Skip to main content
SpringerLink
Log in

Modifications of the reproductive complex and implications for the reproductive biology of Gobiodon oculolineatus (Teleostei: Gobiidae)

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The reproductive anatomy of gobiid fishes (Family Gobiidae) exhibits remarkable morphological diversity and complexity. However, there has been little in the way of detailed anatomical descriptions of species-specific reproductive anatomy among gobiid fishes that could be used to generate hypotheses of homology. Consequently, identifying valid reproductive synapomorphies among extant gobiid lineages remains problematic. Gobiodon oculolineatus, an obligate coral-dwelling fish, exhibits several unusual modifications of the reproductive complex associated with its hermaphroditic sexual pattern and with the production and storage of secretory material. All post-indifferent individuals had either an ovariform gonad or an ovotestis. In addition, all individuals had fully developed secretory structures derived from the gonoduct wall with secretory activity being greatest among male-active fish. Among male-active fish, part of the ovotestis was modified for the storage of secreted material. Based on current reportage, the combination of features seen in G. oculolineatus is unique, with the exception of a congener, G. okinawae, the only other species in the genus for which detailed information on reproductive anatomy is available. This study represents the first step towards identifying and characterizing the functional and anatomical components of the reproductive system in a gobiid taxon in order to develop testable hypotheses regarding homology and the nature of adaptive modifications of various components of the gobiid reproductive system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akihito [Prince], Iwata A, Kobayashi T, Ikeo K, Imanishi T, Ono H, Umehara Y, Hamamatsu C, Sugiyama K, Ikeda Y, Sakamoto K, Fumihito A, Ohno S, Gojobori T (2000) Evolutionary aspects of gobioid fishes based upon a phylogenetic analysis of mitochondrial cytochrome b genes. Gene 259:5–15. doi:10.1016/S0378-1119(00)00488-1

    Article  PubMed  CAS  Google Scholar 

  • Arai R (1964) Sex characters of Japanese gobioid fishes. Bull Natl Sci Mus, Tokyo 7:295–306

    Google Scholar 

  • Asahina K, Suzuki K, Aida K, Hibiya T, Tamaoki B (1985) Relationship between the structures and steroidogenic functions of the testes of the urohaze-goby (Glossogobius olivaceus). Gen Comp Endocrinol 57:281–292. doi:10.1016/0016-6480(85)90273-4

    Article  PubMed  CAS  Google Scholar 

  • Arbuckle WJ, Bélangera AJ, Corkum LD, Zielinski BS, Li W, Yun S-S, Bachynski S, Scott AP (2005) In vitro biosynthesis of novel 5β-reduced steroids by the testis of the round goby, Neogobius melanostomus. Gen Comp Endocrinol 140:1–13. doi:10.1016/j.ygcen.2004.09.014

    Article  PubMed  CAS  Google Scholar 

  • Bonnin PJ (1975) Organotype culture of glandular tissue of the testis of Gobius niger L. Association with hypophysis. C R Seances Soc Biol Fil 169:548–552. (Comptes rendus des séances de la Société de biologie et de ses filiales)

  • Brusléa S (1987) Sex-inversion of the hermaphroditic, protogynous teleost Coris julis L. (Labridae). J Fish Biol 30:605–616. doi:10.1111/j.1095-8649.1987.tb05788.x

    Article  Google Scholar 

  • Bruslé S, Bruslé J (1978) An ultrastructural study of early germ cells in Mugil (Liza) auratus Risso, 1810 (Teleostei : Mugilidae). Ann Biol anim Bioch Biophys 18:1141–1153

    Article  Google Scholar 

  • Bruslé-Sicard S, Debas L, Fourcault B, Fuchs J (1992) Ultrastructural study of sex inversion in a protogynous hermaphrodite, Epinephelus microdon (Teleostei, Serranidae). Reprod Nutr Dev 32:393–406. doi:10.1051/rnd:19920409

    Article  PubMed  Google Scholar 

  • Cole KS (1988) Predicting the potential for sex-change on the basis of ovarian structure in gobiid fishes. Copeia 1988:1082–1086. doi:10.2307/1445741

    Article  Google Scholar 

  • Cole KS (1990) Patterns of gonad structure in hermaphroditic gobies. Environ Biol Fishes 28:125–142. doi:10.1007/BF00751032

    Article  Google Scholar 

  • Cole KS (2008) Transient ontogenetic expression of hermaphroditic gonad morphology within the Gobiosoma group of the Neotropical seven-spined gobies (Teleostei: Gobiidae). Mar Biol (Berl) 154:943–951. doi:10.1007/s00227-008-0986-z

    Article  Google Scholar 

  • Cole KS, Shapiro DY (1992) Gonadal structure and population characteristics of the protogynous goby Coryphopterus glaucofraenum. Mar Biol (Berl) 113:1–9. doi:10.1007/BF00367632

    Article  Google Scholar 

  • Cole KS, Robertson DR (1988) Protogyny in the Caribbean reef goby, Coryphopterus personatus: gonad ontogeny and social influences on sex change. Bull Mar Sci 42:317–333

    Google Scholar 

  • Cole KS, Hoese DF (2001) Gonad morphology, colony demography and evidence for hermaphroditism in Gobiodon okinawae (Teleostei, Gobiidae). Environ Biol Fishes 61:161–173. doi:10.1023/A:1011032228716

    Article  Google Scholar 

  • Cole KS, Robertson DR, Cedeño AA (1994) Does gonad structure reflect sexual pattern in all gobiid fishes? Environ Biol Fishes 41:301–309

    Google Scholar 

  • Colombo L, Burighel P (1974) Fine structure of the testicular gland of the black goby, Gobius jozo L. Cell Tissue Res 154:39–49. doi:10.1007/BF00221070

    Article  PubMed  CAS  Google Scholar 

  • Colombo L, Marconato A, Belvedere PC, Friso C (1980) Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Boll Zool 47:355–364

    Google Scholar 

  • Doitsidou M, Reichman-Fried M, Stebler J, Köprunner M, Dörries J, Meyer D, Esguerra CV, Leung T, Raz E (2002) Guidance of PGC migration by the chemokine SDF-1. Cell 111:647–659. doi:10.1016/S0092-8674(02)01135-2

    Article  PubMed  CAS  Google Scholar 

  • Egami N (1960) Comparative morphology of the sex characters in several species of Japanese gobies, with reference to the effects of sex steroids on the characters. J Fac Sci, Univ Tokyo. Sec IV 9:67–100

    Google Scholar 

  • Essenberg JM (1923) Sex-differentiation in the viviparous teleost Xiphophorus helleri Heckel. Biol Bull 45:46–97. doi:10.2307/1536637

    Article  Google Scholar 

  • Harold AS, Winterbottom R, Munday PL, Chapman RW (2008) Phylogenetic relationships of Indo-pacific coral gobies of the genus Gobiodon (Teleostei: Gobiidae), based on morphological and molecular data. Bull Mar Sci 82:119–136

    Google Scholar 

  • Hiatt RW, Strasburg DW (1960) Ecological relationships of the fish fauna on croal reefs of the Marshall Islands. Ecol Monogr 30:65–127. doi:10.2307/1942181

    Article  Google Scholar 

  • Hoese DF, Gill AC (1993) Phylogenetic relationships of eleotrid fishes (Perciformes: Gobioidei). Bull Mar Sci 52:415–440

    Google Scholar 

  • Kroon FJ, Munday PL, Westcott DA, Hobbs JP, Liley NR (2005) Aromatase pathway mediates sex change in each direction. Proc Royal Soc London. Biol Sci 272:1399–1405. doi:10.1098/rspb.2005.3097

    Article  CAS  Google Scholar 

  • Kurokawa H, Aoki Y, Nakamura S, Ebe Y, Kobayash D, Tanaka M (2006) Time-lapse analysis reveals different modes of primordial germ cell migration in the medaka Oryzias latipes. Dev Growth Differ 48:209–221. doi:10.1111/j.1440-169X.2006.00858.x

    Article  PubMed  Google Scholar 

  • Lee Y-H, Du J-L, Yueh W-S, Lin B-Y, Huang J-D, Lee C-Y, Lee M-F, Lau E-L, Lee F-Y, Morrey C, Nagahama Y, Chang C-F (2001) Sex change in the protandrous black porgy, Acanthopagrus schlegeli: a review in gonadal development, estradiol, estrogen receptor, aromatase activity and gonadotropin. J Exp Zool 290:715–726. doi:10.1002/jez.1122

    Article  PubMed  CAS  Google Scholar 

  • Lo Nostro F, Grier H, Andreone L, Guerrero GA (2003) Involvement of the gonadal germinal epithelium during sex reversal and seasonal testicular cycling in the protogynous swamp eel, Synbranchus marmoratus Bloch 1795 (teleostei, synbranchidae). J Morphol 257:107–126. doi:10.1002/jmor.10105

    Article  PubMed  CAS  Google Scholar 

  • Miller PJ (1984) The tokology of gobioid fishes. In: Potts GW, Wootton RJ (eds) Fish reproduction: strategies and tactics. Academic Press, London, England, pp 119–153

    Google Scholar 

  • Miller PJ (1986) Reproductive biology and systematic problems in gobioid fishes. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-Pacific fish biology. Tokai Univ Press, Tokyo, Japan, pp 640–647

    Google Scholar 

  • Miller PJ (1992) The sperm duct gland: a visceral synapomorphy for gobioid fishes. Copeia 1992:253–256. doi:10.2307/1446565

    Article  Google Scholar 

  • Munday PL (2002) Bi-directional sex change: testing the growth-rate advantage model. Behav Ecol Sociobiol 52:247–254. doi:10.1007/s00265-002-0517-8

    Article  Google Scholar 

  • Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser 152:227–239. doi:10.3354/meps152227

    Article  Google Scholar 

  • Munday PL, Caley MJ, Jones GP (1998) Bi-directional sex change in a coral-dwelling goby. Behav Ecol Sociobiol 43:371–377. doi:10.1007/s002650050504

    Article  Google Scholar 

  • Munday PL, Harold AS, Winterbottom R (1999) Guide to the coral-dwelling gobies, genus Gobiodon (Gobiidae) from Papua New Guinea and the Great Barrier Reef. Rev Fr Aquariol 26:49–54

    Google Scholar 

  • Munday PL, Cardoni AM, Syms C (2006) Cooperative growth regulation in coral-dwelling fishes. Biol Lett 2:355–358. doi:10.1098/rsbl.2006.0488

    Article  PubMed  Google Scholar 

  • Nakashima Y, Kuwamua T, Yogo Y (1996) Both-ways sex change in monogamous coral gobies, Gobiodon spp. Environ Biol Fishes 46:281–288. doi:10.1007/BF00005004

    Article  Google Scholar 

  • Parmentier HK, Timmermans LPM (1985) The differentiation of germ cells and gonads during development of carp (Cyprinus carpio L.). A study with anti-carp sperm monoclonal antibodies. J Embryol Exp Morphol 90:13–32

    CAS  Google Scholar 

  • Pezold F (1993) Evidence for monophyletic Gobiinae. Copeia 1993:634–643. doi:10.2307/1447224

    Article  Google Scholar 

  • Rasotto MB, Mazzoldi C (2002) Male traits associated with alternative reproductive tactics in Gobius niger. J Fish Biol 61:173–184. doi:10.1111/j.1095-8649.2002.tb01744.x

    Article  Google Scholar 

  • Stanley H, Chieffi G, Botte V (1965) Histological and histochemical observations on the testis of Gobius paganellus. Zeit. Zellforsch 65:350–362. doi:10.1007/BF00345636

    Article  CAS  Google Scholar 

  • Suzuki A, Tanaka M, Shibata N (2004) Expression of aromatase mRNA and effects of aromatase inhibitor during ovarian development in the medaka, Oryzias latipes. J Exp Zool 310A:266–273. doi:10.1002/jez.a.20027

    Article  Google Scholar 

  • Thacker CE (2003) Molecular phylogeny of the gobioid fishes (Teleostei: Perciformes: Gobioidei). Mol Phylogenet Evol 26:354–368. doi:10.1016/S1055-7903(02)00361-5

    Article  PubMed  CAS  Google Scholar 

  • Timmermans LPM, Taverne N (1983) Origin and differentiation of primordial germ cells (PGC’s) in the rosy barb, Barbus conchonius, (Cyprinidae, Teleostei). Acta Morphol Neerl Scand 21:182

    Google Scholar 

  • Tyler JC (1971) Habitat preferences of the fishes that dwell in shrub corals on the Great Barrier Reef. Proc Acad Nat Sci 123:1–26

    Google Scholar 

  • Young RT, Fox DL (1937) The seminal vesicles of the goby, with preliminary chemical and physiological studies of the vesicular fluid. Proc Natl Acad Sci USA 23:461–467. doi:10.1073/pnas.23.8.461

    Article  PubMed  CAS  Google Scholar 

  • Xia L, Cheng H, Yu H, Guo Y, Zhou R (2004) Molecular cloning and expression of the osteoclast-stimulating-factor-like gene from the rice field eel. J Exp Zoolog B Mol Dev Evol 302:174–181. doi:10.1002/jez.b.20008

    PubMed  Google Scholar 

Download references

Acknowledgments

Portions of this study were supported by an Australian Museum Curatorial Fellowship to the author and from funds provided by the University of Hawaii at Manoa. I thank D. Hoese for his sponsorship and innumerable helpful conversations, S. Reader for field collection assistance, Ellyn Tong for the artwork for Figure 1, B. Vine for help with digital imaging, A. Dewan for statistical assistance, T. Harold for information on Gobiodon phylogenetics, F. Pezold for insightful comments on the manuscript and informative discussions and two anonymous reviewers.

Author information

Authors and Affiliations

  1. University of Hawaii at Manōa, 2538 McCarthy Mall, Edmondson 160, Honolulu, Hawaii, 96822, USA

    Kathleen S. Cole

Authors
  1. Kathleen S. Cole
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathleen S. Cole.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cole, K.S. Modifications of the reproductive complex and implications for the reproductive biology of Gobiodon oculolineatus (Teleostei: Gobiidae). Environ Biol Fish 84, 261–273 (2009). https://doi.org/10.1007/s10641-008-9433-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-008-9433-8

Keywords

Search

Navigation