Abstract
Crustaceans are known for their unrivalled diversity of sexual systems, as well as peculiar mating associations to achieve maximum mating success and fertilization accomplishment. Although sexes are separate in most species, various types of hermaphroditism characterize these predominantly aquatic arthropods. A low operational sex ratio between female and male, together with temporally limited receptivity of females towards males, imposes restrictions on the structuring of mating systems in crustaceans. The basic mating systems consist of monogamy, polygamy, mate guarding and pure searching. Understandably, ecological influences may also play a determinative role in the evolution of such sexual and mating systems in crustaceans. An important outcome of the crustacean sexual biology is the development of complex social structures in many aquatic species, in much the same way insects have established them in terrestrial conditions. In addition, groups like isopods and certain families of brachyuran crabs have shown terrestrial adaptation, exhibiting peculiar reproductive modes, sometimes reminiscent of their terrestrial counterparts, insects. Many caridean shrimps, living in symbiotic relationship with other marine invertebrates in the coral reef habitats, have reached pinnacle of complexity in sexuality and peculiar mating behaviours, resulting in communal living and establishing advanced social systems, such as eusociality.
Similar content being viewed by others
References
Abe M and Fukuhara H 1996 Protogynous hermaphroditism in the brackish and fresh water isopod Gnorimosphaeroma naktogense (Crustacea : Isopoda, Sphaeromatidae). Zool Sci. 13 325–329
Alexander RD, Noonan K and Crespi BJ 1991 The evolution of eusociality; in: The biology of the naked mole-rat (eds) PW Sherman, JUM Jarvis and RD Alexander (Princeton, NJ: Princeton University Press) pp 3–44
Amdam GV, Norberg K, Hagen A and Omholt SW 2003 Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. USA 100 1799–1802
Anilkumar G, Sudha K and Subramoniam T 1999 Spermatophore transfer and sperm structure in the brachyuran crab Metopograpsus messor (Decapoda: Grapsidae). J. Crust. Biol. 19 361–370
Asakura A 2009 The evolution of mating systems in decapod crustaceans; in Crustacean issues 18, Decapod crustacean phylogenetics (eds) JW Martin, KA Crandall and DL Felder (Boca Raton: CRC Press) pp 121–182
Avise JC 2011 Hermaphroditism: A primer on the biology, ecology, and evolution of dual sexuality (New York: Columbia University Press)
Baeza JA and Thiel M 2007 The mating system of symbiotic crustaceans. A conceptual model based on optimality and ecological constraints; in Evolutionary ecology of social and sexual systems: Crustaceans as model organism (eds) JE Duffy and M Thiel (Texas: Oxford University Press) pp 249–267
Baeza JA 2008 Protandric simultaneous hermaphroditism in the shrimps Lysmata bahia and Lysmata intermedia.. Invert. Biol. 127 181–188
Banner AH and Banner DM 1983 Annotated checklist of the alpheid shrimp from the western Indian Ocean. Travaux Documents L’ORSTOM 158 1–164
Barki A, Karplus I, Manor R and Sagi A 2006 Intersexuality and behavior in crayfish: the de-masculinization effects of androgenic gland ablation. Hormones Behav. 50 322–331
Bauer 1976 Mating behaviour and spermatophore transfer in the shrimp Heptacarpus pictus (Stimpson) (Decapoda: Caridea: Hippolytidar). J. Nat. Hist. 10 315–440
Bauer RT 1986 Sex change and life history pattern in the shrimp Thor manningi (Decapoda: Caridea): a novel case of protandric hermaphroditism. Biol. Bull. 179 11–31
Bauer RT 2000 Simultaneous Hermaphroditism in caridean shrimps: a unique and puzzling sexual system in the Decapoda. J. Crust. Biol. 20 116–128
Bauer RT and Abdalla JA 2001 Male mating tactics in the shrimp Palaemonetes pugio (Decapoda, Caridea): Precopulatory mate guarding vs. pure searching. Ethology 1107 185–199
Bauer RT 2002 Reproductive ecology of a protandric simultaneous hermaphrodite, The shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). J. Crust. Biol., 22 742–749
Bauer RT 2004 Remarkable shrimps: Natural history and adaptations of the carideans (Norman: University of Okalahoma Press)
Bauer RT 2007 Hermaphroditism in caridean shrimps: mating systems, sociobiology, and evolution, with special reference to Lysmata; in Evolutionary ecology of social and sexual systems: Crustaceans as model organism (eds) JE Duffy and M Thiel (Texas: Oxford University Press) pp 232—248
Bergstrom BI 1997 Do protandric pandalid shrimp have environmental sex determination? Mar. Biol. 128 397–407
Bergström BI 2000 The biology of Pandalus. Adv. Mar. Biol. 38 55–245
Boddeke R, Bosschieter JR and Goudswaard PC 1991 Sex change, mating, and sperm transfer in Crangon crangon (L.); in Crustacean sexual biology (eds) RT Bauer and JW Martin (New York: Columbia University Press) pp 164–182
Brook HJ, Rawlings TA and Davies RW 1994 Protogynous sex change in the intertidal isopod Gnorimosphaeroma oregonense (Crustacea: Isopoda). Biol. Bull. 187 99–111
Buchanan JB 1963 The biology of Calocaris macandreae (Crustacea: Thalassinidea). J. Mar. Biol Assoc. U.K. 43 729–748
Bull JJ 1983 Evolution of sex determining mechanisms (Menlo Park: Benjamin/ Cummings Publishing Co)
Butler TH 1964 Growth, reproduction and distribution of pandalid shrimps in British Columbia. J. Fish. Res. Board Can. 21 1403–1452
Butler TH 1980 Shrimps of the Pacific coast of Canada. Can. Bull. Fish. Aquat. Sci. 202–280
Chace FA 1972 The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contribut. Zool. 98 1–179
Charniaux-Cotton H 1975 Hermaphroditism and gynandromorphism in malacostracan Crustacea; in Intersexuality in the animal kingdom (ed) R Reinboth (Berlin/Heidelberg: Springer-Verlag) pp 91–105
Charniaux-Cotton H and Payen G 1985 Sexual differentiation; in The biology of Crustacea Vol 9 Integument, pigments, and hormonal processes (eds) DE Bliss and LH Mantel (New York: Academic Press) pp 217–299
Charnov EL, Gotshall DW and Robinson JG 1978 Sex ratio: an adaptive response to population fluctuations in pandalid shrimps. Science 200 204–206
Charnov EL 1979 Natural selection in Pandalid shrimp: a test of life history theory. Am. Nat. 134 824–827
Charnov EL 1982 The theory of sex allocation (New Jersey: Princeton University Press)
Charnov EL and Hannah RW 2002 Shrimp adjust their sex ratio to fluctuating age. Evol. Ecol. Res. 4 239–246
Charnov E 1993 Life history invariants (Oxford University Press)
Choe JC and Crespi BJ 1997 The evolution of social behavior in insects and arachnids (Cambridge: Cambridge University Press) pp 1–541
Christy H 1987 Competitive mating, mate choice and mating associations of brachyuran crabs. Bull. Mar. Sci. 41 177–191
Christy JH 2007 Predation and the reproductive behavior in the fiddler crabs (genus Uca); in Evolutionary ecology of social and sexual systems (eds) JE Duffy and M Thiel (Oxford: Oxford University Press) pp 211–231
Choe JC and Crispi BJ 1997 Social behaviour in insects and arachnids (Cambridge: Cambridge University Press)
Clark WH 1978 Hermaphroditism as a reproductive strategy for metazoans. some correlated benefits. New Zeal. J. Zool. 5 769–780
Correa C, Baeza A, Hinojosa I and Thiel M 2003 Male dominance hierarchy and mating tactics in the rock shrimp Rhynchocinetes typus (Decapoda: Caridea). J. Crust. Biol. 23 33–45
Diesel R and Schubart CD 2007 The Social Breeding Systems of the Jamaican Bromeliad Crab, Metopaulias Depressus); in Evolutionary ecology of social and sexual systems (eds) JE Duffy and M Thiel (New York: Oxford University Press) pp 365–386
Dohrn PFR and Holthuis LB 1950 Lysmata nitida, a new species of prawn (Crustacea:Decapoda) from the western Mediterranean. PubbLStn. ZooLNapoli 22 339–347
Duffy JE 1996 Eusociality in a coral-reef shrimp. Nature 381 512–514
Duffy JE and KS Macdonald 1999 Colony structure of the social snapping shrimp, Synalpheus filidigitus in Belize. J. Crust. Biol. 19 283–292
Duffy JE 2007 Ecology and evolution of eusociality in sponge-dwelling shrimp; in Evolutionary ecology of social and sexual systems (eds) JE Duffy and M Thiel (New York: Oxford University Press) pp 387–409
Emlen ST and Oring LW 1977 Ecology, sexual selection, and the evolution of mating systems. Science 197 215–233
Erdman RB and Balke NJ 1987 Population dynamics of the sponge-dwelling alpheid Synalpheus longicarpus with observations on S. brooksi and S.pectiniger in shallow-water assemblages of the eastern Gulf of Mexico. J. Crust. Biol. 7 328–337
Farmer AS 1972 A bilateral gynandromorph of Nephrops norvegicus (Decapoda: Nephropidae). Mar. Biol. 15 344–349
Fiedler GC, Rhyne A, Segawa R, Aotsuka T and Schizas N 2010 The evolution of euhermaphroditism in caridean shrimps: a molecular perspective of sexual systems and systematic. BMC Evol. Biol. 10 297–306
Fréchette JG, Corrivault GW and Couture R 1970 Hermaphrodisme protérandrique chez une crevette de la famille des crangonidés, Argis dentata Rathbun. Naturaliste Can. 97 805–822
Frey DG 1965 Differentiation of Alona costata Sars from two related species (Cladocera, Chydoridae). Crustaceana 8 159–173
García-Velazco H, Obregón-Barboza H, Rodríguez-Jaramillo C and Maeda-Martínez AM 2009 Reproduction of the tadpole shrimp Triops (Notostraca) in Mexican waters Curr. Sci. 96 91–97
Gherardi F and Calloni C 1993 Protandrous hermaphroditism in the tropical shrimp Athanus indicus (Decapoda: Caridea), a symbiont of sea urchins. J. Crust. Biol. 13 675–689
Ghiselin MT 1969 The evolution of hermaphroditism among animals. Q. Rev. Biol. 44 189–208
Grafen A and M Ridley 1983 A model of mate guarding. J. Theor. Biol. 102 549–567
Graham EB and Maximiliam JT 2009 The origine and evolution of arthropods. Nature 457 812–817
Guiasu RC and Dunham DW 1998 Inter-form agonistic contests in male crayfishes, Cambarus robustus (Decapoda, Cambaridae). Invert. Biol. 117 144–154
Hamilton WD 1964 The genetical evolution of social behavior I, II. J. Theor. Biol. 7 1–52
Hanamura Y and Ohtsuka S 2003 Occurrence of Intersex individuals in the sertgestid shrimp Acetus sibogae, in Darwin Harbour, Northern Teritory, Australia. Crustaceana 76 749–754
Hartnoll RG 1960 Swimming in spider crabs of the genus Macropodia. Nature 185 181
Hoffman DL 1972 The development of the ovotestis and copulatory organs in a population of protandric shrimp. Pandalus plalyceros from Lopez Sound. Washington. Biol. Bull. 142 251–270
Hayashi KI and Ogawa Y 1987 Spongicola levigata sp. Nov., a new shrimp associated with a hexactinellid sponge from the East China Sea (Decapoda, Stenopodidae). Zool. Sci. 4 367–373
Jarvis JUM and Bennett NC 1993 Eusociality has evolved independently in two species of bathyergid mole-rats but occurs in no other subterranean mammal. Behav. Ecol. Sociobiol. 33 253–260
Jarvis JUM, O’Riain MJ, Bennett NC and Sherman PW 1994 Mammalian eusociality: a family affair. Trends Ecol. Evol. 9 47–51
Jivoff P and Hines AH 1998 Female behaviour, sexual competition and mate guarding in the blue crab, Callinectes sapidus. Anim. Behav. 55 589–603
Johnson VR 1969 Behavior associated with pair formation in the banded shrimp Stenopus hispidus. Pac. Sci. 23 40–52.
Johnson PT and Otto SV 1981 Histology of a bilateral gynandromorphy of the blue crab, Callinectes sapidus Rathbun (Decapoda, Portunidae). Biol. Bull. 161 236–245
Jormalainen V and Shuter SM 1999 Female reproductive cycle and sexual conflict over precopulatory mate guarding in Thermosphaeroma isopods. Ethology 105 233–246
Jormalainen V 2007 Mating strategies in isopods: from male monopolization to conflicts; in Evolutionary ecology of social and sexual systems (eds) JE Duffy and M Thiel (New York: Oxford University Press) pp 167–191
Kelly A, Hatcher M and Dunn A 2004 Intersexuality in the amphipod Gammarus duebeni results from incomplete feminisation by the vertically transmitted parasitic sex ratio distorter Nosema granulosis. Evol. Ecol. 18 121–132
Kim TW, Kim KW, Srygley RB and Choe JC 2004 Semilunar courtship rhythm of the fiddler crab Uca lactea in a habitat with great tidal variation. J. Ethol. 22 63–68
Kleiman DG 1977 Monogamy in mammals. Q. Rev. Biol. 52 39–69
Knowlton N 1980 Sexual Selection and dimorphism in two demes of a symbiotic, pair-bonding snapping shrimp. Evolution 34 161–173
Lack D 1968 Ecological adaptations for breeding in birds (London: Chapman & Hall)
Legrand JJ and P Juchault 1963 Mise en évidence d'un hennaphrodisme protogynique fonctionnel chez l'Isopode Anthuride Cyanthura carinata (Kroyer) et étude du mecanisme de l'inversion sexuelle. CR. Acad. Sci. 256 2931–2933
Legrand JJ, Legrand-Hamelin E and Juchault P 2007 Sex determination in Crustacea. Biol. Rev. 62 439–470
Linsenmair KE 2007 Sociobiology of terrestrial isopods; in Evolutionary ecology of social and sexual systems (eds) JE Duffy and M Thiel (New York: Oxford University Press) pp 339–365
Mathews LM 2003 Tests of the mate-guarding hypothesis for social monogamy: male snapping shrimp prefer to associate with high-value females. Behav. Ecol. 14 63–67
Morrison CL, Rios R and Duffy JE 2004 Phylogenetic evidence for an ancient rapid radiation of Carribean sponge-dwelling snapping shrimps. Mol. Phylog. Evol. 30 563–581
Murai M, Koga T and Yong HS 2002 The assessment of female reproductive state during courtship and scramble competition in the fiddler crab, Uca paradussmieri. Behav. Ecol. Sociobiol. 52 137–142
Nakashima Y 1987 Reproductive strategies in a partially protandrous shrimp, Athanas kominatoensis (Decapoda: Alpheidae): sex change as the best of a bad situation for subordinates. J. Ethol. 5 145–159
Nakasone Y and Murai M 1998 Mating behaviour of Uca lactea perplexa (Decapoda: Ocypodidae). J. Crust. Biol. 18 70–77
Nöel P 1973 Cycle biologique et inversion sexuelle du crustacé décapode Natantia Processa edulis. Cah. Biol. Mar. 14 217–227
Noël P 1976 L'evolution des caracteres sexuels chez Processa edulis Risso (Decapode, Natantia). Vie Milieu 26 65–104
Nolan B and Salmon M 1970 The behaviour and ecology of snapping shrimp (Crustacea: Alpheus heterochaelis and Alpheus noraonni). Forma Funct. 2 289–335
Pannell JR 2002 The evolution and maintenance of androdioecy. Annu. Rev. Ecol. Syst. 33 397–425
Parnes S, Khalaila I, Hulata G and Sagi A 2003 Are intersex crayfish Cherax quadricarinatus (Von Martens) genetically females? Genet. Res. 82 107–116
Parker GA 1970 Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45 525–567
Ra’anan Z and Sagi A 1985 Alternative mating strategies in male morphotypes of the freshwater prawn Macrobrachium rosenbergii (DeMan). Biol. Bull. 169 592–601
Rafael C-R, Alejandro M, Maeda-Martínez, Hortencia O-B, Gopal M, Danitzia A and Guerrero-Tortolero 2005 First report of gynandromorphy in parthenogenetic Artemia (branchiopoda: anostraca). J. Crust. Biol. 26 107–112
Rios R and Duffy JE 1999 Synalpheus williamsi (Decapoda: Alpheidae), a new sponge-dwelling shrimp from the Caribbean. Proc. Biol. Soc. Washington 112 541–552
Rudolph E, Verdi A and Tapia J 2001 Intersexuality in the burrowing crayfish Parastacus varicosus Faxon 1898 (Decapoda, Parastacidae). Crustaceana 74 27–37
Rufino MM and Jones DA 2001 Binary individual recognition in Lysmata debelius (Decapoda: Hippolytidae) under laboratory conditions. J. Crust. Biol. 21 388–392
Sagi A, Manor R, Segall C, Davis C and Khalaila I 2002 On intersexuality in the crayfish Cherax quadricarinatus: an inducible sexual plasticity model. Invert. Reprod. Develop. 41 27–33
Sassaman C 1991 Sex-ratio variation in female-biased populations of Notostracans. Hydrobiologia 212 169–179
Sassaman C and Weeks SC 1993 The genetic mechanism of sex determination in the conchostracan shrimp Eulimnadia texana. Am. Nat. 141 314–328
Sassaman C, Simovich MA and Fugate M 1997 Reproductive isolation and genetic differentiation in North American species of Triops (Crustacea: Branchiopoda: Notostraca). Hydrobiologia 359 125–147
Shuster SM and Caldwell RL 1989 Male defense of the breeding captivity and factors affecting the persistence of breeding pairs in the stomatopod, Gonodactylus bredini (Manning) (Crustacea, Hoplocarida). Ethology 82 192–207
Shuster SM 1992 The reproductive behaviour of α- ,β- and γ- males in Paracerceis sculpta, a common marine isopod crustacean. Behaviour 121 231–258
Shuster SM and Wade MJ 2003 Mating systems and strategies (Princeton, NJ: Princeton University Press)
Subramoniam T 1977 Aspects of sexual biology of the anomuran crab Emerita asiatica. Mar. Biol. 43 369–377
Subramoniam T 1979 Heterosexual raping in the mole crab, Emerita asiatica. Int. J. Invert. Reprod. 1 197–199
Subramoniam T 1981 Protandric hermaphroditiism in a mole crab Emerita Asiatica (Decapoda: Anomura). Biol. Bull. 160 161–174
Subramoniam T 1993 Spermatophores and sperm transfer strategy in marine crustaceans; in Advances in marine biology vol 29 (New York: Academic Press) pp 129–214
Sutcliffe DW 1992 Reproduction in Gammarus (Crustacea, Amphipoda): basic processes. Freshwater Forum 2 102–129
Thorn MJ and Fielder DR 1991 The red cuticle on the claw of male Cherax quadricarinatus (Decapoda: Parastacidae). Memoirs of the Queensland Museum 31 277
Thiel M and Hinojosa IA 2003 Mating behavior of female rock shrimp Rhynchocinetes typus (Decapoda: Caridae) indication for convenience polyandry and cryptic female choice. Behav. Ecol. Sociobiol. 55 113–121
Thiel M 2007 Social behaviour of parent-offspring groups in crustaceans; in Evolutionary ecology of social and sexual systems: Crustaceans as model organism (eds) JE Duffy and M Thiel (London: Oxford University Press) pp 294–318
Thiel M 2011 The evolution of sociality: Peracarid crustaceans as model organisms; in New frontiers in crustacean biology (eds) Asakura et al. (Leiden: Koninkliike Brill NV) pp 285–297
Thornhill R and Alcock J 1983 The evolution of insect mating systems (Harvard University Press)
Toth E and Bauer RT 2007 Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps. Mar. Biol. 151 1875–1886
Wenner AM 1972 Sex ratio as a function of size in marine Crustacea. Ann. Nat. 1O 321–330
Warner RR 1988 Sex change and size-advantage model. Trends Ecol. Evol. 3 133–136
Weeks SC, Posgai RT, Cesari M and Scanabissi F 2005 Androdioecy inferred in the clam shrimp Eulimnadia agassizii. J. Crust. Biol. 25 323–328
Weeks SC, Reed SK, Cesari M and Scanabissi F 2006 Production of intersexes and the evolution of androdioecy in the clam shrimp Eulimnadia texana (Crustacea, Branchiopoda, Spinicaudata). Invert. Reprod. Dev. 49 113–119
Wickler W and Seibt U 1981 Monogamy in crustacean and man. Z. Tierpsychol. 57 215–234
Wilson EO 1971 The insect societies (Cambridge, MA: Belknap Press)
Wilson EO 1975 Sociobiology (Cambridge, MA: Belknap Press)
Wilson EO 2012 The social conquest of earth (New York: Liveright Publishing Corporation)
Yager J 1991 The reproductive biology of two species of remipedes; in Crustacean sexual biology (eds) RT Bauer and JW Martin (New York: Columbia University Press) pp 271–289
Yaldwyn JC 1966 Protandrous hermaphroditism in decapod prawns of the families Hippolytidae and Campylonotidae. Nature 209 1366
Zhang D, Lin J and Creswell RL 1977 Larviculture and effect of food on larval survival and development in the golden coral shrimp Stenopus scutellatus. J. Shellfish Res. 16 367–369
Zhang XG, Siveter DJ, Waloszek D and Maas A 2007 An epipodite bearing crown-group crustaceans from the lower Cambrian. Nature 449 595–598
Zucker N, Cunningham M and Adams HP 1997 Anatomical evidence for androdioecy in the clam shrimp Eulimnadia texana. Hydrobiologia 359 171–175
Zucker N, Stafki B and SC Weeks 2001 Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: relative longevity of males to hermaphrodites. Can. J. Zool. 79 393–401
Zucker N, Aguilar GA, Weeks SC and McCandless LG 2002 Impact of males on variation in reproductive cycle in an androdioecious desert shrimp. Invert. Biol. 121 66–72
Acknowledgements
I am thankful to Indian National Science Academy, New Delhi, for the award of senior Scientist and honorary scientist positions to me. I am also thankful to Dr MA Atmanand, Director NIOT, for providing facility at ANCOST, Port Blair, for my study on caridean shrimps. I thank Ms Padmini for her editorial assistance. I thank the anonymous reviewer for his critical comments which have significantly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: ROBERT M GREENBERG
[Subramoniam T 2013 Origin and occurrence of sexual and mating systems in Crustacea: A progression towards communal living and eusociality. J. Biosci. 38 1–19] DOI
Rights and permissions
About this article
Cite this article
Subramoniam, T. Origin and occurrence of sexual and mating systems in Crustacea: A progression towards communal living and eusociality. J Biosci 38, 951–969 (2013). https://doi.org/10.1007/s12038-013-9392-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-013-9392-x