Advertisement

The goby Lythrypnus pulchellus is a bi-directional sex changer

  • Sayuri Muñoz-Arroyo
  • Carmen Rodríguez-Jaramillo
  • Eduardo F. BalartEmail author
Article

Abstract

Sex change in both directions is a novelty reported in some species of fishes belonging to seven families associated to reefs. This study demonstrated that Lythrypnus pulchellus, a small cryptobenthic haremic reef fish, is a bi-directional sex changer, at least in experimental conditions. The influence of body size in duration and direction of sex reversal was tested, and the changes of sexual dimorphic traits (elongated anterior dorsal spine, genital papillae, body size) and sex-cell allocation in the gonad during sex change were described. Unisex pairs of individuals, male-male and female-female of similar and different body size, were housed in aquaria recording the changes until spawning. Sex change duration showed no significant differences between protogyny (11 days) and protandry (12 days), regardless of their size. Among pairs of males of different size, the smaller individual changes sex to female whilst among pairs of females of different size larger individuals change sex to male. Among pairs of males of similar size, dominant individuals remained as male whilst subordinate individual did change sex to female. If the pair of similar size were females, the dominant individual changed sex to male whilst the subordinate remained as female. The gonads, before, throughout, and after sex change, showed that females and males contained both ovarian and testicular tissues in different ratios. The length/width ratio of the genital papilla probed to be useful to predict functional sex of individuals. The results support the idea that extreme sexual plasticity is a widespread reproductive trait in the genus Lythrypnus.

Keywords

Fishes Bi-directional sex change Sexual plasticity Size-advantage model Sex-cell allocation Gonad structure 

Notes

Acknowledgements

The authors are grateful to two anonymous referees for their valuable comments improving this manuscript; Enrique Calvillo, Jorge Angulo, Mario Cota and Andrés González for assistance in field work at the culture farm. Pablo Monsalvo, Gabriel Robles, Miguel Trujillo García, and Jorge Cobos for helping in fish aquaria maintenance throughout the study; María E. Meza Chávez for assistance in histological analysis; Claudia J. Pérez Estrada for laboratory and photography support and Noemí Bocanegra Castillo for laboratory assistance; Diana Fischer for editorial services in English. This research was partially funded by Centro de Investigaciones Biológicas del Noroeste (CIBNOR) project PEP. Sayuri Muñoz-Arroyo was a recipient of a CONACYT (351061) student fellowship.

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10641_2019_913_Fig10_ESM.png (3.6 mb)
Fig. S1

Cross-section of gonads of Lythrypnus pulchellus. (a, b) Focal fish that reallocated from male-to-female function; (c, d) focal fish that reallocated from female-to-male function; (e) AGS, accessory gonadal structure with abundant number of spermatozoids. Abbreviations: O, ovary; T, testis; EP, early perinucleolar oocyte; LP, late perinucleolar oocyte; CA, cortical alveoli oocyte; LI, lipid inclusions; MO, mature oocyte; sg, spermatogonia; spt, spermatids; spc1, primary and spc2, secondary spermatocytes; sz, spermatozoa (PNG 3664 kb)

10641_2019_913_MOESM1_ESM.tif (55.6 mb)
High resolution image (TIF 56967 kb)
10641_2019_913_Fig11_ESM.png (1.4 mb)
Fig. S2

Gonad structure of male individuals of Lythrypnus pulchellus showing spermatic tissue at the dorsal and ventral poles (a, b, c, d). Abbreviations: G, gut; AGS, accessory gonadal structure; s, spermatic tissue (PNG 1425 kb)

10641_2019_913_MOESM2_ESM.tif (20.5 mb)
High resolution image (TIF 20942 kb)

References

  1. Aho KA (2013) Foundational and applied statistics for biologists using R. Chapman and Hall, Idaho, USAGoogle Scholar
  2. Allen GR, Robertson DR (1994) Fishes of the tropical eastern Pacific. University of Hawaii Press, HonoluluGoogle Scholar
  3. Archambeault S, Cerino D, Solomon-Lane T, Grober M (2015) Reproduction, larviculture and early development of the Bluebanded goby, Lythrypnus dalli, an emerging model organism for studies in evolutionary developmental biology and sexual plasticity. Aquac Res 1–15.  https://doi.org/10.1111/are.12648
  4. Balart EF, González-Cabello A, Romero-Ponce RC, Zayas-Alvarez A, Calderón-Parra M, Campos-Dávila L, Findley LT (2006) Length–weight relationships of cryptic reef fishes from the southwestern Gulf of California, México. J Appl Ichthyol 22:316–318.  https://doi.org/10.1111/j.1439-0426.2006.00670.x CrossRefGoogle Scholar
  5. Behrents KC (1983) The comparative ecology and interactions between two sympatric gobies (Lythrypnus dalli and Lythrypnus zebra). University of Southern California, PhD dissertationGoogle Scholar
  6. Black MP, Moore B, Canario AVM, Ford D, Reavis RH, Grober MS (2005) Reproduction in context: field testing a lab model of socially controlled sex change in Lythrypnus dalli (Gilbert). J Exp Mar Biol Ecol 318:127–143.  https://doi.org/10.1016/j.jembe.2004.12.015 CrossRefGoogle Scholar
  7. Black MP, Balthazart J, Baillien M, Grober MS (2011) Rapid increase in aggressive behavior precedes the decrease in brain aromatase activity during socially mediated sex change in Lythrypnus dalli. Gen Comp Endocrinol 170:119–124.  https://doi.org/10.1016/j.ygcen.2010.09.019 CrossRefGoogle Scholar
  8. Carlisle SL, Marxer-Miller SK, Canario AVM, Oliveira RF, Carneiro L, Grober MS (2000) Effects of 11-ketotestosterone on genital papilla morphology in the sex changing fish Lythrypnus dalli. J Fish Biol 57:445–456.  https://doi.org/10.1111/j.1095-8649.2000.tb02183.x CrossRefGoogle Scholar
  9. Cole KS (1990) Patterns of gonad structure in hermaphroditic gobies (Teleostei: Gobiidae). Environ Biol Fish 28:125–142.  https://doi.org/10.1007/BF00751032
  10. Cole KS (2010) Gonad morphology in hermaphroditic gobies. In: Cole KS (ed) Reproduction and sexuality in marine fishes. University of California Press, Berkeley, pp 117–162Google Scholar
  11. Cole KS, Robertson DR (1988) Protogyny in the Caribbean reef goby, Coryphopterus personatus: gonad ontogeny and social influences on sex-change. Bull Mar Sci 42:317–333Google Scholar
  12. Del Moral-Flores LF, González-Acosta AF, Espinosa-Pérez H, Ruiz-Campos G, Castro-Aguirre JL (2013) Annotated checklist of the ichthyofauna from the islands of the Gulf of California, with comments on its zoogeographic affinities Rev Mex Biodivers 84:184–214  https://doi.org/10.7550/rmb.27335
  13. Drilling CC, Grober MS (2005) An initial description of alternative male reproductive phenotypes in the bluebanded goby, Lythrypnus dalli (Teleostei, Gobiidae). Environ Biol Fish 72(4):361–372.  https://doi.org/10.1007/s10641-004-2590-5 CrossRefGoogle Scholar
  14. Findley L, Van Tassell J (2010) Lythrypnus pulchellus. The IUCN red list of threatened species 2010: e.T183335A8095707.  https://doi.org/10.2305/IUCN.UK.2010-3.RLTS.T183335A8095707.en
  15. Fukuda K, Tanazawa T, Sunobe T (2017) Polygynous mating mystem and field evidence for bidirectional sex change in the gobiid fish Trimma grammistes. Int J Pure Appl Zool 5:92–99Google Scholar
  16. Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208.  https://doi.org/10.1086/406066 CrossRefGoogle Scholar
  17. Ginsburg I (1938) Eight new species of gobioid fishes from the American Pacific coast. Allan Hancock Pacific Exped 2:109–121Google Scholar
  18. Grober MS, Sunobe T (1996) Serial adult sex change involves rapid and reversible changes in forebrain neurochemistry. Neuroreport 7:2945–2949.  https://doi.org/10.1097/00001756-199611250-00029 CrossRefGoogle Scholar
  19. Hartney KB (1989) The foraging ecology of two sympatric gobiid fishes: importance of behavior in prey type selection. Environ Biol Fish 26:105–118.  https://doi.org/10.1007/BF00001027 CrossRefGoogle Scholar
  20. Humanson GL (1979) Animal Tissue Techniques, 4th edn. Freeman WH and Co, San Francisco, CAGoogle Scholar
  21. Kadota T, Osato J, Nagata K, Sakai Y (2012) Reversed sex change in the haremic protogynous hawkfish Cirrhitichthys falco in natural conditions. Ethology 118:226–234.  https://doi.org/10.1111/j.1439-0310.2011.02005.x CrossRefGoogle Scholar
  22. Kobayashi Y, Sunobe T, Kobayashi T, Nagahama Y, Nakamura M (2005) Gonadal structure of the serial-sex changing gobiid fish Trimma okinawae. Devel Growth Diffe 47:7–13.  https://doi.org/10.1111/j.1440-169x.2004.00774.x CrossRefGoogle Scholar
  23. Kobayashi Y, Usami T, Sunobe T, Manabe H, Nagahama Y, Nakamura M (2012) Histological observation of the urogenital papillae in the bidirectional sex-changing gobiid fish, Trimma okinawae. Zool Sci 29(2):121–126.  https://doi.org/10.2108/zsj.29.121 CrossRefGoogle Scholar
  24. Kuwamura T, Nakashima Y (1998) New aspects of sex change among reef fishes: recent studies in Japan. Environ Biol Fish 52:125–135.  https://doi.org/10.1023/A:1007389519702 CrossRefGoogle Scholar
  25. Kuwamura T, Nakashimn Y, Yogo Y (1994) Sex change in either direction by growth-rate advantage in the monogamous coral goby, Paragobiodon echinocephalus. Behav Ecol 5:434–438.  https://doi.org/10.1093/beheco/5.4.434 CrossRefGoogle Scholar
  26. Kuwamura T, Kadota T, Suzuki S (2014) Testing the low-density hypothesis for reversed sex change in polygynous fish: experiments in Labroides dimidiatus. Sci Rep 4:4369.  https://doi.org/10.1038/srep04369 CrossRefGoogle Scholar
  27. Kuwamura T, Kadota T, Suzuki S (2015) Bidirectional sex change in the magenta dottyback Pictichromis porphyrea: first evidence from the field in Pseudochromidae. Environ Biol Fish 98:201–207.  https://doi.org/10.1007/s10641-014-0265-4 CrossRefGoogle Scholar
  28. Kuwamura T, Suzuki S, Kadota T (2016) Male-to-female sex change in widowed males of the protogynous damselfish Dascyllus aruanus. J Ethol 34:85–88.  https://doi.org/10.1007/s10164-015-0450-8 CrossRefGoogle Scholar
  29. Lorenzi V, Earley RL, Grober MS (2006) Preventing behavioural interactions with a male facilitates sex change in female bluebanded gobies, Lythrypnus dalli. Behav Ecol Sociobiol 59:715–722.  https://doi.org/10.1007/s00265-005-0101-0 CrossRefGoogle Scholar
  30. Lorenzi V, Carpenter RE, Summers CH, Earley RL, Grober MS (2009) Serotonin, social status and sex change in the bluebanded goby Lythrypnus dalli. Physiol Behav 97:476–483.  https://doi.org/10.1016/j.physbeh.2009.03.026 CrossRefGoogle Scholar
  31. Lorenzi V, Earley RL, Grober MS (2012) Differential responses of brain, gonad and muscle steroid levels to changes in social status and sex in a sequential and bidirectional hermaphroditic fish. PLoS One 7:e51158.  https://doi.org/10.1371/journal.pone.0051158 CrossRefGoogle Scholar
  32. Lutnesky M (1996) Size-dependent rate of protogynous sex change in pomacanthid angelfish, Centropyge potteri. Copeia 1:209–212CrossRefGoogle Scholar
  33. Manabe H, Ishimura M, Shinomiya A, Sunobe T (2007a) Field evidence for bi-directional sex change in the polygynous gobiid fish Trimma okinawae. J Fish Biol 70:600–609.  https://doi.org/10.1111/j.1095-8649.2007.01338.x CrossRefGoogle Scholar
  34. Manabe H, Ishimura M, Shinomiya A, Sunobe T (2007b) Inter-group movement of females of the polygynous gobiid fish Trimma okinawae in relation to timing of protogynous sex change. J Ethol 25:133–137.  https://doi.org/10.1007/s10164-006-0007-y CrossRefGoogle Scholar
  35. Manabe H, Matsuoka M, Goto K, Dewa S, Shinomiya A, Sakurai M, Sunobe T (2008) Bi-directional sex change in the gobiid fish Trimma sp.: does size-advantage exist? Behaviour 145:99–113.  https://doi.org/10.1163/156853908782687214 CrossRefGoogle Scholar
  36. Manabe H, Toyoda K, Nagamoto K, Dewa SI, Sakurai M, Hagiwara K, Shinomiya A, Sunobe T (2013) Bidirectional sex change in seven species of Priolepis (Actinopterygii: Gobiidae). B Mar Sci 89:635–642.  https://doi.org/10.5343/bms.2012.1050 CrossRefGoogle Scholar
  37. Maxfield JM, Van Tassell JL, St. Mary CM, Joyeux JC, Crow KD (2012) Extreme gender flexibility: using a phylogenetic framework to infer the evolution of variation in sex allocation, phylogeography, and speciation in a genus of bidirectional sex changing fishes (Lythrypnus, Gobiidae). Mol Phylogenet Evol 64:416–427.  https://doi.org/10.1016/j.ympev.2012.04.016 CrossRefGoogle Scholar
  38. Munday PL (2002) Bi-directional sex change: testing the growth-rate advantage model. Behav Ecol Sociobiol 52:247–254.  https://doi.org/10.1007/s00265-002-0517-8 CrossRefGoogle Scholar
  39. Munday PL, Caley MJ, Jones GP (1998) Bi-directional sex change in a coral-dwelling goby. Behav Ecol Sociobiol 43:371–377.  https://doi.org/10.1007/s002650050504 CrossRefGoogle Scholar
  40. Munday PL, Buston PM, Warner RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21:89–95.  https://doi.org/10.1016/j.tree.2005.10.020 CrossRefGoogle Scholar
  41. Munday PL, Kuwamura T, Kroon FJ (2010) Bidirectional sex change in marine fishes. In: Cole KS (ed) Reproduction and sexuality in marine fishes: patterns and processes. University of California Press, Berkeley, pp 241–271Google Scholar
  42. Muñoz RC, Warner RR (2003) A new version of the size-advantage hypothesis for sex change: incorporating sperm competition and size-fecundity skew. Am Nat 161:749–761.  https://doi.org/10.1086/374345 CrossRefGoogle Scholar
  43. Muñoz RC, Warner RR (2004) Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians. Behav Ecol 15:129–136.  https://doi.org/10.1093/beheco/arg086 CrossRefGoogle Scholar
  44. Nakashima Y, Kuwamura T, Yogo Y (1995) Why be a both-ways sex changer. Ethology 101:301–307.  https://doi.org/10.1111/j.1439-0310.1995.tb00367.x CrossRefGoogle Scholar
  45. Nakashima Y, Kuwamura T, Yogo Y (1996) Both-ways sex change in monogamous coral gobies, Gobiodon spp. Environ Biol Fish 46:281–288.  https://doi.org/10.1007/BF00005004 CrossRefGoogle Scholar
  46. Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world. John Wiley and Songs, Hoboken, New JerseyCrossRefGoogle Scholar
  47. Orians GH (1969) On the evolution of mating mystems in birds and mammals. Am Nat 103:589–603.  https://doi.org/10.1086/282628 CrossRefGoogle Scholar
  48. Pradhan DS, Willis MC, Solomon-Lane TK, Thonkulpitak K, Grober MS (2015) Simultaneous courtship and parenting in males and sex role reversal in females of the haremic bluebanded goby, Lythrypnus dalli. Behaviour 152:917–940.  https://doi.org/10.1163/1568539X-00003262 CrossRefGoogle Scholar
  49. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org
  50. Reavis R, Grober MS (1999) An integrative approach to sex change: social, behavioral and neurochemical changes in Lythrypnus dalli (Pisces). Acta Ethol 2:51–60.  https://doi.org/10.1007/PL00012232 CrossRefGoogle Scholar
  51. Robertson DR, Allen GR (2017) Shorefishes of the tropical eastern Pacific online information system. Version 2.0. Smithsonian Tropical Research Institute, Balboa, PanamaGoogle Scholar
  52. Rodgers EW, Drane S, Matthew SG (2005) Sex reversal in pairs of Lythrypnus dalli: behavioral and morphological changes. Biol Bull 208:120–126.  https://doi.org/10.2307/3593120 CrossRefGoogle Scholar
  53. Rodgers EW, Earley RL, Grober MS (2007) Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. J Fish Biol 70:1660–1668.  https://doi.org/10.1111/j.1095-8649.2007.01427.x CrossRefGoogle Scholar
  54. Sadovy de Mitchenson Y, Liu M (2008) Functional hermaphroditism in teleosts. Fish Fish 9:1–43.  https://doi.org/10.1111/j.1467-2979.2007.00266.x CrossRefGoogle Scholar
  55. Sakurai M, Nakakoji S, Manabe H, Dew S, Shinomiya A, Sunobe T (2009) Bidirectional sex change and gonad structure in the gobiid fish Trimma yanagitai. Ichthyol Res 56:82–86.  https://doi.org/10.1007/s10228-008-0054-1 CrossRefGoogle Scholar
  56. Sheenan DC, Hrapchak BB (1980) Theory and practice of histotechnology. Mosby Co, St. LouisGoogle Scholar
  57. Shiobara Y (2000) Reproduction and hermaphroditism of the gobiid fish, Trimma grammistes, from Suruga Bay, Central Japan. Sci Rep Mus Tokai Univ 2:19–30Google Scholar
  58. Solomon-Lane TK, Crespi EJ, Grober MS (2013) Stress and serial adult metamorphosis: multiple roles for the stress axis in socially regulated sex change. Front Neurosci 7:1–12.  https://doi.org/10.3389/fnins.2013.00210 CrossRefGoogle Scholar
  59. Solomon-Lane TK, Pradhan DS, Willis MC, Grober MS (2014) Female, but not male, agonistic behaviour is associated with male reproductive success in stable Bluebanded Goby (Lythrypnus dalli) hierarchies. Behaviour 151:1367–1387.  https://doi.org/10.1163/1568539X-00003188 CrossRefGoogle Scholar
  60. St. Mary CM (1993) Novel sexual patterns in two simultaneously hermaphroditic gobies, Lythrypnus dalli and Lythrypnus zebra. Copeia 1993:1062–1107.  https://doi.org/10.2307/1447085 CrossRefGoogle Scholar
  61. St. Mary CM (1994) 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. Behav Ecol 5:304–313.  https://doi.org/10.1093/beheco/5.3.304 CrossRefGoogle Scholar
  62. St. Mary CM (1996) Sex allocation in a simultaneous hermaphrodite, the zebra goby Lythrypnus zebra: insights gained through a comparison with its sympatric congener, Lythrypnus dalli. Environ Biol Fish 45:177–190.  https://doi.org/10.1007/BF00005232 CrossRefGoogle Scholar
  63. St. Mary CM (1998) Characteristic gonad structure in the Gobiid genus Lythrypnus with comparisons to other hermaphroditic gobies. Copeia 3:720–724.  https://doi.org/10.2307/1447803 CrossRefGoogle Scholar
  64. St. Mary CM (2000) Sex allocation in Lythrypnus (Gobiidae): variations on a hermaphroditic theme. Environ Biol Fish 58:321–333.  https://doi.org/10.1023/A:1007644010331 CrossRefGoogle Scholar
  65. Steele MA (1997) The relative importance of processes affecting recruitment of two temperate reef fishes. Ecology 78:129–145.  https://doi.org/10.2307/2265984 CrossRefGoogle Scholar
  66. Steele MA (1998) The relative importance of predation and competition in two reef fishes. Oecologia 115:222–232.  https://doi.org/10.1007/s004420050511 CrossRefGoogle Scholar
  67. Sunobe T, Nakazono A (1993) Sex change in both directions by alteration of social dominance in Trimma okinawae (Pisces: Gobiidae). Ethology 94:339–345.  https://doi.org/10.1111/j.1439-0310.1993.tb00450.x CrossRefGoogle Scholar
  68. Thacker C (2011) Systematics of Gobiidae. In: Patzner RA, Van Tassell JL, Kovacic M, Kapoor BG (eds) The biology of gobies. CRC Press, Taylor and Francis Group, pp 129–136CrossRefGoogle Scholar
  69. Van Tassell JL (2011) Gobiiformes of the Americas. In: Patzner RA, Van Tassell JL, Kovacic M, Kapoor BG (eds) The biology of gobies. CRC Press, Taylor and Francis Group, pp 139–696CrossRefGoogle Scholar
  70. Warner RR (1975) The adaptive significance of sequential hermaphroditism in animals. Am Nat 109:61–82.  https://doi.org/10.1086/282974 CrossRefGoogle Scholar
  71. Warner RR (1988) Sex change and the size-advantage model. Trends Ecol Evol 3:133–136.  https://doi.org/10.1016/0169-5347(88)90176-0 CrossRefGoogle Scholar
  72. Wiley JW (1976) Life histories and systematics of the western North American gobies L. dalli (Gilbert) and L. zebra (Gilbert). San Diego. Soc Nat Hist 18:169–184Google Scholar
  73. Yamaguchi S, Iwasa Y (2017) Advantage for the sex changer who retains the gonad of the nonfunctional sex. Behav Ecol Sociobiol 71:39.  https://doi.org/10.1007/s00265-017-2269-5 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Universidad Autónoma de Baja California SurLa PazMexico
  2. 2.Centro de Investigaciones Biológicas del Noroeste, S.C. (CIBNOR)La PazMexico

Personalised recommendations