indian major carp, Labeo rohita. Gen. Comp. Endocrinol. 2008, 159:143-149.
57. Tacon P., Baroiller J.F., Le Bail P.Y., Prunet P., Jalabert B. Effect of egg deprivation on sex steroids, gonadotropin, prolactin, and growth hormone profiles during the reproductive cycle of the mouthbrooding cichlid fish Oreochromis niloticus. Gen. Comp. Endocrinol. 2000, 117:54-65.
58. Uphouse L. Female gonadal hormones, serotonin, and sexual receptivity. Brain Res. Brain Res. Rev. 2000, 33:242-257.
59. Verzijden M.N., Van Heusden J., Bouton N., Witte F., Ten Cate C., Slabbekoorn H. Sounds of male Lake Victoria cichlids vary within and between species and affect female mate preferences. Behav. Ecol. 2010, 21:548-555.
60. Wilczynski W., Lynch K.S. Female sexual arousal in amphibians. Horm. Behav. 2011, 59:630-636.