Skip to main content
Log in

High prevalence of multiple paternity in the deep-sea shrimp Acanthephyra pelagica

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Acanthephyra pelagica is a deep-sea pelagic shrimp with a global distribution. Mating has never been observed in this species as its pelagic lifestyle makes direct observations difficult. Multiple paternity has been reported for many other crustaceans, although not for deep-sea shrimp species like A. pelagica. Here we used four polymorphic microsatellite loci to test for multiple paternity. We genotyped the mother and a maximum of 63 of her brooded embryos in 19 ovigerous females, all of which exhibited evidence of multiple paternity; the frequency of multiple paternity is thus deemed to be close to 100 % in this species. The number of males contributing to each brood varied between 2 and 4 with evidence of pronounced reproductive skew suggesting the potential importance of mating order, different sperm contribution, the existence of pre-copulatory female choice, or post-copulatory sperm competition or selection. Our results with respect to multiple paternity, together with the size patterns, suggest a pure-search mating system. Our findings on the mating system of A. pelagica contribute to a better understanding of the reproductive behavior of this species.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton 599 pp

    Google Scholar 

  • Baggio RA, Pil MW, Boeger WA, Patella LA, Ostrensky A, Pie M (2011) Genetic evidence for multiple paternity in the mangrove land crab Ucides cordateus (Decapoda: Ocypodidae). Mar Biol Res 7:520–524. doi:10.1080/17451000.2010.528771

    Article  Google Scholar 

  • Bailie DA, Fitzpatrick S, Connolly M, Thiel M, Hynes R, Prodöhl PA (2014) Genetic assessment of parentage in the caridean rock shrimp Rhynchocinetes typus based on microsatellite markers. J Crust Biol 34:658–662. doi:10.1163/1937240X-00002254

    Article  Google Scholar 

  • Baragona MA, Haig-Ladewig LA, Wang SY (2000) Multiple paternity in the grass shrimp Palaemontes pugio. Am Zool 40:935

    Google Scholar 

  • Bauer R (1986) Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans. J Crust Biol 6:313–325. doi:10.1163/193724086X00181

    Article  Google Scholar 

  • Bauer R (2004) Remarkable shrimps: adaptations and natural history of the carideans. University of Oklahoma Press, Norman

    Google Scholar 

  • Bauer R, Abdalla J (2001) Male mating tactics in the shrimp Palaemontes pugio (Decapoda: Caridea): precopulatory mate guarding vs. pure searching. Ethology 107:185–199. doi:10.1046/j.1439-0310.2001.00636.x

    Article  Google Scholar 

  • Bauer R, Thiel M (2011) First description of a pure-search mating system and protandry in the shrimp Rhynchocinetes uritai (Decapoda: Caridea). J Crust Biol 31:286–295. doi:10.1651/10-3378.1

    Article  Google Scholar 

  • Berg A, Sandifer P (1984) Mating behaviour of the grass shrimp Palaemonetes pugio Holthuis (Decapoda, Caridea). J Crust Biol 4:417–424. doi:10.1163/1937240X84X00228

    Article  Google Scholar 

  • Bilodeau A, Felder D, Neigel J (2005) Multiple paternity in the thalassinidean Ghost shrimp, Callichirus islagrande (Crustacea: Decapoda: Callianassidae). Mar Biol 146:381–385. doi:10.1007/s00227-004-1444-1

    Article  Google Scholar 

  • Burukovsky R, Andreeva V (2010) On the biology of Acanthephyra pelagica (Decapoda: Natantia: Oplophoridae) of the North Atlantic Subtropical convergence zone. J Sib Fed Univ 3:303

    Google Scholar 

  • Correa C, Thiel M (2003) Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Rev Chil Hist Nat 76:187–203

    Article  Google Scholar 

  • Dennenmoser S, Thiel M (2015) Cryptic female choice in crustaceans. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Berlin, pp 203–237

    Chapter  Google Scholar 

  • Elphinstone M, Hinten G, Anderson M, Nock C (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320. doi:10.1046/j.1471-8286.2003.00397.x

    Article  CAS  Google Scholar 

  • Evans J, Magurran A (2000) Multiple benefits of multiple mating in guppies. Proc Natl Acad Sci 97:10074–10076. doi:10.1073/pnas.180207297

    Article  CAS  Google Scholar 

  • Felgenhauer B, Abele L (1991) Morphological diversity of decapod spermatozoa. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, p 322

    Google Scholar 

  • Fleming I, Gross M (1994) Breeding competition in a pacific salmon (Coho: Oncorhynchus kisutch): measures of natural and sexual selection. Evolution. doi:10.2307/2410475

    Google Scholar 

  • Gayanilo FC, Sparre P, Pauly D (2005) FAO-ICLARM stock assessment tools II: user’s guide, vol 8. Food & Agriculture Org, Rome

    Google Scholar 

  • Gosselin T, Sainte-Marie B, Bernatchez L (2005) Geographic variation of multiple paternity in the American lobster, Homarus americanus. Mol Ecol 14:1517–1525. doi:10.1111/j.1365-294X.2005.02498.x

    Article  CAS  Google Scholar 

  • Gross M (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98. doi:10.1016/0169-5347(96)81050-0

    Article  CAS  Google Scholar 

  • Haase M, Baur B (1995) Variation in spermathecal morphology and storage of spermatozoa in the simultaneously hermaphroditic land snail Arianta arbustorum (Gastropoda: Pulmonata: Stylommatophora). Invertebr Reprod Dev 28:33–41. doi:10.1080/07924259.1995.9672461

    Article  Google Scholar 

  • Herring PJ (1967) Observations on the early larvae of three species of Acanthephyra (Crustacea, Decapoda, Caridea). Deep-Sea Res 14:325–329. doi:10.1016/0011-7471(67)90075-7

    Google Scholar 

  • Jennions M, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  Google Scholar 

  • Jensen P, Bentzen P (2012) A molecular dissection of the mating system of the dungeness crab, Metacarcinus magister (Brachyura: Cancridae). J Crust Biol 32:443–456. doi:10.1163/193724012X626458

    Article  Google Scholar 

  • Jones A (2005) Gerud 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Mol Ecol Notes 5:708–711. doi:10.1111/j.1471-8286.2005.01029.x

    Article  CAS  Google Scholar 

  • Jones A, Ardren W (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523. doi:10.1046/j.1365-294X.2003.01928.x

    Article  CAS  Google Scholar 

  • Jones M, O’Reilly P, McPherson A, McParland T, Armstrong D, Cox A, Spence K, Kenchington E, Taggart C, Bentzen P (2003) Development, characterisation, inheritance, and cross-species utility of American lobster (Homarus americanus) microsatellite and mtDNA PCR-RFLP markers. Genome 46:59–69. doi:10.1139/g02-105

    Article  CAS  Google Scholar 

  • Jormalainen V (1998) Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. Q Rev Biol 73:275–304

    Article  Google Scholar 

  • Jorquera E, Anstey L, Paterson I, Kenchington E, Ruzzante DE (2014) Isolation and characterization of 26 novel microsatellite loci in the deep-sea shrimp Acanthephyra pelagica. Conserv Genet Resour 6:731–733. doi:10.1007/s12686-014-0201-0

    Article  Google Scholar 

  • Jossart Q, Wattier R, Kastally C, Aron S, David B, Ridder C, Rigaud T (2014) Genetic evidence confirms polygamous mating system in a crustacean parasite with multiple hosts. PLoS ONE 9:e90680. doi:10.1371/journal.pone.0090680

    Article  Google Scholar 

  • Kahrl AF, Laushman RH, Roles A (2014) Evidence for multiple paternity in two species of Orconectes crayfish. Can J Zool 92:985–988. doi:10.1139/cjz-2014-0132

    Article  CAS  Google Scholar 

  • Kenchington T, Best M, Bourbonnais-Boyce C, Clement P, Cogswell A, MacDonald B, MacEachern W, MacIsaac K, MacNab P, Paon L, Reid J, Roach S, Shea L, Themelis D, Kenchington E (2009) Methodology of the 2007 survey of meso- and bathypelagic micronekton of the Sable Gully: cruise TEM 768. Can Tech Rep Fish Aquat Sci 2853, vi + 91 pp

  • Kenchington T, Benjamin R, Best M, Cogswell A, Cook A, Devaney S, Lirette C, MacDonald B, MacIsaac K, Mallam P, McIntyre T, McMillan A, Moors-Murphy H, Morton G, Paon L, Roach S, Shea E, Themelis D, Kenchington E (2014) Field methods of the 2008, 2009 and 2010 surveys of meso- and bathypelagic micronekton in The Gully. Can Tech Rep Fish Aquat Sci 3076: iv + 73p

  • Martinez J, Moran P, Perez J, De Gaudemar B, Beall E, Garcia-Vazquez E (2000) Multiple paternity increases effective size of southern Atlantic salmon populations. Mol Ecol 9:293–298. doi:10.1046/j.1365-294x.2000.00857.x

    Article  CAS  Google Scholar 

  • Mathews D (1956) The probable method of fertilization in the terrestrial hermit crabs based on a comparative study of spermatophores. Pac Sci 10:303

    Google Scholar 

  • Mathews L (2007) Evidence for high rates of in-pair paternity in the socially monogamous snapping shrimp Alpheus angulosus. Aquat Biol 1:55–62. doi:10.3354/ab00007

    Article  Google Scholar 

  • Moyano M, Gavio M, Luppi T (2015) Different sperm allocation strategies in two populations of the semiterrestrial crab Neohelice granulata (Brachyura, Grapsoidea, Varunidae). Mar Ecol. doi:10.1111/maec.12338

    Google Scholar 

  • Neff B, Pitcher T (2002) Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J Fish Biol 61:739–750. doi:10.1111/j.1095-8649.2002.tb00908.x

    Article  Google Scholar 

  • Neff B, Repka J, Gross M (2000) Parentage analysis with incomplete sampling of candidate parents and offspring. Mol Ecol 9:515–528. doi:10.1046/j.1365-294x.2000.00888.x

    Article  CAS  Google Scholar 

  • Pugh T, Comeau M, Benhalima K, Watson W (2015) Variation in the size and composition of ejaculates produced by male American lobsters, H. Milne Edwards, 1837 (Decapoda: Nephropidae). J Crust Biol 35:593–604. doi:10.1163/1937240X-00002365

    Article  Google Scholar 

  • Reynolds J (1996) Animal breeding systems. Trends Ecol Evol 11:68–72. doi:10.1016/0169-5347(96)81045-7

    Article  CAS  Google Scholar 

  • Rojas-Hernandez N, Véliz D, Pardo LM (2014) Use of novel microsatellite markers for population and paternity analysis in the commercially important crab Metacarcinus edwardsii (Brachyura: Cancridae). Mar Biol Res 10:839–844. doi:10.1080/17451000.2013.863350

    Article  Google Scholar 

  • Rondeau A, Sainte-Marie B (2001) Variable mate-guarding time and sperm allocation by male snow crab (Chionoecetes opilio) in response to sexual competition, and their impact on the mating success of females. Biol Bull (Woods Hole) 201:204–217

    Article  CAS  Google Scholar 

  • Roy N (2003) Incidence de la polyandrie chez le crabe des neiges, Chionoecetes opilio (Brachyura, Majidae). Master thesis, Université du Québec à Rimouski, Canada

  • Sainte-Marie B, Gosselin T, Sévigny JM, Urbani N (2008) The snow crab mating system: opportunity for natural and unnatural selection in a changing environment. Bull Mar Sci 83:131–161

    Google Scholar 

  • Salmon M (1983) Courtship, mating systems, and sexual selection in decapods. Studies in adaptation: the behaviour of higher crustacea. Wiley, New York, pp 143–169

    Google Scholar 

  • Sato T, Ashidate M, Wada S, Goshima S (2005) Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab Paralithodes brevipes. Mar Ecol Prog Ser 296:251–262

    Article  Google Scholar 

  • Slatyer RA, Jennions MD, Backwell PRY (2012) Polyandry occurs because females initially trade sex for protection. Anim Behav 83:1203–1206. doi:10.1016/j.anbehav.2012.02.011

    Article  Google Scholar 

  • Sørdalen TK (2012) Multiple paternity assessment and paternity assignment in wild European lobster (Homarus gammarus). Master thesis, Norwegian University of Life Sciences, Norway

  • Streiff R, Mira S, Castro M, Cancela M (2004) Multiple paternity in Norway lobster (Nephrops norvegicus) assessed with microsatellite markers. Mar Biotechnol 6:60–66. doi:10.1007/s10126-003-0015-7

    Article  CAS  Google Scholar 

  • Subramoniam T (1993) Spermatophores and sperm transfer in marine crustaceans. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology. Academic Press, New York, pp 129–201

    Google Scholar 

  • Subramoniam T (2013) Origin and occurrence of sexual and mating systems in Crustacea: a progression towards communal living and eusociality. J Biosci 38:951–969. doi:10.1007/s12038-013-9392-x

    Article  CAS  Google Scholar 

  • Sugg D, Chesser R (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155

    CAS  Google Scholar 

  • Thiel M, Correa C (2004) Female rock shrimp Rhynchocinetes typus mate in rapid succession up a male dominance hierarchy. Behav Ecol Sociobiol 57:62–68. doi:10.1007/s00265-004-0828-z

    Article  Google Scholar 

  • Thiel M, Hinojosa IA (2003) Mating behaviour of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea)—indication for convenience polyandry and cryptic female choice. Behav Ecol Sociobiol 55:113–121

    Article  Google Scholar 

  • Thonhauser K, Thoß M, Musolf K, Klaus T, Penn DJ (2014) Multiple paternity in wild house mice (Mus musculus musculus): effects on offspring genetic diversity and body mass. Ecol Evol 4:200–209. doi:10.1002/ece3.920

    Article  Google Scholar 

  • Toonen R (2004) Genetic evidence of multiple paternity of broods in the intertidal crab Petrolisthes cinctipes. Mar Ecol Prog Ser 270:259–263. doi:10.3354/meps270259

    Article  Google Scholar 

  • Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580. doi:10.1111/j.1365-294X.2008.03772.x

    Article  Google Scholar 

  • Villesen P, Gertsch PJ, Frydenberg J, Mueller UG, Boomsma JJ (1999) Evolutionary transition from single to multiple mating in fungus-growing ants. Mol Ecol 8:1819–1825. doi:10.1046/j.1365-294x.1999.00767.x

    Article  CAS  Google Scholar 

  • Walker D, Porter B, Avise J (2002) Genetic parentage assessment in the crayfish Orconectes placidus, a high-fecundity invertebrate with extended maternal brood care. Mol Ecol 11:2115–2122. doi:10.1046/j.1365-294X.2002.01609.x

    Article  CAS  Google Scholar 

  • Yue G, Chang A (2010) Molecular evidence for high frequency of multiple paternity in a freshwater shrimp species Caridina ensifera. PLoS ONE 5:e12721. doi:10.1371/journal.pone.0012721

    Article  Google Scholar 

  • Yue G, Li J, Wang C, Xia J, Wang G, Feng J (2010) High prevalence of multiple paternity in the invasive crayfish species, Procambarus clarkii. Int J Biol Sci 6:107–115. doi:10.7150/ijbs.6.107

    Article  Google Scholar 

Download references

Acknowledgments

We thank MartinThiel and an anonymous referee for their very helpful comments on a previous version of the manuscript. The authors would like to thank Chief Scientist Dr. T. J. Kenchington (Gadus Associates, Musquodoboit Harbour, Nova Scotia) and other participants of the 2007–2010 trawl surveys of the mesopelagic fauna of the Gully MPA for collecting the samples used in this study. The surveys were funded by Fisheries and Oceans, Canada, through the Bedford Institute of Oceanography under the project management of EK. Also authors thank the Marine Gene Probe Lab colleagues: Ian Paterson, Gregory McCraken, Abby Van der Jagt and Ivan Vera. We also thank Paul Bentzen for valuable advice as well as Kevin MacIsaac and Lynne Anstey (Bedford Institute of Oceanography) for the help with taxonomy and support with laboratory analyses, respectively.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erika Jorquera.

Additional information

Responsible Editor: O. Puebla.

Reviewed by M. Thiel and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jorquera, E., Kenchington, E. & Ruzzante, D.E. High prevalence of multiple paternity in the deep-sea shrimp Acanthephyra pelagica . Mar Biol 163, 89 (2016). https://doi.org/10.1007/s00227-016-2868-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2868-0

Keywords

Navigation