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The Evolution of Allorecognition Specificity

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Part of the book series: Bodega Marine Laboratory Marine Science Series ((BMSS))

Abstract

Intraspecific aggression between clonal cnidarians is not random with respect to genotype; instead, agonistic behavior is modified according to the relatedness of contestants such that clonemates and close relatives behave passively, whereas more distant relatives behave aggressively. Aggression is often costly, with contestants suffering injury and losing space for attachment and growth. Similarly, intraspecific somatic fusion in many sponges, cnidarians, bryozoans, and ascidians is limited to interactions between close relatives and is thought to carry substantial fitness costs.

Such behavioral restriction requires the existence of both an allorecognition system and a set of cues that provides specific labels or relatedness. Several studies suggest that labels of identity (allotypes) are provided by one, or a few loci. Individual specificity therefore requires that the loci conferring allotypic specificity carry high levels of allelic variation. In the case of aggression, allotypic specificity directs aggression away from clonemates and close kin, and toward more distant relatives. In the context of fusion, allotypic specificity limits the potential for intraspecific fusion and its attendant costs.

Taken together, these considerations impiy that rare allorecognition alleles, and the labels of individuality that they confer, should be favored by natural selection. However, the mechanistic models of aggression analyzed in this paper show that the individual costs and benefits of aggression alone will not favor the accumulation and maintenance of allotypic specificity. In contrast, allotypic polymorphism can be maintained directly by the individual costs and benefits of fusion provided fusion carries a net fitness cost. This raises the question of how fusion conditioned on relatedness can be evolutionarily stable. Our results suggest that selection acting at the level of clonal or kin-aggregations, rather than at the level of the individual, may provide an explanation for the evolution of allotypic specificity through aggression or fusion.

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References

  • Ayre, D. J. 1983. The effects of asexual reproduction and intergenotypic aggression on the genotypic structure of populations of the sea anemone Actinia tenebrosa. Oecologia 57: 158–165.

    Article  Google Scholar 

  • Ayre, D. J. 1987. The formation of clones in experimental populations of the sea anemone Actinia tenebrosa. Biol. Bull. 172: 178–186.

    Article  Google Scholar 

  • Bodmer, W. F. 1972. Evolutionary significance of the HL-A system. Nature 237: 139–145.

    Article  PubMed  CAS  Google Scholar 

  • Burnet, F. M. 1973. Multiple polymorphism in relation to histocompatibility antigens. Nature 245: 359–361.

    Article  PubMed  CAS  Google Scholar 

  • Buss, L. W. 1982. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl. Acad. Sci. USA 79: 5337–5341.

    Article  PubMed  CAS  Google Scholar 

  • Buss, L. W., C. S. McFadden and D. R. Keene. 1984. Biology of hydractiniid hydroids. 2. Histocompatibility effector system mediated by nematocyst discharge. Biol. Bull. 167: 139–158.

    Article  Google Scholar 

  • Crozier, R. H. 1986. Genetic clonal recognition abilities in marine invertebrates must be maintained by selection for something else. Evolution 40: 1100–1101.

    Article  Google Scholar 

  • Francis, L. 1973a. Intraspecific aggression and its effect on the distribution of Anthopleura elegantissima. Biol. Bull. 144: 73–92.

    Article  Google Scholar 

  • Francis, L. 1973b. Clone specific segregegation in the sea anemone Anthopleura elegantissima. Biol. Bull. 144: 64–72.

    Article  Google Scholar 

  • Francis, L. 1976. Social organization within clones of the sea anemone Anthopleura elegantissima. Biol. Bull. 150: 361–376.

    Article  Google Scholar 

  • Fujii, H. 1987. The predominance of clones in populations of the sea anemone Anthopleura asiatica (Uchida). BioL Bull. 172: 202–211.

    Article  Google Scholar 

  • Grafen, A. 1979. The hawk-dove game played between relatives. Anim. Behay. 27: 905–907.

    Article  Google Scholar 

  • Grosberg, R. K. 1987. Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri. Evolution 41: 372–384.

    Google Scholar 

  • Grosberg, R. K. 1988. The evolution of allorecognition specificity: in clonal invertebrates. Q. Rev. Biol. (In press).

    Google Scholar 

  • Grosberg, R. K. and J. F. Quinn. 1986. The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322: 456–459.

    Article  Google Scholar 

  • Hamilton, W. D. 1982. Pathogens as causes of genetic diversity in their host populations. p. 269–296. In: Population Biology of Infectious Diseases, R. M. Anderson and R. M. May (eds.). Springer-Verlag, Berlin.

    Google Scholar 

  • Hildemann, W. H., C. H. Bigger and I. S. Johnston. 1979. Histocompatibility reactions and allogeneic polymorphism among invertebrates. Transplant. Proc. 11: 1136–1142.

    PubMed  CAS  Google Scholar 

  • Hildemann, W. H., P. L. Jokiel, C. H. Bigger and I. S. Johnston. 1980. Allogeneic polymorphism and alloimmune memory in the coral Montipora verrucosa. Transplantation 30: 297–301.

    CAS  Google Scholar 

  • Ivker, F. B. 1972. A hierarchy of histo-incompatibility in Hydractinia echinata. Biol. Bull. 143: 162–174.

    Article  Google Scholar 

  • Jackson, J. B. C. 1985. Distribution and ecology of clonal and aclonal benthic invertebrates. p. 297–356. In: Population Biology and Evolution of Clonal Organisms, J. B. C. Jackson, L. W. Buss and R. E. Cook (eds.). Yale University Press, New Haven.

    Google Scholar 

  • Jackson, J. B. C. 1986. Modes of dispersal of clonal epibenthic invertebrates: consequences for species’ distribution and genetic structure of local populations. Bull. Mar. Sci. 39: 588–606.

    Google Scholar 

  • Levin, B. R. 1986. Restriction-modification immunity and the maintenance of genetic diversity in bacterial populations. p. 669–688. In: Evolutionary Processes and Theory, S. Karlin and E. Nevo (eds.). Academic Press, New York.

    Google Scholar 

  • Mirmirani, M. and G. Oster. 1978. Competition, kin selection, and evolutionary [sic] stable strategies. Theoret. PopuL Biol. 13: 304–339.

    Article  CAS  Google Scholar 

  • Neigel, J. E. and J. C. Avise. 1983a. Histocompatibility bioassays of population structure in marine sponges. J. Heredity 74: 134–140.

    Google Scholar 

  • Neigel, J. E. and J. C. Avise. 1983b. Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation. Evolution 37: 437–453.

    Article  Google Scholar 

  • Oka, H. 1970. Colony specificity in compound ascidians. p. 195–206. In: Profiles of Japanese Science and Scientists, H. Yukawa (ed.). Kodansha, Tokyo.

    Google Scholar 

  • Oka, H. and H. Watanabe. 1957. Colony-specificity in compound ascidians as tested by fusion experiments. Proc. Jpn. Acad. 33: 657–659.

    Google Scholar 

  • Oka, H. and H. Watanabe. 1960. Problems of colony specificity in compound ascidians. Bull. Mar. Biol. Stn. Asamushi 10: 153–155.

    Google Scholar 

  • Olson, R. R. 1985. The consequences of short-distance larval dispersal in a sessile marine invertebrate. Ecology 66: 30–39.

    Article  Google Scholar 

  • Rinkevich, B. and I. L. Weissman. 1987. The fate of Botryllus (Ascidiacea) larvae cosettled with parental colonies: beneficial or deleterious consequences? Biol Bull. 173: 474–488.

    Article  Google Scholar 

  • Sabbadin, A. 1962. Le basi genetiche della capcitâ di fusione fra colonie in Botryllus schlosseri (Ascidiacea). Rend. Accad. Lincei 32: 1031–1035.

    Google Scholar 

  • Sabbadin, A. 1982. Formal genetics of ascidians. Am. Zool. 22: 765–773.

    Google Scholar 

  • Scofield, V. L., J. M. Schlumpberger, L. A. West and I. L. Weissman. 1982. Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295: 499–502.

    Article  PubMed  CAS  Google Scholar 

  • Sebens, K. P. 1982a. Recruitment and habitat selection in the intertidal sea anemone Anthopleura elegantissima (Brandt) and A. xanthogrammica (Brandt). J. Exp. Mar. Biot. Ecol. 59: 103–124.

    Article  Google Scholar 

  • Sebens, K. P. 1982b. Asexual reproduction in Anthopleura elegantissima (Anthozoa: Actiniaria): seasonality and spatial extent of clones. Ecology 63: 434–444.

    Article  Google Scholar 

  • Tanaka, K. 1975. Allogeneic distinction in Botryllus primigenus and in other colonial ascidians. p. 115–124. In: Immunologic Phylogeny, W. H. Hildemann and A. A. Benedict (eds.). Plenum Press, New York.

    Google Scholar 

  • Van de Vyver, G. 1970. La non-confluence intraspécifique chez les spongiares et al notion d’individu. Ann. Embryol. Morphog. 3: 251–262.

    Google Scholar 

  • von Hauenschild, C. 1954. Genetische und entwicklungsphysiologische Untersuchungen über Intersexualität und Gewebeverträglichkeit bei Hydractinia echinata Flemm. (Hydroz. Bougainvill.). Wilhelm Roux’s Arch. Develop. Biol. 147:1–41.

    Article  Google Scholar 

  • von Hauenschild, C. 1956. Über die Vererbung einer GewebeverträglichkeitsEigenschaft bei dem Hydroidpolypen Hydractinia echinata. Z. Naturforsch. 116: 132–138.

    Google Scholar 

  • Wakeland, E. K. and J. H. Nadeau. 1980. Immune responsiveness and polymorphism of the major histocompatibility complex: an interpretation. p. 149–156. In: Strategies of Immune Regulation, E. Sercarz and A. J. Cunningham (eds.). Academic Press, New York.

    Google Scholar 

  • Wulff, J. L. 1986. Variation in clone structure of fragmenting coral reef sponges. Biol. J. Linn. Soc. 27: 311–330.

    Article  Google Scholar 

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© 1988 Plenum Press, New York

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Grosberg, R.K., Quinn, J.F. (1988). The Evolution of Allorecognition Specificity. In: Grosberg, R.K., Hedgecock, D., Nelson, K. (eds) Invertebrate Historecognition. Bodega Marine Laboratory Marine Science Series. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-1053-2_12

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  • DOI: https://doi.org/10.1007/978-1-4613-1053-2_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8311-9

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