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The ‘paradox’ of polyembryony: A review of the cases and a hypothesis for its evolution

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Abstract

Animal polyembryony appears to be paradoxical because it clones an unproven genotype at the expense of genetic diversity in a clutch. However, it is employed by at least 18 taxa in six phyla (excluding instances of occasional twinning). Most polyembryony occurs in parasitic stages or in other environments whose quality is not predictable by the mother; in some instances, it compensates for a constraint on zygote number. We predict that polyembryony is likely to evolve when the offspring has more information regarding optimal clutch size than the parents.

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References

  • Arillo, A., Bavestrello, G. and Boero, F. (1989) Circannual cycle and oxygen consumption in Eudendrium glomeratum (Cnidaria, Anthomedusae): Studies on a shallow water population. Marine Ecol. 10, 289–301.

    Google Scholar 

  • Baer, J.G. and Joyeux, C. (1961) Classe des Trématodes. In Traité de Zoologie, IV,I (P. Grassé, ed.), pp. 561–692. Masson, Paris.

    Google Scholar 

  • Baer, J.G. and Euzet, L. (1961) Classe des Monogènes. In Traité de Zoologie, IV,I (P. Grassé, ed.), pp. 241–325. Masson, Paris.

    Google Scholar 

  • Bell, G. (1982) The Masterpiece of Nature. University of California Press, Berkeley, CA.

    Google Scholar 

  • Benazzi, M. and Benazzi Lentati, G. (1993) Platyhelmithes — Turbellaria. In Reproductive Biology of Invertebrates K.G. Adiyodi and R.G. Adiyodi, eds). Vol. VI, Part A, Asexual Propagation and Reproductive Strategies, pp. 107–141. John Wiley, Chichester.

    Google Scholar 

  • Berland, L. (1951) Super-ordre des Hyménoptéroïdes: Reproduction. In Traité de Zoologie, X,I (P. Grassé, ed.), pp. 821–843. Masson, Paris.

    Google Scholar 

  • Berrill, N.J. (1949) Developmental analysis of Scyphomedusae. Biol. Rev. 24, 393–410.

    Google Scholar 

  • Berrill, N.J. (1952) Regeneration and budding in worms. Biol. Rev. 27, 401–438.

    Google Scholar 

  • Bigelow, H.B. (1909) The Medusae. Mem. Mus. Comp. Zool. 37, 9–245.

    Google Scholar 

  • Boero, F. (1994) Bright young people, biodiversity and species lists. Trends Ecol. Evol. 9, 399.

    Google Scholar 

  • Boero, F., Bouillon, J. and Piraino, S. (1992) On the origins and evolution of hydromedusan life cycles (Cnidaria, Hydrozoa). In Sex Origin and Evolution (R. Dallai, ed.), pp. 59–68. Selected Symposia and Monographs U.Z.I. No. 6. Mucchi, Modena.

    Google Scholar 

  • Borg, F. (1926) Studies on recent Cyclostomatous Bryozoa. Zool. Bidrag. Uppsala 10, 181–507.

    Google Scholar 

  • Borg, F. (1933) A revision of the recent Heteroporidae (Bryozoa). Zool. Bidrag. Uppsala 14, 254–394.

    Google Scholar 

  • Bosch, I., Rivkin, R.B. and Alexander, S.P. (1989) Asexual reproduction by oceanic planktotrophic echinoderm larvae. Nature 337, 169–170.

    Google Scholar 

  • Bouillon, J. (1985) Essai de classification des Hydropolyps-Hydromeduses (Hydrozoa-Cnidaria). Indo-Malayan Zool. 1, 29–243.

    Google Scholar 

  • Brien, P. (1960) Classe des Bryozoaires. In Traité de Zoologie, V,II (P. Grassé, ed.), pp. 1053–1379. Masson, Paris.

    Google Scholar 

  • Buchanan, G.D. (1957) Variation in litter size of nine-banded armadillos. J. Mamm. 38, 529.

    Google Scholar 

  • Bulmer, M.G. (1970) The Biology of Twinning in Man. Clarendon Press, Oxford.

    Google Scholar 

  • Calvet, L. (1900) Contributions á l'histoire naturelle des Bryozoaires ectoproctes marins. Trav. Inst. Zool. Univ. Montpellier 8, 1–488.

    Google Scholar 

  • Charnov, E.L., Downhower, J.F. and Brown, L.P. (1995) Optimal offspring size in small litters. Evol. Ecol. 9, 57–63.

    Google Scholar 

  • Craig, S.F., Slobodkin, L.B. and Wray, G. (1995) The ‘paradox’ of polyembryony. Trends Ecol. Evol. 9, 371–372.

    Google Scholar 

  • Cruz, Y.P. (1981) A sterile defender morph in a polyembryonic hymenopterous parasite. Nature 294, 446–477.

    Google Scholar 

  • Cruz, Y.P. (1986) The defender role in the precocious larvae of Copidosomopsis tanytmemus (Encyrtidae, Hymenoptera). J. Exp. Zool. 237, 309–318.

    Google Scholar 

  • Dawydoff, C. (1959) Ontogenese des Annélides. In Traité de Zoologie, V,I (P. Grassé, ed.), pp. 594–686. Masson, Paris.

    Google Scholar 

  • de Beauchamp, P. (1961) Classe des Turbellariés. In Traité de Zoologie, IV,I (P. Grassé, ed.), pp. 35–212. Masson, Paris

    Google Scholar 

  • Esch, G.W. and Fernàndez, J.C. (1993). A Functional Biology of Parasitism. Chapman and Hall, London.

    Google Scholar 

  • Fernandez, M. (1909) Beiträge zur Embryologie der Gürteltiere. 1. Zur Keimblätterinversion und spezifischen Polyembryonie der Mulita (Tatusia hybrida Desm.) Morpholog. Jahrb. 39, 302–333.

    Google Scholar 

  • Fioroni, P. (1987) Allgemeine und vergleichende Embryologie der Tiere: Ein Lehrbuch. Springer-Verlag, Berlin.

    Google Scholar 

  • Galbreath, G.J. (1985) The evolution of monozygotic polyembryony in Dasypus. In The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas (G.G. Montgomery, ed.), pp. 243–246. Smithsonian Institute Press, Washington, DC.

    Google Scholar 

  • Gilbert, S.F. (1991) Developmental Biology, 3rd edn. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Glenner, H. and Høeg, J.T. (1995) A new motile, multicellular stage involved in host invasion by parasitic barnacles (Rhizocephala). Nature 377, 147–150.

    Google Scholar 

  • Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Grbic, M., Ode, P.J. and Strand, M.R. (1992) Sibling rivalry and brood sex ratios in polyembryonic wasps. Nature 360, 254–256.

    Google Scholar 

  • Hague, F.S. (1923) Studies on Sparganophilus eiseni. Smith. Trans. Am. Micr. Soc. 42, 1–42.

    Google Scholar 

  • Haig, D. (1993) Genetic conflicts in human pregnancy. Quart. Rev. Biol. 68, 495–532.

    Google Scholar 

  • Hardy, I.C.W. (1995a) Protagonists of polyembryony. Trends Ecol. Evol. 10, 179–180.

    Google Scholar 

  • Hardy, I.C.W. (1995b) Reply to ‘The “paradox” of polyembryony’. Trends Ecol. Evol. 10, 372.

    Google Scholar 

  • Hardy, I.C.W., Ode, P.J. and Strand, M.R. (1993) Factors influencing brood sex ratios in polyembryonic Hymenoptera. Oecologia 93, 343–348.

    Google Scholar 

  • Harmer, S.F. (1890) On the origin of the embryos in the ovicells of cyclostomatous Polyzoa. Proc. Cambridge Phil. Soc. 7, 48–55.

    Google Scholar 

  • Harmer, S.F. (1893) On the occurrence of embryonic fission in Cyclostomatous Polyzoa. Quart. J. Micr. Soc. 34, 199–241.

    Google Scholar 

  • Harmer, S.F. (1896) On the development of Lichenopora verrucaria Fabr. Quart. J. Micr. Sci. 39, 71–144 (pl. 7–10).

    Google Scholar 

  • Harmer, S.F. (1898) On the development of Tubulipora, and on some British and northern species of this genus. Quart. J. Micr. Sci. New. Ser. 41, 73–157.

    Google Scholar 

  • Hart, M.W. and Strathmann, R.R. (1995) Mechanisms and rates of suspension feeding. In Ecology of Marine Invertebrate Larvae (L.R. McEdwards, ed.), pp. 193–221. CRC Marine Science Series. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Høeg, J.T. (1995) The biology and life cycle of the Rhizocephala (Cirripedia). J. Mar. Biol. Ass. UK 75, 517–550.

    Google Scholar 

  • Hughes, R.N. (1989) A Functional Biology of Clonal Animals. Chapman and Hall, London.

    Google Scholar 

  • Hummon, M.R. and Hummon, W.D. (1993) Gastrotricha. In Reproductive Biology of Invertebrates (K.G. Adiyodi and R.G. Adiyodi, eds), Vol. VI, Part A, Asexual Propagation and Reproductive Strategies. John Wiley, Chichester.

    Google Scholar 

  • Ivanova-Kasas, O.M. (1972) Polyembryony in insects. In Developmental Systems (S.J. Counce and C.H. Waddington, eds), Vol. 1, pp. 243–271. Academic Press, New York.

    Google Scholar 

  • Jaeckle, W.B. (1994) Multiple modes of asexual reproduction by tropical and subtropical sea star larvae: An unusual adaptation for genet dispersal and survival. Biol. Bull. 186, 62–71.

    Google Scholar 

  • Jeannel, R. (1951) Ordre des Strepsiptères. In Traité de Zoologie X,II (P. Grassé, ed.), pp. 1277–1299. Masson, Paris.

    Google Scholar 

  • Katheriner, L. (1904) Ueber die Entwicklung von Gyrodactylus elegans v. Nrdm. Zool. Jahrb. 70, 519–550.

    Google Scholar 

  • Kennedy, J.S. and Stroyan, H.L.G. (1959) Biology of aphids. Ann. Rev. Entomol. 4, 139–160.

    Google Scholar 

  • Kleinenberg, N. (1879) The development of the earthworm Lumbricus trapezoides Dugès. Quart. J. Micr. Sci. 19, 206–244.

    Google Scholar 

  • Koscielski, B. (1973) Polyembryony in Dendrocoelum lacteum O.F. Muller. In Biology of Turbellaria: Experimental Advances (Shapira et al., eds), pp. 103–107. MSS Information Corp., New York.

    Google Scholar 

  • Lack, D. (1947) The significance of clutch size. Ibis 89, 302–352.

    Google Scholar 

  • Levitan, D.R. (1995) The ecology of fertilization in free-spawning invertebrates. In Ecology of Marine Invertebrate Larvae (L.R. McEdwards, ed.), pp. 123–156. CRC Marine Science Series. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Levitan, D.R. and Petersen, C. (1995) Sperm limitation in the sea. Trends Ecol. Evol. 10, 228–231.

    Google Scholar 

  • MacGillivray, I., Nylander, P.P.S. and Corney, G. (1975) Human Multiple Reproduction. W.B. Saunders, Philadelphia, PA.

    Google Scholar 

  • Marchal, P. (1898) Le cycle évolutif de l'Encyrtus fuscicolli. Société Entomologie de France Bull. 1898, 109–111.

    Google Scholar 

  • McLaren, A. (1982) The embryo. In Reproduction in Mammals 2: Embryonic and Fetal Development (C.R. Austin and R.V. Short, eds), pp. 1–25. Cambridge University Press, Cambridge.

    Google Scholar 

  • Moore, J. (1981) Asexual reproduction and environmental predictability in cestodes (Cyclophyllidea, Taeniidae). Evolution 35, 723–741.

    Google Scholar 

  • Mortensen, T.H. (1921) Studies of the Development and Larval Forms of Echinoderms. G.E.C. Gad, Copenhagen.

    Google Scholar 

  • Nénon, J.-P. (1983). La polyembryonie: reproduction par vrais jumeaux (Series Que sais-je?). Presses Universitaires de France, Paris.

    Google Scholar 

  • Newman, H.H. (1913) The natural history of the nine-banded armadillo of Texas. Am. Nat. 47, 513–539.

    Google Scholar 

  • Noble, E.R., Noble, G.A., Schad, G.A. and MacInnes, A.J. (1989) Parasitology: The Biology of Animal Parasites, 6th edn. Lea and Febiger, Philadelphia, PA.

    Google Scholar 

  • Noskiewicz, J. and Poluszynski, G. (1935). Embryologische Untersuchungen an Strepsipteren. II. Teil; Polyembryonie. Zoologica Poloniae, Lwów, 1, 53–94.

    Google Scholar 

  • Nowak, R.M. (1991) Walker's Mammals of the World, 5th edn, Vol. 1, pp. 525–535. Johns Hopkins University Press, Baltimore, MD.

    Google Scholar 

  • Ode, P.J. and Strand, M.R. (1995) Progeny and sex allocation decisions of the polyembryonic wasp Copidosoma floridanum. J. Animal Ecol. 64, 213–224.

    Google Scholar 

  • Parker, H.L. (1931) Macrocentrus gifuensis Ashmead, a polyembryonic braconid parasite of the European Corn Borer. US Department of Agriculture Technical Bulletin 230.

  • Patterson, J.T. (1927) Polyembryony in animals. Quart. Rev. Biol. 2, 399–426.

    Google Scholar 

  • Penners, A. (1924) Doppelbildungen bei Tubifex rivulorum Lam. Zool. Jahrb. 41, 91–120.

    Google Scholar 

  • Raikova, E.V. (1973) Life cycle and systematic position of Polypodium hydriforme Ussov (Coelenterata), a cnidarian parasite of the eggs of Acipenseridae. Publ. Seto Marine Biological Laboratory 20, 165–174.

    Google Scholar 

  • Raikova, E.V. (1980) Morphology, ultrastructure and development of the parasitic larva and its surrounding trophamnion of Polypodium hydriforme Coelenterata. Cell Tissue Res. 206, 487–500.

    Google Scholar 

  • Reed, C.G. (1991) Bryozoa. In Reproduction of Marine Invertebrates. VI. Echinoderms and Lophophorates (A.C. Giese and J.S. Pearse, eds), pp. 85–245. Boxwood Press, Pacific Grove, CA.

    Google Scholar 

  • Robertson, A. (1903) Embryology and embryonic fission in the genus Crisia. Univ. Calif. (Berkeley) Publ. Zool. 1, 115–156.

    Google Scholar 

  • Ryland, J.S. (1970) Bryozoans. Hutchinson, London.

    Google Scholar 

  • Ryland, J.S. (1996) Polyembryony ‘paradox’: The case of cyclostomate Bryozoa. Trends Ecol. Evol. 11, 26.

    Google Scholar 

  • Shostak, S. (1993) Cnidaria. In Reproductive Biology of Invertebrates (K.G. Adiyodi and R.G. Adiyodi, eds), Vol. VI, Part A, Asexual Propagation and Reproductive Strategies, pp. 45–105. John Wiley, Chichester.

    Google Scholar 

  • Silvestri, F. (1906) Contribuzioni alla conoscenza biologica degli imenotteri parasiti. I. Biologia del Litomastix truncatellus (Dalm.) Bolletino del Laboratorio di Zoologia generale e agraria della P. Scuolo Superiore d'Agricoltura, Porciti 1, 17–64.

    Google Scholar 

  • Slifer, E.H. and Shulow, A. (1947) Sporadic polyembryony in grasshopper eggs. Ann. Ent. Soc. Am. 40, 652–655.

    Google Scholar 

  • Slobodkin, L.B. (1954) Population dynamics in Daphnia obtusa Kurz. Ecol. Monogr. 24, 69–88.

    Google Scholar 

  • Slobodkin, L.B. (1980) Growth and Regulation of Animal Populations, 2nd edn. Dover Publications, New York.

    Google Scholar 

  • Slobodkin, L.B. and Bossert, P.E. (1991) The freshwater cnidaria-or coelenterates. In Ecology and Classification of North American Freshwater Invertebrates (J.H. Thorp and A.P. Covich, eds), pp. 125–142. Academic Press, New York.

    Google Scholar 

  • Storrs, E.E. (1967) Individuality in monozygotic quadruplets of the armadillo, Dasypus novemcinctus. PhD Dissertation, University of Texas.

  • Strand, M.R. (1989a) Development of the polyembryonic parasitoid Copidosoma floridanum in Trichoplusia ni. Entomologia Experimentalis et Applicata 50, 37–46.

    Google Scholar 

  • Strand, M.R. (1989b) Oviposition behavior and progeny allocation of the polyembryonic wasp Copidosoma floridanum (Hymenoptera: Encyrtidae). J. Insect Behav. 2, 355–369.

    Google Scholar 

  • Strand, M.R. (1989c) Clutch size, sex ratio, and mating by the polyembryonic encyrtid Copidosoma floridanum. Florida Entomologist 72, 32–42.

    Google Scholar 

  • Strand, M.R., Johnson, J.A. and Dover, B.A. (1990) Ecdysteroid and juvenile hormone esterase profiles of Trichoplusia ni parasitized by the polyembryonic wasp Copidosoma floridanum. Arch. Insect Biochem. Physiol. 13, 41–51.

    Google Scholar 

  • Strand, M.R., Baehrecke, E.H. and Wong, E.A. (1991a) The role of host endocrine factors in the development of polyembryonic parasitoids. Biological Control 1, 144–152.

    Google Scholar 

  • Strand, M.R., Goodman, W.G. and Baehrecke, E.H. (1991b) The juvenile hormone titer of Trichoplusia ni and its potential role in embryogenesis of the polyembryonic wasp Copidosoma floridanum. Insect Biochem. 21, 205–214.

    Google Scholar 

  • Strathmann, R.R. (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Ann. Rev. Ecol. Syst. 16, 339–361.

    Google Scholar 

  • von Jhering, H. (1885) Über die Fortpflanzung der Gürtelthiere. Sitzungsberichte d. Koenigl. Preuss. Akad. d. Wissenschaften zu Berlin 1885, 1051–1053.

    Google Scholar 

  • von Jhering, H. (1886) Ueber ‘Generationswechsel’ bei Säugethieren. Archiv für Anat. u. Physiol., Physiol. Abthlg. 1886, 433–450.

    Google Scholar 

  • Voukassovitch, P. (1927) Observations biologiques sur le Macrocentrotus abdominalis Fab.; braconide parasite. Compte Rendu des Seances de la Societe de Biologie 96, 379–381.

    Google Scholar 

  • Welch, P.S. (1921) Bifurcation in the embryos of Tubifex. Biol. Bull. 14, 188–202.

    Google Scholar 

  • Wetzel, R.M. (1985) Taxonomy and distribution of armadillos, Dasypodidae. In The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas (G.G. Montgomery, ed.), pp. 23–46. Smithsonian Institute Press, Washington, DC.

    Google Scholar 

  • Willadsen, S.M. (1979) A method for culture of micromanipulated sheep embryos and its use to produce monozygotic twins. Nature 277, 298–300.

    Google Scholar 

  • Williams, G.C. (1966) Adaptation and Natural Selection. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Williams, G.C. (1975) Sex and Evolution. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Wray, G.A. and Raff, R.A. (1991) The evolution of developmental strategy in marine invertebrates. Trends Ecol. Evol. 6, 45–50.

    Google Scholar 

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  1. Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794–5245, USA

    SEAN F. Craig

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  1. SEAN F. Craig
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  2. LAWRENCE B. Slobodkin
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  3. GREGORY A. Wray
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  4. CHRISTIANE H. Biermann
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Craig, S.F., Slobodkin, L.B., Wray, G.A. et al. The ‘paradox’ of polyembryony: A review of the cases and a hypothesis for its evolution. Evolutionary Ecology 11, 127–143 (1997). https://doi.org/10.1023/A:1018443714917

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