Comparative analysis of multiple paternity in different populations of viviparous black rockfish, Sebastes schlegelii, a fish with long-term female sperm storage

  • Tianxiang Gao
  • Kui Ding
  • Na Song
  • Xiumei Zhang
  • Zhiqiang Han
Original Paper


The black rockfish (Sebastes schlegelii) has a viviparous reproductive pattern and long-term sperm storage. Multiple paternity is frequently reported in this species. Six polymorphic microsatellite markers were applied to genotype 23 pregnant females (11 wild and 12 cultured) and 645 of their embryos, which were collected from the coast of the Shandong Peninsula in China. The number of sires and the quantity of paternal contributions for each brood were estimated. The results of a cultured group from Japan were reanalysed for comparison and illustration as a quoted group. Multiple paternity was detected in 10 (90.9%) of 11 broods in the wild group, 11 (91.7%) of 12 broods in the cultured group, and eight (88.9%) of nine broods in the quoted group. The number of sires in the cultured group appears to be significantly larger than that of the quoted group (P = 0.030), but the difference between the wild and the cultured groups was not significant (P = 0.219) nor was that between the wild and the quoted groups (P = 0.146). Additionally, in the 29 multiply sired broods, 22 broods were significantly skewed from equal paternal contributions, indicating that sperm competition and cryptic female choice might play key roles in the post-copulatory paternity biasing of this species. Furthermore, within the quoted data, the male was distinctly older than the female in 16 of 18 (88.9%) copulation pairs, demonstrating that females are apt at selecting older males to mate with. These results may provide some guidance or knowledge for artificial breeding, the evolutionary mechanism of polyandry, and sexual selection in black rockfish.


Black rockfish Multiple paternity Sperm competition Cryptic female choice 



We thank Dr. Li Ning for valuable reviews of previous versions of this manuscript. We also thank Mr. Yan Long, Zhou Wei, Shan Binbin, Ding Pengwei and others for handling our samples. Additionally, we thank shipmaster Liu for collecting samples in the offshore waters of Jiaonan. This study was supported by the National Natural Science Foundation of China (31172447) and the Public Science and Technology Research Funds Projects of Ocean (201305043, 201405010).

The collection of gravid wild females of S. schlegelii from the offshore waters of Jiaonan and Rushan was permitted by Chengxian Song and Yuchen Liu, managers of Jiaonan Tianyuan Aquatic CO. Ltd. and Rushan Chenyu Aquatic CO. Ltd., respectively. In addition, the collection of twelve gravid cultured females was permitted by Xuze Zhang, manager of Penglai Hongyu Aquatic Products CO., Ltd. Ethical approval was not applicable for this study because no endangered animals were involved. However, all handling of fish was conducted in strict accordance with the standards of Animal Care Quality Assurance in China.


  1. An HS, Park JY, Kim MJ, Lee EY, Kim KK (2009) Isolation and characterization of microsatellite markers for the heavily exploited rockfish Sebastes schlegeli, and cross-species amplification in four related Sebastes spp. Conserv Genet 10(6):1969–1972. doi: 10.1007/s10592-009-9870-8 CrossRefGoogle Scholar
  2. Barreto FS, Avise JC (2008) Polygynandry and sexual size dimorphism in the sea spider Ammothea hilgendorfi (Pycnogonida: Ammotheidae), a marine arthropod with brood-carrying males. Mol Ecol 17:4164–4175. doi: 10.1111/j.1365-294X.2008.03895.x CrossRefPubMedGoogle Scholar
  3. Bateman PB (1998) Mate preference for novel partners in the cricket Gryllus bimaculatus. Ecol Entomol 23:473–475. doi: 10.1046/j.1365-2311.1998.00156.x CrossRefGoogle Scholar
  4. Birkhead TR, Pizzari T (2002) Postcopulatory sexual selection. Nat Rev Genet 3(4):262–273. doi: 10.1038/nrg774 CrossRefPubMedGoogle Scholar
  5. Boehlert GW, Yamada J (1991) Introduction to the symposium on rockfishes. Environ Biol Fish 11:9–14. doi: 10.1007/978-94-011-3792-8_1 CrossRefGoogle Scholar
  6. Boehlert GW, Kusakari M, Shimizu M (1986) Energetics during embryonic development in kurosoi, Sebastes schlegeli Hilgendorf. J Exp Mar Biol Ecol 101(3):239–256. doi: 10.1016/0022-0981(86)90266-2 CrossRefGoogle Scholar
  7. Boomer JJ, Harcourt RG, Francis MP, Walker TI, Braccini JM, Stow AJ (2013) Frequency of multiple paternity in gummy shark, Mustelus antarcticus, and rig, Mustelus lenticulatus, and the implications of mate encounter rate, postcopulatory influences, and reproductive mode. J Hered 104(3):371–379. doi: 10.1093/jhered/est010 CrossRefPubMedGoogle Scholar
  8. Byrne RJ, Avise JC (2012) Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Mar Biol 159(4):749–756. doi: 10.1007/s00227-011-1851-z CrossRefGoogle Scholar
  9. Clark E, Rabin JS, Holderman S (1988) Reproductive behavior and social organization in the sand tilefish, Malacanthus plumieri. Environ Biol Fish 22(4):273–286. doi: 10.1007/BF00004893 CrossRefGoogle Scholar
  10. Coleman SW, Jones AG (2011) Patterns of multiple paternity and maternity in fishes. Biol J Linn Soc 103(4):735–760. doi: 10.1111/j.1095-8312.2011.01673.x CrossRefGoogle Scholar
  11. Eberhard W (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  12. Evans JP, Simmons LW (2008) The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy- sperm? Genetica 134(1):5–19. doi: 10.1007/s10709-007-9162-5 CrossRefPubMedGoogle Scholar
  13. Fitzpatrick JL, Kempster RM, Daly-Engel TS, Colliin SP, Evans JP (2012) Assessing the potential for post-copulatory sexual selection in elasmobranchs. J Fish Biol 80(5):1141–1158. doi: 10.1111/j.1095-8649.2012.03256.x CrossRefPubMedGoogle Scholar
  14. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425(6959):714–717. doi: 10.1038/nature01969 CrossRefPubMedGoogle Scholar
  15. Fujita H, Kohda M (1996) Male mating effort in the viviparous scorpionfish, Sebastiscus marmoratus. Ichthyol Res 43(3):247–255. doi: 10.1007/BF02347597 CrossRefGoogle Scholar
  16. Gomez-Uchida D (2006) Spatial and temporal scales of genetic change in two overfished rockfishes. [Doctoral dissertation] Oregon State University, CorvallisGoogle Scholar
  17. Gonzalez EB, Murakami T, Teshima Y, Yoshioka K, Jeong DS, Umino T (2009) Paternity testing of wild black rockfish Sebastes inermis (brownish type) from the Seto Inland Sea of Japan. Ichthyol Res 56(1):87–91. doi: 10.1007/s10228-008-0055-0 CrossRefGoogle Scholar
  18. Haskins CP, Haskins EF, McLaughlin JJA, Hewitt RE (1961) Polymorphism and population structure in Lebistes reticulatus, an ecological study. In Vertebrate Speciation ed. Blair WF, pp. 32–395. University Texas Press, AustinGoogle Scholar
  19. Helvey M (1982) First observations of courtship behavior in rockfish, genus Sebastes. Copeia 4:763–770. doi: 10.2307/1444084
  20. Hyde JR, Kimbrell C, Robertson L, Clifford K, Lynn E, Vetter R (2008) Multiple paternity and maintenance of genetic diversity in the live-bearing rockfishes Sebastes spp. Mar Ecol Prog Ser 357:245. doi: 10.3354/meps07296 CrossRefGoogle Scholar
  21. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Cambridge Philos Soc 75(01):21–64CrossRefPubMedGoogle Scholar
  22. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. doi: 10.1111/j.1755-0998.2009.02787.x CrossRefPubMedGoogle Scholar
  23. Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos T R Soc B 361(1466):319–334. doi: 10.1098/rstb.2005.1784 CrossRefGoogle Scholar
  24. Kusakari M (1991) Mariculture of kurosoi, Sebastes schlegeli. Environ Biol Fish 30:245–251. doi: 10.1007/978-94-011-3792-8_22 CrossRefGoogle Scholar
  25. Lee CE, Frost BW (2002) Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480(1–3):111–128. doi: 10.1023/A:1021293203512 CrossRefGoogle Scholar
  26. Liu JX, Avise JC (2011) High degree of multiple paternity in the viviparous shiner perch, Cymatogaster aggregata, a fish with long-term female sperm storage. Mar Biol 158(4):893–901. doi: 10.1007/s00227-010-1616-0 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu JX, Tatarenkov A, Teejay A, Moyle PB, Avise JC (2013) Molecular evidence for multiple paternity in a population of the viviparous tule perch Hysterocarpus traski. J Hered 104(2):217–222. doi: 10.1093/jhered/ess105 CrossRefPubMedGoogle Scholar
  28. Mori H, Nakagawa M, Soyano K, Koya Y (2003) Annual reproductive cycle of black rockfish Sebastes schlegeli in captivity. Fisheries Sci 69(5):910–923. doi: 10.1046/j.1444-2906.2003.00707.x CrossRefGoogle Scholar
  29. Nagasawa T, Domon K (1997) The early life history of kurosoi, Sebastes schlegeli (Scorpaenidae), in the sea of Japan. Ichthyol Res 44(2–3):237–248. doi: 10.1007/BF02678703 CrossRefGoogle Scholar
  30. Nakabō T (2000) Fishes of Japan: with pictorial keys to the species, 2nd edn. Tokai University Press, KanagawakenGoogle Scholar
  31. Nakagawa M (1998) Broodstock management of black rockfish. Annual Report of Japan Sea-Farming Association in 1996 32–33. (In Japanese)Google Scholar
  32. Nakagawa M (1999) Broodstock management of black rockfish. Annual Report of Japan Sea-Farming Association in 1997 34–36. (In Japanese)Google Scholar
  33. Nakagawa M (2000) Broodstock management of black rockfish. Annual Report of Japan Sea-Farming Association in 1998 40–42. (In Japanese)Google Scholar
  34. Nakagawa M (2001) Broodstock management of black rockfish. Annual Report of Japan Sea-Farming Association in 1999 42–44. (In Japanese)Google Scholar
  35. Nakagawa M, Ichikawa T, Maekawa H (2002) Broodstock management of black rockfish. Annual Report of Japan Sea-Farming Association in 2000 38–39. (In Japanese)Google Scholar
  36. Neff BD, Pitcher TE (2002) Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J Fish Biol 61(3):739–750. doi: 10.1111/j.1095-8649.2002.tb00908.x CrossRefGoogle Scholar
  37. Nonacs P (2000) Measuring and using skew in the study of social behavior and evolution. Am Nat 156:577–589. doi: 10.1086/316995 CrossRefGoogle Scholar
  38. Nosal AP, Lewallen EA, Burton RS (2013) Multiple paternity in leopard shark (Triakis semifasciata) litters sampled from a predominantly female aggregation in la Jolla, California, USA. J Exp Mar Biol Ecol 446:110–114. doi: 10.1016/j.jembe.2013.05.002 CrossRefGoogle Scholar
  39. Omoto N, Koya Y, Chin B, Yamashita Y, Nakagawa M, Noda T (2010) Gonadal sex differentiation and effect of rearing temperature on sex ratio in black rockfish (Sebastes schlegeli). Ichthyol Res 57(2):133–138. doi: 10.1007/s10228-009-0137-7 CrossRefGoogle Scholar
  40. Parker GA (1990) Sperm competition games: raffles and roles. Proc Roy Soc Lond B Bio 242(1304):120–126. doi: 10.1098/rspb.1990.0114 CrossRefGoogle Scholar
  41. Parker GA (1992) Snakes and female sexuality. Nature 355(6359):395–396. doi: 10.1038/355395a0 CrossRefGoogle Scholar
  42. Sambrook J, Russell David W (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  43. Shinomiya A, Ezaki O (1991) Mating habits of the rockfish Sebastes inermis. Environ Biol Fish 30:15–22. doi: 10.1007/978-94-011-3792-8_2 CrossRefGoogle Scholar
  44. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol S 36:125–146CrossRefGoogle Scholar
  45. Sogard SM, Gilbert-Horvath E, Anderson EC, Fisher R, Berkeley SA, Garza JC (2008) Multiple paternity in viviparous kelp rockfish, Sebastes atrovirens. Environ Biol Fish 81(1):7–13. doi: 10.1007/s10641-006-9170-9 CrossRefGoogle Scholar
  46. Soucy S, Travis J (2003) Multiple paternity and population genetic structure in natural populations of the poeciliid fish, Heterandria formosa. J Evolution Biol 16(6):1328–1336. doi: 10.1046/j.1420-9101.2003.00608.x CrossRefGoogle Scholar
  47. Takahashi H, Takano K, Takemura A (1991) Reproductive cycles of Sebastes taczanowskii, compared with those of other rockfishes of the genus Sebastes//rockfishes of the genus Sebastes: their reproduction and early life history. Environ Biol Fish 30:23–29. doi: 10.1007/BF02296873 CrossRefGoogle Scholar
  48. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and process. Mol Ecol 17(11):2566–2580. doi: 10.1111/j.1365-294X.2008.03772.x CrossRefPubMedGoogle Scholar
  49. Van Doornik DM, Parker SJ, Millard SR, Berntson EA, Moran P (2008) Multiple paternity is prevalent in Pacific ocean perch (Sebastes alutus) off the Oregon coast, and is correlated with female size and age. Environ Biol Fish 83(3):269–275. doi: 10.1007/s10641-008-9331-0 CrossRefGoogle Scholar
  50. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166(4):1963–1979. doi: 10.1534/genetics.166.4.1963 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wang WQ, Zhang Y, Liu MX, Wu ZX, Wang LJ, Zi J, Guan J, You F (2012) Microsatellite analysis of genetic diversity in four wild stocks of black rockfish Sebastes schlegeli. Mar Sci 36(1):10–16 (In Chinese)Google Scholar
  52. Warner RR, Robertson DR (1982) Sperm competition and sperm storage as determinants of sexual dimorphism in the dwarf surfperch, Micrometrus minimus. Evolution 36(1):44–55CrossRefGoogle Scholar
  53. Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13(6):246–250. doi: 10.1016/S0169-5347(98)01383-4 CrossRefPubMedGoogle Scholar
  54. Yoshida K, Nakagawa M, Wada S (2001) Pedigree tracing of a hatchery-reared stock used for aquaculture and stock enhancement based on DNA markers. Fish Genet Breeding Sci 30:27–35 (In Japanese)Google Scholar
  55. Yoshida K, Nakagawa M, Wada S (2005) Multiplex PCR system applied for analysing microsatellite loci of Schlegel’s black rockfish, Sebastes schlegeli. Mol Ecol Resour 5(2):416–418. doi: 10.1111/j.1471-8286.2005.00945.x CrossRefGoogle Scholar
  56. Zajitschek SRK, Lindholm AK, Evans JP, Brooks RC (2009) Experimental evidence that high levels of inbreeding depress sperm competitiveness. J Evolution Biol 22(6):1338–1345. doi: 10.1111/j.1420-9101.2009.01738.x CrossRefGoogle Scholar
  57. Zeh JA, Zeh DW (2000) Reproductive mode and speciation: the viviparity-driven conflict hypothesis. BioEssays 22:938–946. doi: 10.1002/1521-1878(200010)22:10<938::AID-BIES9>3.3.CO;2-0 CrossRefPubMedGoogle Scholar
  58. Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61(6):1051–1063. doi: 10.1006/anbe.2000.1705 CrossRefGoogle Scholar
  59. Zhang YQ, Xu Q, Alós J, Liu H, Xu QZ, Yang HS (2015) Short-term fidelity, habitat use and vertical movement behavior of the black rockfish Sebastes schlegelii as determined by acoustic telemetry. PLoS One 10(8):e0134381. doi: 10.1371/journal.pone.0134381 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Tianxiang Gao
    • 1
  • Kui Ding
    • 2
  • Na Song
    • 2
  • Xiumei Zhang
    • 2
  • Zhiqiang Han
    • 1
  1. 1.Fishery CollegeZhejiang Ocean UniversityZhoushanChina
  2. 2.Fishery CollegeOcean University of ChinaQingdaoChina

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