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Multiple paternity in the thalassinidean ghost shrimp, Callichirus islagrande (Crustacea: Decapoda: Callianassidae)

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Abstract

Adult ghost shrimp, Callichirus islagrande (Schmitt, 1935), are obligate inhabitants of burrow systems that they excavate deeply into beachfront sediments in the northern Gulf of Mexico. Mating presumably occurs in these burrows but has never been directly observed in C. islagrande or any other thalassinidean. A variety of possible mating systems is suggested by those of other decapods, among which are examples of both internal and external sperm deposition, sperm competition among males, and male adaptations for paternity assurance. We used genetic markers to determine if clutches brooded by individual female ghost shrimp had been fertilized by multiple males. The two microsatellite loci we employed were sufficiently polymorphic to detect 95% of the occurrences of fertilization by two males. Among 40 ovigerous females collected from the Louisiana Isles Dernieres barrier island, eight (20%) carried egg masses for which more than two paternal alleles were detected, indicating fertilization by multiple males. In two cases of multiple paternity, alleles from one of the males were detected in only a portion of an egg mass. These observations suggest several, possibly novel characteristics of the mating system that can be further investigated.

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References

  • Bauer RT (1986) Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans. J Crustac Biol 6:313–325

    Google Scholar 

  • Bauer RT (1992) Repetitive copulation and variable success of insemination in the marine shrimp Sicyonia dorsalis (Decapoda: Penaeoidea). J Crustac Biol 12:153–160

    Google Scholar 

  • Bauer RT, Min LJ (1993) Spermatophores and plug substance of the marine shrimp Trachypenaeus similis (Crustacea: Deacapoda: Penaeidae): formation in the male reproductive tract and disposition in the inseminated female. Biol Bull 185:174–185

    Google Scholar 

  • Burfitt AH (1980) Glucose phosphate isomerase inheritance in Cancer pagurus L broods as evidence of multiple paternity (Decapoda: Brachyura). Crustaceana 39:306–310

    Google Scholar 

  • Caldwell RL (1991) Variation in reproductive behavior in stomatopod Crustacea. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 67–90

  • Coelho VR, Rodrigues SD (2001) Setal diversity, trophic modes and functional morphology of feeding appendages of two callianassid shrimps, Callichirus major and Sergio mirim (Decapoda: Thalassinidea: Callianassidae). J Nat Hist 35:1447–1483

    Article  Google Scholar 

  • Coelho VR, Cooper RA, Rodrigues SD (2000) Burrow morphology and behavior of the mud shrimp Upogebia omissa (Decapoda: Thalassinidea: Upogebiidae). Mar Ecol Prog Ser 200:229–240

    Google Scholar 

  • Diesel R (1991) Sperm competition and the evolution of mating behavior in Brachyura, with special reference to spider crabs (Decapoda: Majidae). In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 126–144

  • Durbaum J (1995) Discovery of postcopulatory mate guarding in Copepoda harpacticoida (Crustacea). Mar Biol 123:81–88

    Google Scholar 

  • Elner RW, Gass CA, Campbell A (1985) Mating behavior of the Jonah crab, Cancer borealis Stimpson (Decapoda, Brachyura). Crustaceana 48:34–39

    Google Scholar 

  • Felder DL (2001) Diversity and ecological significance of deep-burrowing macrocrustaceans in coastal tropical waters of the Americas (Decapoda: Thalassinidea). Interciencias 26:2–12

    Google Scholar 

  • Felgenhauer BE, Abele LG (1991) Morphological diversity of decapod spermatozoa. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 322–341

  • Heath DJ, Ratford JR, Riddoch BJ, Childs D (1990) Multiple mating in a natural population of the isopod Sphaeroma rugicauda—evidence from distorted ratios in offspring. Heredity 64:81–85

    Google Scholar 

  • Hinsch GW (1968) Reproductive behavior in the spider crab, Libinia emarginata (L.). Biol Bull 135:273–278

    Google Scholar 

  • Hooper RG (1986) A spring breeding migration of the snow crab, Chionoecetes opilio (O. Fabr.), into shallow water in Newfoundland. Crustaceana 50:257–264

    Google Scholar 

  • Jamieson, BGM, Tudge CC (2000) Crustacea-Decapoda. In: Jamieson BGM (ed) Progress in male gamete ultrastructure and phylogeny. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of the invertebrates. Wiley, Chichester, pp 1–95

  • Jones MW, O’Reilly PT, McPherson AA, McParland TL, Armstrong DE, Cox AJ, Spence KR, Kenchington EL, Taggart CT, Bentzen P (2003) Development, characterization, inheritance, and cross-species utility of American lobster (Homarus americanus) microsatellite and mtDNA PCR-RFLP markers. Genome 46:59–69

    Article  CAS  PubMed  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 

  • Koga T, Henmi Y, Murai M (1993) Sperm competition and the assurance of underground copulation in the sand-bubbler crab Scopimera globosa (Brachyura: Ocypodidae). J Crustac Biol 13:134–137

    Google Scholar 

  • Minouchi S, Goshima S (1998) Effect of male/female size ratio on mating behavior of the hermit crab Pagurus filholi (Anomura: Paguridae) under experimental conditions. J Crustac Biol 18:710–716

    Google Scholar 

  • Morell V (1998) Evolution of sex: a new look at monogamy. Science 281:1982–1983

    Article  CAS  PubMed  Google Scholar 

  • Murai M, Goshima S, Henmi Y (1987) Analysis of the mating system of the fiddler crab, Uca lactea. Anim Behav 35:1334–1342

    Google Scholar 

  • Nelson K, Hedgecock D (1977) Electrophoretic evidence of multiple paternity in the lobster Homarus americanus (Milne-Edwards). Am Nat 111:361–365

    Article  Google Scholar 

  • Sainte-Marie B, Urbani N, Sevigny JM, Hazel F, Kuhnlein U (1999) Multiple choice criteria and the dynamics of assortative mating during the first breeding season of female snow crab Chionoecetes opilio (Brachyura, Majidae). Mar Ecol Prog Ser 181:141–153

    Google Scholar 

  • Sevigny JM, Sainte-Marie B (1996) Electrophoretic data support the last-male sperm precedence hypothesis in the snow crab Chionoecetes opilio (Brachyura: Majidae). J Shellfish Res 15:437–440

    Google Scholar 

  • Strasser KM, Felder DL (2000) Larval development of the ghost shrimp Callichirus islagrande (Decapoda: Thalassinidea: Callianassidae) under laboratory conditions. J Crustac Biol 20:100–117

    Google Scholar 

  • Subramoniam T (1977) Aspects of sexual biology of the anomuran crab, Emerita asiatica. Mar Biol 43:369–377

    Google Scholar 

  • Subramoniam T (1979) Some aspects of reproductive ecology of a mole crab Emerita asiatica (Milne Edwards). J Exp Mar Biol Ecol 36:259–268

    Article  Google Scholar 

  • Subramoniam T (1993) Spermatophores and sperm transfer in marine crustaceans. Adv Mar Biol 29:129–214

    Google Scholar 

  • Tamaki A, Tanoue H, Itoh J, Fukuda Y (1996) Brooding and larval developmental periods of the callianassid ghost shrimp, Callianassa japonica (Decapoda: Thalassinidea). J Mar Biol Assoc UK 76:675–689

    Google Scholar 

  • Tamaki A, Itoh J, Kumiko K (1999) Distributions of three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) in intertidal habitats along an estuary to open-sea gradient in western Kyushu, Japan. Crustac Res 28:37–51

    Google Scholar 

  • Tudge CC, Cunningham CW (2002) Molecular phylogeny of the mud lobsters and mud shrimps (Crustacea: Decapoda: Thalassinidea) using nuclear 18S rDNA and mitochondrial 16S rDNA. Invert Systematics 16:839–847

    Article  Google Scholar 

  • Urbani N, Sainte-Marie B, Sevigny JM, Zadworny D, Kuhnlein U (1998a) Sperm competition and paternity assurance during the first breeding period of female snow crab (Chionoecetes opilio) (Brachyura: Majidae). Can J Fish Aquat Sci 55:1104–1113

    Article  Google Scholar 

  • Urbani N, Sevigny JM, Sainte-Marie B, Zadworny D, Kuhnlein U (1998b) Identification of microsatellite markers in the snow crab Chionoecetes opilio. Mol Ecol 7:357–358

    CAS  PubMed  Google Scholar 

  • Walker D, Porter BA, Avise JC (2002) Genetic parentage assessment in the crayfish Orconectes placidus, a high-fecundity invertebrate with extended maternal brood care. Mol Ecol 11:2115–2122

    Article  CAS  PubMed  Google Scholar 

  • Watson J (1972) Mating behavior of the spider crab, Chionoecetes opilio. J Fish Res Bd Can 27:447–449

    Google Scholar 

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Acknowledgements

We extend thanks to R. Bourgeois for help with specimen collection. This study was funded by grants from the U.S. Department of Energy (grant no. DE-FG02-97ER12220) and the National Science Foundation. This is contribution no. 101 from the UL Lafayette Laboratory for Crustacean Research. All experiments that were conducted comply with current laws of the United States of America.

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Correspondence to A. L. Bilodeau.

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Communicated by P.W. Sammarco, Chauvin

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Bilodeau, A.L., Felder, D.L. & Neigel, J.E. Multiple paternity in the thalassinidean ghost shrimp, Callichirus islagrande (Crustacea: Decapoda: Callianassidae). Marine Biology 146, 381–385 (2005). https://doi.org/10.1007/s00227-004-1444-1

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