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Marine Biology

, Volume 116, Issue 3, pp 459–470 | Cite as

Genetic population structure in two tropical sponge-dwelling shrimps that differ in dispersal potential

  • J. E. Duffy
Article

Abstract

The spatial context in which “host races” of parasitic animals originate is a central issue in the controversial theory of sympatric speciation. Sponge-dwelling shrimps in the genus Synalpheus provide a good system for evaluating the possibility of resource-associated divergence in sympatry. I used allozyme electrophoresis to assess the genetic population structure of two Caribbean Synalpheus species sampled in 1988 to 1990 at a hierarchy of spatial scales. S. brooksi Coutière is a host-generalist, using several sponge species in an area, and develops directly, with no planktonic larval stage. G-tests and estimates of FST revealed highly structured populations in this species, with significant differentiation among samples from individual reefs within a region, and strong divergence among regions (Panama, Belize, Florida). Moreover, samples of S. brooksi taken from the two sponges Spheciospongia vesparium (Lamarck) and Agelas clathrodes (Schmidt) in Panama, and separated by ≤3 km, showed significant differentiation at both of the loci that were polymorphic in these populations. Genetic distances between these host-associated populations averaged >60% greater than distances between samples from the same host species and were comparable to, or greater tha, those for some inter-regional comparisons. These genetic data corroborate a previous finding of demographic differences between the same populations. The second species, S. pectiniger Coutière, occurs only in Spheciospongia vesparium, and produces swimming larvae. Although allele frequencies in this species differed significantly among the three regions, S. pectiniger showed no differentiation within regions, and significantly lower differentiation (FST) among regions than its direct-developing congener. These data suggest that genetic population structure in these two commensal crustaceans is related to dispersal potential, and that restricted dispersal may allow the divergence of host-associated populations on a local scale.

Keywords

Sponge Significant Differentiation Genetic Population Structure Strong Divergence Sympatric Speciation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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Literature cited

  1. Banner, D. M., Banner, A. H. (1975). The alpheid shrimp of Australia. Part 2: the genus Synalpheus. Rec. Aust. Mus. 29: 267–389Google Scholar
  2. Brewer, G. J. (1970). Introduction to isozyme techniques. Academic Press, New YorkGoogle Scholar
  3. Bruce, A. J. (1976). Shrimps and prawns of coral reefs, with special reference to commensalism. In: Jones, O. A., Endean, R. (eds.) Biology and geology of coral reefs, Vol. III. Biology 2. Academic Press, New YorkGoogle Scholar
  4. Bruce, A. J. (1978). The evolution and zoogeography of shallow-water tropical shrimps. Inf. Ser. Dep. scient. ind. Res. N.Z. 137: 337–355Google Scholar
  5. Burton, R. S. (1983). Protein polymorphisms and genetic differentiation of marine invertebrate populations. Mar. Biol. Lett. 4: 193–206Google Scholar
  6. Burton, R. S., Feldman, M. W. (1982). Population genetics of coastal and estuarine invertebrates: does larval behavior influence population structure? In: Kennedy, V. S. (ed.) Estuarine comparisons. Academic Press, New York, p. 537–551Google Scholar
  7. Bush, G. L. (1975). Modes of animal speciation. A. Rev. Ecol. Syst. 6: 339–364Google Scholar
  8. Clayton, J. W., Tretiak, D. N. (1972). Amine citrate buffers in starch gel electrophoresis. J. Fish. Res. Bd Can. 29: 1169–1172Google Scholar
  9. Dardeau, M. R. (1984). Synalpheus shrimps (Crustacea: Decapoda: Alpheidae). I. The gambarelloides group, with a description of a new species. Mem. ‘Hourglass’ Cruises 7 (Part 2): 1–125Google Scholar
  10. Dobkin, S. R. (1965). The first post-embryonic stage of Synalpheus brooksi Coutiere. Bull. mar. Sci. 15: 450–462Google Scholar
  11. Dobkin, S. R. (1969). Abbreviated larval development in caridean shrimps and its significance in the artifical culture of these animals. F.A.O. Fish. Rep. 57: 935–946Google Scholar
  12. Duffy, J. E. (1992). Host use patterns and demography in a guild of tropical sponge-dwelling shrimps. Mar. Ecol. Prog. Ser. 90: 127–138Google Scholar
  13. Feder, J. L., Chilcote, C. A., Bush, G. L. (1990a). Regional, local, and microgeographic allele frequency variation between apple and hawthorn populations of Rhagoletis pomonella in western Michigan. Evolution, Lawrence, Kansas 44: 595–608Google Scholar
  14. Feder, J. L., Chilcote, C. A., Bush, G. L. (1990b). The geographic pattern of genetic differentiation between host-associated populations of Rhagoletis pomonella (Diptera: Tephritidae) in the eastern United States and Canada. Evolution, Lawrence, Kansas 44: 570–594Google Scholar
  15. Futuyma, D. J., Mayer, G. C. (1980). Non-allopatric speciation in animals. Syst. Zool. 29: 254–271Google Scholar
  16. Guttman, S. I., Wood, T. K., Karlin, A. A. (1981). Genetic differentiation along host plant lines in the sympatric Enchenopa binotata Say complex (Homoptera: Membracidae). Evolution, Lawrence, Kansas 35: 205–217Google Scholar
  17. Harris, H., Hopkinson, D. A. (1976). Handbook of enzyme electrophoresis in human genetics. American Elsevier, New YorkGoogle Scholar
  18. Hedgecock, D. (1986). Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull. mar. Sci. 39: 550–564Google Scholar
  19. Hedgecock, D., Tracey, M. L., Nelson, K. (1982). Genetics. In: Abele, L. G. (ed.) The biology of Crustacea, Vol. 2. Embryology, morphology, and genetics. Academic Press, New York, p. 283–403Google Scholar
  20. Hochberg, Y. (1988). A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75: 800–802Google Scholar
  21. Jablonski, D., Lutz, R. A. (1983). Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rev. 58: 21–89Google Scholar
  22. Jaenike, J. (1981). Criteria for ascertaining the existence of host races. Am. Nat. 117: 830–834Google Scholar
  23. Katakura, H., Shioi, M., Kira, Y. (1989). Reproductive isolation by host specificity in a pair of phytophagous ladybird beetles. Evolution, Lawrence, Kansas 43: 1045–1053Google Scholar
  24. Knowlton, N. (1986). Cryptic and sibling species among the decapod Crustacea. J. Crust. Biol. (Lawrence, Kansas) 6: 356–363Google Scholar
  25. Knowlton, N., Keller, B. D. (1986). Larvae which fall far short of their potential: highly localized recruitment in an alpheid shrimp with extended larval development. Bull. mar. Sci. 39: 213–223Google Scholar
  26. Lessios, H. A. (1992). Testing electrophoretic data for agreement with Hardy-Weinberg expectations. Mar. Biol. 112: 517–523Google Scholar
  27. Mayr, E. (1963). Animal species and evolution. Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  28. Mitter, C., Farrell, B., Wiegmann, B. (1988). The phylogenetic study of adaptive zones: has phytophagy promoted insect diversification? Am. Nat. 132: 107–128Google Scholar
  29. Palumbi, S. R. (1992). Marine speciation on a small planet. Trends Ecol. Evol. 7: 114–118Google Scholar
  30. Patton, W. K. (1976). Animal associates of living reef corals. In: Jones, O. A., Endean, R. (eds.). Biology and geology of coral reefs, Vol. III. Biology 2. Academic Press, New York, p. 1–43Google Scholar
  31. Pearse, A. S. (1934). Inhabitants of certain sponges at Dry Tortugas. Pap. Tortugas Lab. 28: 119–122Google Scholar
  32. Price, P. W. (1980). Evolutionary biology of parasites. Princeton University Press, Princeton, New JerseyGoogle Scholar
  33. Prokopy, R. J., Diehl, S. R., Cooley, S. S. (1988). Behavioral evidence for host races in Rhagoletis pomonella flies. Oecologia 76: 138–147Google Scholar
  34. Ridgway, G. J., Sherburne, S. W., Lewis R. D. (1970). Polymorphisms in the esterases of Atlantic herring. Trans. Am. Fish. Soc. 99: 147–151Google Scholar
  35. Robertson, D. R. (1987). Responses of two coral reef toadfishes to the demise of their primary prey, the sea urchin. Copeia 1987: 637–642Google Scholar
  36. Sastry, A. N. (1983). Pelagic larval ecology and development. In: Vernberg, F. J., Vernberg, W. B. (eds.) The biology of Crustacea, Vol. 7. Behavior and ecology. Academic Press, New YorkGoogle Scholar
  37. Scheltema, R. S. (1971). Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biol. Bull. mar. biol. Lab., Woods Hole 140: 284–322Google Scholar
  38. Selander, R. K., Smith, M. H., Yang, S. Y., Johnson, W. E., Gentry, J. B. (1971). Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old field mouse (Peromyscus polionotus). Stud. Genet., Austin, Tex. (Univ. Tex. Publ. No. 7103) 4: 49–90Google Scholar
  39. Slatkin, M. (1985). Gene flow in natural populations. A. Rev. Ecol. Syst. 16: 393–430Google Scholar
  40. Smith, D. C. (1988). Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature, Lond. 336: 66–67Google Scholar
  41. Sokal, R. R., Rohlf, F. J. (1981). Biometry. Freeman, San FranciscoGoogle Scholar
  42. Stevens, P. M. (1990). A genetic analysis of the pea crabs (Decapoda: Pinnotheridae) of New Zealand. I. Patterns of spatial and host-associated genetic structuring in Pinnotheres novaezelandiae Filhol. J. exp. mar. Biol. Ecol. 141: 195–212Google Scholar
  43. Strong, D. R., Lawton, J. H., Southwood, R. (1984). Insects on plants. Harvard University Press, CambridgeGoogle Scholar
  44. Swofford, D. L., Selander, R. K. (1981). BIOSYS-1: A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J. Hered. 72: 281–283Google Scholar
  45. Tauber, C. A., Tauber, M. J. (1989). Sympatric speciation in insects: perception and perspective. In: Otte, D., Endler, J. A. (eds.) Speciation and its consequences. Sinauer Associates, Sunderland, Massachusetts, p. 307–344Google Scholar
  46. Waring, G. L., Abrahamson, W. G., Howard, D. J. (1990). Genetic differentiation among host-associated populations of the gall-maker Eurosta solidaginis (Diptera: Tephritidae). Evolution, Lawrence, Kansas 44: 1648–1655Google Scholar
  47. Weir, B. S. (1990). Intraspecific differentiation. In: Hillis, D. M., Moritz, C. (eds.) Molecular systematics. Sinauer Associates, Sunderland, Massachusetts, p. 373–410Google Scholar
  48. Weir, B. S., Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, Lawrence, Kansas 38: 1358–1370Google Scholar
  49. Wood, T. K., Guttman, S. I. (1982). Ecological and behavioral basis for reproductive isolation in the sympatric Enchenopa binotata complex (Homoptera: Membracidae). Evolution, Lawrence, Kansas 36: 233–242Google Scholar
  50. Wood, T. K., Olmstead, K. L., Guttman, S. I. (1990). Insect phenology mediated by host-plant water relations. Evolution, Lawrence, Kansas 44: 629–636Google Scholar
  51. Workman, P. L., Niswander, J. D. (1970). Population studies on southwestern Indian tribes. II. Local genetic differentiation in the Papago. Am. J. Hum. Genet. 22: 24–49Google Scholar
  52. Wright, S. (1978). Evolution and the genetics of populations, Vol. 4. Variability within and among natural populations. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • J. E. Duffy
    • 1
  1. 1.Department of Invertebrate Zoology, National Museum of Natural HistorySmithsonian InstitutionWashington, D.C.USA

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