Reproduction in context: Field testing a laboratory model of socially controlled sex change in Lythrypnus

Social interactions can have profound effects on reproduction and the proximate mechanisms involved are just beginning to be understood. Lythrypnus dalli, the bluebanded goby, is an ideal organism for analyzing the dynamics of socially controlled sex change both in the laboratory and field. As with most research species, the majority of its behavioural and physiologic study has been performed in the laboratory. The goal of our study was to induce sex change of L. dalli in a more natural environment and compare field dynamics with our laboratory-based model. Groups of L. dalli, composed of one large male and three females of varying sizes, were introduced into artificial habitats in the field. After male removal, the dominant, largest female underwent protogynous sex change in the majority of the groups. Within 15 days, 9 of 15 of the dominant females (focal fish) successfully fertilized eggs as males, compared to 13 of 17 in the laboratory. Focal fish displayed the distinctive temporal sequence of behaviour changes consisting of a dominance, quiescent, and courtship phase. In addition, focal fish had gonads, genital papillae, and accessory gonadal structures with morphology in between that of females and males. Those fish that fertilized eggs had this transitional morphology, but were functionally male. Steroids of focal fish were assayed by water sample, and morning samples of free 11-ketotestosterone (11-KT) positively correlated with the percent of male tissue in the gonad, with the size of the accessory gonadal structure but not the genitalia (genital papilla), and with aggressive displacement behaviour on the last day before the fish were sacrificed. These morphological, physiological, and behavioural patterns parallel those seen in the laboratory. Lower rates of behaviour and the dramatic

[1]  L. Fishelson Comparative Cytology and Morphology of Seminal Vesicles in male gobiid fishes , 1991 .

[2]  A. Bass,et al.  Gonadal steroids affect LHRH preoptic cell number in a sex/role changing fish. , 1991, Journal of neurobiology.

[3]  Rui F. Oliveira,et al.  Effects of 11‐ketotestosterone on genital papilla morphology in the sex changing fish Lythrypnus dalli , 2000 .

[4]  R. Jardim Effects of 11-ketotestosterone on genital papilla morphology in the sex changing fish Lythrypnus dalli S. L. C*, S. K. M-M*, A. V. M. C†, R. F. O‡, L. C‡ M. S. G*¶ , 2000 .

[5]  Rui F. Oliveira,et al.  Social Modulation of Sex Steroid Concentrations in the Urine of Male Cichlid FishOreochromis mossambicus , 1996, Hormones and Behavior.

[6]  R. Wootton,et al.  Fish Reproduction: Strategies and Tactics , 1984 .

[7]  M. Steele Effects of predators on reef fishes: separating cage artifacts from effects of predation , 1996 .

[8]  J. Wiley Life histories and systematics of the western North American gobies Lythrypnus dalli (Gilbert) and Lythrypnus zebra (Gilbert) , 1976 .

[9]  T. Miura,et al.  Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D. Shapiro,et al.  Gonad Structure and Hermaphroditism in the Gobiid Genus Coryphopterus (Teleostei: Gobiidae) , 1990 .

[11]  A. Scott,et al.  Dynamics of excretion of 17α, 20β-dihydroxy-4-pregnen-3-one 20-sulphate, and of the glucuronides of testosterone and 17β-oestradiol, by urine of reproductively mature male and female rainbow trout (Oncorhynchus mykiss) , 1994 .

[12]  T. Hourigan,et al.  Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey , 1989, Environmental Biology of Fishes.

[13]  M. Grober,et al.  An integrative approach to sex change: social, behavioural and neurochemical changes in Lythrypnus dalli (Pisces) , 1999, acta ethologica.

[14]  Y. Sadovy,et al.  Criteria for the Diagnosis of Hermaphroditism in Fishes , 1987 .

[15]  C. Mazzoldi,et al.  SPERM COMPETITION AND MODE OF FERTILIZATION IN THE GRASS GOBY ZOSTERISESSOR OPHIOCEPHALUS (TELEOSTEI : GOBIIDAE) , 1999 .

[16]  R. Ross,et al.  The evolution of sex-change mechanisms in fishes , 1990, Environmental Biology of Fishes.

[17]  P. Nelson,et al.  Social Control of Sex Reversal in a Coral-Reef Fish , 1972, Science.

[18]  K. Aida,et al.  Induction of Testis Development by Implantation of 11-Ketotestosterone in Female Goldfish , 1991 .

[19]  K. B. Hartney The foraging ecology of two sympatric gobiid fishes: importance of behavior in prey type selection , 1989, Environmental Biology of Fishes.

[20]  P. J. Miller The tokology of gobioid fishes , 1984 .

[21]  K. Cole,et al.  Gonad Morphology, Colony Demography and Evidence for Hermaphroditism in Gobiodon Okinawae (Teleostei, Gobiidae) , 2001, Environmental Biology of Fishes.

[22]  L. A. Carneiro,et al.  Watching fights raises fish hormone levels , 2001, Nature.

[23]  A. Marconato,et al.  On the mechanism of sperm release in three gobiid fishes (Teleostei: Gobiidae) , 1996, Environmental Biology of Fishes.

[24]  C. Mazzoldi,et al.  Reproductive apparatus and male accessory structures in two batrachoid species (Teleostei, Batrachoididae) , 2001 .

[25]  J. Wingfield,et al.  Sex Steroid Levels in Porichthys notatus, a Fish with Alternative Reproductive Tactics, and a Review of the Hormonal Bases for Male Dimorphism among Teleost Fishes , 1993, Hormones and Behavior.

[26]  R. C. Anderson Why do fish have so few roundworm (nematode) parasites? , 1996, Environmental Biology of Fishes.

[27]  M. Grober,et al.  An initial description of alternative male reproductive phenotypes in the bluebanded goby, Lythrypnus dalli (Teleostei, Gobiidae) , 2005, Environmental Biology of Fishes.

[28]  R. Ross Anatomical changes associated with sex reversal in the fish Thalassoma duperrey (Teleostei: Labridae) , 1984 .

[29]  Daniel J. Miller Miller and Lea's Guide to the Coastal Marine Fishes of California. , 1972, Ichthyology & Herpetology.

[30]  J. Godwin,et al.  Sex change and steroid profiles in the protandrous anemonefish Amphiprion melanopus (Pomacentridae, Teleostei). , 1993, General and comparative endocrinology.

[31]  Does gonad structure reflect sexual pattern in all gobiid fishes , 1994 .

[32]  C. R. Kramer,et al.  The effects of testosterone implants on ovarian morphology in the bluehead wrasse, Thalassoma bifasciatum (Bloch) (Teleostei: Labridae) , 1988 .

[33]  E. Ferrero,et al.  The seminal vesicles of the male grass goby,Zosterisessor ophiocephalus (Teleostei, Gobiidae) , 1992, Zoomorphology.

[34]  M. Steele The relative importance of predation and competition in two reef fishes , 1998, Oecologia.

[35]  C. Mary CHARACTERISTIC GONAD STRUCTURE IN THE GOBIID GENUS LYTHRYPNUS WITH COMPARISONS TO OTHER HERMAPHRODITIC GOBIES , 1998 .

[36]  F. Kroon,et al.  The role of steroid hormones in protogynous sex change in the Blackeye goby, Coryphopterus nicholsii (Teleostei: Gobiidae). , 2000, General and comparative endocrinology.

[37]  R. F. Oliveira,et al.  Endocrine correlates of male polymorphism and alternative reproductive tactics in the Azorean rock-pool blenny, Parablennius sanguinolentus parvicornis. , 2001, General and comparative endocrinology.

[38]  K. B. Hartney,et al.  The effect of sea urchins as biogenic structures on the local abundance of a temperate reef fish , 2002, Oecologia.

[39]  R. Ross,et al.  Sex Change in a Coral-Reef Fish: Dependence of Stimulation and Inhibition on Relative Size , 1983, Science.

[40]  C. Mary Novel sexual patterns in two simultaneously hermaphroditic gobies, Lythrypnus dalli and Lythrypnus zebra , 1993 .

[41]  R. F. Oliveira,et al.  Effects of Androgens on Social Behavior and Morphology of Alternative Reproductive Males of the Azorean Rock-Pool Blenny , 2001, Hormones and Behavior.

[42]  C. Mary Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction , 1994 .

[43]  D. R. Robertson,et al.  Does gonad structure reflect sexual pattern in all gobiid fishes? , 2004, Environmental Biology of Fishes.

[44]  J. Godwin,et al.  Hypothalamic Arginine Vasotocin mRNA Abundance Variation Across Sexes and with Sex Change in a Coral Reef Fish , 2000, Brain, Behavior and Evolution.

[45]  D. Shapiro Behavioural changes of protogynous sex reversal in a coral reef fish in the laboratory , 1981, Animal Behaviour.

[46]  R. R. Warner Mating Behavior and Hermaphroditism in Coral Reef Fishes , 1984 .

[47]  J. Wingfield,et al.  The "Challenge Hypothesis": Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies , 1990, The American Naturalist.