Skip to main content
Log in

An initial description of alternative male reproductive phenotypes in the bluebanded goby, Lythrypnus dalli (Teleostei, Gobiidae)

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

Synopsis

Contrary to the generally accepted life history theory regarding sequential hermaphroditism (‘size-advantage model’), we have recently identified ‘mini males’ in Lythrypnus dalli, the bluebanded goby. These are small (female-sized) fish that appear male based on their external genitalia. We investigated the reproductive anatomy and demography of these mini males. Based on their small size and the sexual plasticity of this species, we expected that mini males are not actually reproductively functioning males. However, when we examined their gonad anatomy, with particular attention to the male-typical accessory gonadal structure (AGS), we found that mini males have gonads that are comparable to those of nesting males in relative size and the percentage of tissue that is ‘male’ (testicular and AGS). Although this is contradictory to theories of sperm competition in alternative male phenotypes, reproductive strategies of these two types of males were clearly distinguishable based on their AGS content – as described in other examinations of differing ejaculate quality in alternative male phenotypes in the Gobiidae. Regular sampling of the L. dalli population showed that mini males make up a small fraction of the small size classes and that as the breeding season progressed, mini male frequency decreased and standard length increased significantly – thus allowing us to discuss their role within the social system. Based on these findings as well as comparisons with other species with multiple male phenotypes, we can begin to categorize L. dalli males as either bourgeois or parasitic, primarily based on their secondary sex characteristics and AGS contents.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • V.C. Almada E.J. Gonçalves A.J. Santos C. Baptista (1994) ArticleTitleBreeding ecology and nest aggregations in a population of Salaria pavo (Pisces: Blenniidae) in an area where nest sites are very scarce J. Fish Biol. 45 819–830

    Google Scholar 

  • V.C. Almada E.J. Gonçalves R.F. Oliveira A.J. Santos (1995) ArticleTitleCourting females: ecological constraints affect sex roles in a natural population of the blenniid fish Salaria pavo Anim. Behav. 49 1125–1127 Occurrence Handle10.1006/anbe.1995.0142

    Article  Google Scholar 

  • S.H. Alonzo M. Taborsky P. Wirtz (2000) ArticleTitleMale alternative reproductive behaviours in a Mediterranean wrasse, Symphodus ocellatus: evidence from otoliths for multiple life-history pathways Evol. Ecol. Res. 2 997–1007

    Google Scholar 

  • S.H. Alonzo R.R. Warner (2000) ArticleTitleDynamic games and field experiments examining intra- and intersexual conflict: explaining counterintuitive mating behavior in a Mediterranean wrasse, Symphodus ocellatus Behav. Ecol. 11 56–70 Occurrence Handle10.1093/beheco/11.1.56

    Article  Google Scholar 

  • J.C. Avise D.Y. Shapiro (1986) ArticleTitleEvaluating kinship of newly settled juveniles within social groups of the coral reef fish Anthias squamipinnis Evolution 40 1051–1059

    Google Scholar 

  • A.H. Bass (1992) ArticleTitleDimorphic male brains and alternative reproductive tactics in a vocalizing fish Trends Neurosci. 15 139–145 Occurrence Handle10.1016/0166-2236(92)90356-D Occurrence Handle1:STN:280:DyaK383mtlGntw%3D%3D Occurrence Handle1374972

    Article  CAS  PubMed  Google Scholar 

  • A.H. Bass M.A. Marchaterre (1989) ArticleTitleSound-generating (sonic) motor system in a teleost fish (Porichthys notatus): sexual polymorphism in the ultrastructure of myofibrils J. Compar. Neurol. 286 141–153 Occurrence Handle10.1002/cne.902860202 Occurrence Handle1:STN:280:DyaK3c%2FgvFCmtw%3D%3D

    Article  CAS  Google Scholar 

  • A. Barni C. Mazzoldi M.B. Rasotto (2001) ArticleTitleReproductive apparatus and male accessory structures in two batrachoid species (Teleostei, Batrachoididae) J. Fish Biol. 58 1557–1569

    Google Scholar 

  • Behrents, K.C. 1983. The comparative ecology and interactions between two sympatric gobies (Lythrypnus dalli and Lythrypnus zebra). Ph.D. dissertation. Los Angeles: University of Southern California.

  • K.C. Behrents (1987) ArticleTitleThe influence of shelter availability on recruitment and early juvenile survivorship of Lythrypnus dalli Gilbert (Pisces: Gobiidae) J. Exp. Mar. Biol. Ecol. 107 45–59 Occurrence Handle10.1016/0022-0981(87)90122-5

    Article  Google Scholar 

  • S.L. Carlisle S.K. Marxer-Miller A.V.M. Canario R.F. Oliveira L. Carneiro M.S. Grober (2000) ArticleTitleEffects of 11-ketotestosterone on genital papilla morphology in the sex changing fish Lythrypnus dalli J. Fish Biol. 57 445–456 Occurrence Handle10.1006/jfbi.2000.1320 Occurrence Handle1:CAS:528:DC%2BD3cXms1eisb4%3D

    Article  CAS  Google Scholar 

  • K.S. Cole D.R. Robertson (1988) ArticleTitleProtogyny in the Caribbean reef goby, Coryphopterus personatus: gonad ontogeny and social influences on sex-change Bull. Mar. Sci. 42 317–333

    Google Scholar 

  • K.S. Cole D.F. Hoese (2001) ArticleTitleGonad morphology, colony demography and evidence for hermaphroditism in Gobidon okinawae (Teleostei, Gobiidae) Environ. Biol. Fish. 61 161–173 Occurrence Handle10.1023/A:1011032228716

    Article  Google Scholar 

  • W.J. Dominey (1980) ArticleTitleFemale mimicry in male bluegill sunfish–a genetic polymorphism Nature 284 546–548 Occurrence Handle10.1038/284546a0

    Article  Google Scholar 

  • L. Fishelson (1989) ArticleTitleBisexuality and pedogenesis in gobies (Gobiidae: Teleostei) and other fish, or, Why so many little fish in the tropical seas Senckenbergiana maritima 20 147–169

    Google Scholar 

  • L. Fishelson (1991) ArticleTitleComparative cytology and morphology of seminal vesicles in male gobiid fishes Jpn. J. Ichthyol. 38 17–30

    Google Scholar 

  • G.E. Forrester (1999) ArticleTitleThe influence of adult density on larval settlement in a coral reef fish, Coryphopterus glaucofraenum Coral Reefs 18 85–89 Occurrence Handle10.1007/s003380050159

    Article  Google Scholar 

  • M.J. Gage P. Stockley G.A. Parker (1995) ArticleTitleEffects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations Philos.Trans. Roy. Soc. Lond. B 350 391–399

    Google Scholar 

  • M.T. Ghiselin (1969) ArticleTitleThe evolution of hermaphroditism among animals Quart. Rev. Biol. 44 189–208 Occurrence Handle10.1086/406066 Occurrence Handle1:STN:280:DyaE3c%2Fkt1Cjtg%3D%3D Occurrence Handle4901396

    Article  CAS  PubMed  Google Scholar 

  • M.S. Grober (1998) ArticleTitleSocially controlled sex change: integrating ultimate and proximate levels of analysis Acta Ethol. 1–2 3–17

    Google Scholar 

  • M.R. Gross (1991) ArticleTitleEvolution of alternative reproductive strategies: frequency-dependent sexual selection in male bluegill Philos. Trans. Roy. Soc. Lond. B 332 59–66

    Google Scholar 

  • M.R. Gross E.L. Charnov (1980) ArticleTitleAlternative male life histories in bluegill sunfish Procs. Nat. Acad. Sci. USA 77 6937–6940

    Google Scholar 

  • K.B. Hartney K.A. Grorud (2002) ArticleTitleThe effect of sea urchins as biogenic structures on the local abundance of a temperate reef fish Oecologia 131 506–513 Occurrence Handle10.1007/s00442-002-0908-6

    Article  Google Scholar 

  • F. Lahnsteiner M. Seiwald R.A. Patzner E.A. Ferrero (1992) ArticleTitleThe seminal vesicles of the male grass goby, Zosterisessor ophiocephalus (Teleostei, Gobiidae), fine structure and histochemistry Zoomorphology 111 239–248

    Google Scholar 

  • B. Leach R. Montgomerie (2000) ArticleTitleSperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus) Behav. Ecol. Sociobiol. 49 31–37 Occurrence Handle10.1007/s002650000268

    Article  Google Scholar 

  • C. Mazzoldi M. Scaggiante E. Ambrosin M.B. Rasotto (2000) ArticleTitleMating system and alternative male mating tactics in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae) Mar. Biol. 137 1041–1048 Occurrence Handle10.1007/s002270000417

    Article  Google Scholar 

  • P.J. Miller (1984) The tokology of gobioid fishes G.W. Potts R. J. Wootton (Eds) Fish Reproduction: Strategies and Tactics Academic Press London 119–153

    Google Scholar 

  • D.J. Miller R.N. Lea (1972) Guide to the Coastal Marine Fishes of California Fish Bulletin No. 157. California Department of Fish and Game Sacramento California 187

    Google Scholar 

  • R.F. Oliveira L.A. Carneiro D.M. Gonçalves A.V.M. Canario M.S. Grober (2001) ArticleTitle11-ketotestosterone inhibits the alternative mating tactic in sneaker males of the peacock blenny, Salaria pavo Brain, Behav. Ecol. 58 28–37 Occurrence Handle1:STN:280:DC%2BD38%2FntFOrsg%3D%3D

    CAS  Google Scholar 

  • G.A. Parker (1970) ArticleTitleSperm competition and its evolutionary consequences in the insects Biol. Rev. 45 525–567

    Google Scholar 

  • G.A. Parker (1982) ArticleTitleWhy are there so many tiny sperm Sperm competition and the maintenance of two sexes J. Theoret. Biol. 96 281–294 Occurrence Handle10.1016/0022-5193(82)90225-9 Occurrence Handle1:STN:280:DyaL3s%2FhtFCmtQ%3D%3D

    Article  CAS  Google Scholar 

  • G. A. Parker (1990) ArticleTitleSperm competition games: sneaks and extra-pair copulations Proc. Roy. Soc. Lond. B 242 127–133

    Google Scholar 

  • R.H. Reavis M.S. Grober (1999) ArticleTitleAn integrative approach to sex change: social, behavioural and neurochemical changes in Lythrypnus dalli (Pisces) Acta Ethol. 2 51–60

    Google Scholar 

  • F. Ruchon T. Laugier J.P. Quignard (1995) ArticleTitleAlternative male reproductive strategies in the peacock blenny J. Fish Biol. 47 826–840

    Google Scholar 

  • M. J. Ryan D. K. Hews W. E. Wagner Jr (1990) ArticleTitleSexual selection on alleles that determine body size in the swordtail Xiphophorus nigrensis Behav. Ecol. Sociobiol. 26 231–237 Occurrence Handle10.1007/BF00178316

    Article  Google Scholar 

  • M.J. Ryan C.M. Pease M.R. Morris (1992) ArticleTitleA genetic polymorphism in the swordtail Xiphophorus nigrensis: testing the prediction of equal fitness Am. Nat. 139 21–32 Occurrence Handle10.1086/285311

    Article  Google Scholar 

  • M.J. Ryan G.G. Rosenthal (2001) Variation and selection in swordtails L.A. Dugatkin (Eds) Fish, Amphibian, & Reptile Model Systems Princeton University Press New Jersey 133–148

    Google Scholar 

  • Y. Sadovy D.Y. Shapiro (1987) ArticleTitleCriteria for the diagnosis of hermaphroditism in fishes Copeia 1987 136–156

    Google Scholar 

  • M. Scaggiante C. Mazzoldi C.W. Petersen M. Rasotto (1999) ArticleTitleSperm competition and mode of fertilization in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae) J. Exp. Zool. 283 81–90 Occurrence Handle10.1002/(SICI)1097-010X(19990101)283:1<81::AID-JEZ9>3.0.CO;2-9

    Article  Google Scholar 

  • M.P. Schreibman K.D. Kallman (1977) ArticleTitleThe genetic control of the pituitary-gonadal axis in the platyfish, Xiphophorus maculatus J. Exp. Zool. 200 277–294 Occurrence Handle1:STN:280:DyaE2s7ovFGjug%3D%3D Occurrence Handle864425

    CAS  PubMed  Google Scholar 

  • D.Y. Shapiro (1981) ArticleTitleSize, maturation and the social control of sex reversal in the coral reef fish Anthias squamipinnis J. Zool. Lond. 193 105–128 Occurrence Handle10.1111/j.1469-7998.1981.tb01494.x

    Article  Google Scholar 

  • D. Y. Shapiro (1984) Sex reversal and sociodemographic processes in coral reef fishes G.W. Potts R.J. Wootton (Eds) Fish Reproduction: Strategies and Tactics Academic Press London 103–118

    Google Scholar 

  • T. Soljan (1930) ArticleTitleNestbau eines adriatischen Lippfisches Zeitschrift fur Morphologie Okologie der Tiere 17 145–153 Occurrence Handle10.1007/BF00406256

    Article  Google Scholar 

  • M.A. Steele (1996) ArticleTitleEffects of predators on reef fishes: separating cage artifacts from effects of predation J. Exp. Mar. Biol. Ecol. 198 249–267 Occurrence Handle10.1016/0022-0981(96)00011-1

    Article  Google Scholar 

  • M.A. Steele (1997) ArticleTitleThe relative importance of processes affecting recruitment of two temperate reef fishes Ecology 78 129–145

    Google Scholar 

  • C.M. St. Mary (1993) ArticleTitleNovel sexual patterns in two simultaneously hermaphroditic gobies, Lythrypnus dalli and Lythrypnus zebra Copeia 4 1062–1072

    Google Scholar 

  • C.M. St. Mary (1994) ArticleTitleSex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavior gender and the consequences for reproduction Behav. Ecol. 5 304–313

    Google Scholar 

  • C.M. St. Mary (1997) ArticleTitleSequential patterns of sex allocation in simultaneous hermaphrodites: do we need models that specifically incorporate this complexity Am. Nat. 150 73–97 Occurrence Handle10.1086/286057 Occurrence Handle1:STN:280:DC%2BD1cnit1OmtQ%3D%3D

    Article  CAS  Google Scholar 

  • P. Stockley M.J. Gage G.A. Parker A.P. Møller (1997) ArticleTitleSperm competition in fishes: the evolution of testis size and ejaculate characteristics Am. Nat. 149 933–954 Occurrence Handle10.1086/286031 Occurrence Handle1:STN:280:DC%2BD1cnit1OgtQ%3D%3D

    Article  CAS  Google Scholar 

  • M. Taborksy (1994) ArticleTitleSneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction Advan. Study Behav. 23 1–100 Occurrence Handle10.1016/S0065-3454(08)60351-4

    Article  Google Scholar 

  • M. Taborsky (2001) ArticleTitleThe evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes J. Heredity 92 100–110 Occurrence Handle10.1093/jhered/92.2.100 Occurrence Handle1:STN:280:DC%2BD38%2Fht1Wksw%3D%3D

    Article  CAS  Google Scholar 

  • M. Taborsky B. Hudde P. Wirtz (1987) ArticleTitleReproductive behaviour and ecology of Symphodus crenilabrus ocellatus, a European wrasse with four types of male behaviour Behaviour 102 82–118

    Google Scholar 

  • E. van den Berghe F. Wernerus R. R. Warner (1989) ArticleTitleFemale choice and the mating cost of peripheral males Ani. Behav. 38 875–884

    Google Scholar 

  • R.R. Warner (1975) ArticleTitleThe adaptive significance of sequential hermaphroditism in animals Am. Nat. 109 61–82 Occurrence Handle10.1086/282974

    Article  Google Scholar 

  • R.R. Warner (1984) ArticleTitleMating behavior and hermaphroditism in coral reef fishes Am. Scientist 72 128–136

    Google Scholar 

  • R.R. Warner (1988) ArticleTitleSex change and the size-advantage model Trends Ecol. Evol. 3 133–136 Occurrence Handle10.1016/0169-5347(88)90176-0

    Article  Google Scholar 

  • R.R. Warner D.R. Robertson (1978) ArticleTitleSexual patterns in the labroid fishes of the western Caribbean, I: the wrasses (Labridae) Smithsonian Contribut. Zool. 255 1–27

    Google Scholar 

  • R.R. Warner S.E. Swearer (1991) ArticleTitleSocial control of sex change in the bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae) Biol. Bull. 181 199–204

    Google Scholar 

  • R.R. Warner D.Y. Shapiro A. Marcanato C.W. Petersen (1995) ArticleTitleSexual conflict: males with highest mating success convey the lowest fertilization benefits to females Proc. Roy Soc. Lond. B 262 135–139 Occurrence Handle1:STN:280:DyaK28%2Fpt1Smtw%3D%3D

    CAS  Google Scholar 

  • J.W. Wiley (1976) ArticleTitleLife histories and systematics of the western North American gobies Lythrypnus dalli (Gilbert) and Lythrypnus zebra (Gilbert) San Diego Soc. Nat. Hist.: Trans. Mem. 18 169–184

    Google Scholar 

  • J. Wilson C.W. Osenberg (2002) ArticleTitleExperimental and observational patterns of density-dependent settlement and survival in the marine fish Gobiosoma Oecologia 130 205–215

    Google Scholar 

  • J. H. Zar (1996) Biostatistical Analysis, 3rd edn Prentice Hall Inc. New Jersey 226

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthew S. Grober.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Drilling, C.C., Grober, M.S. An initial description of alternative male reproductive phenotypes in the bluebanded goby, Lythrypnus dalli (Teleostei, Gobiidae). Environ Biol Fish 72, 361–372 (2005). https://doi.org/10.1007/s10641-004-2590-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-004-2590-5

Keywords

Navigation