Marine Biology

, Volume 107, Issue 2, pp 205–213 | Cite as

Divergence between populations of a monogamous polychaete with male parental care: Premating isolation and chromosome variation

  • J. R. Weinberg
  • V. R. Starczak
  • C. Mueller
  • G. C. Pesch
  • S. M. Lindsay
Article
Accepted:

Abstract

Low dispersal and sexual selection are characteristic of the coastal polychaeteNereis acuminata Ehlers 1868 [also known asNereis arenaceodentata Moore 1903 andNereis (Neanthes) caudata Delle Chiaje 1841]. We assessed levels of premating isolation between populations of this polychaete. Four North American populations were used, two from the Atlantic and two from the Pacific. Worms from all sites (1) were collected in 1987 and 1988 from the same habitat type, (2) were morphologically similar and keyed out asN. acuminata, and (3) reproduced monogamously and exhibited male parental care, an extremely rare reproductive mode in marine invertebrates. There was no evidence from 10-min or 36-h trials of premating isolation between the two Pacific populations. Incomplete premating isolation was found between the two Atlantic populations. High aggression and non-pairing occurred in some 10-min trials between males and females. However, in 36-h trials males and females from the two Atlantic populations always paired to mate. Complete premating isolation was found between Atlantic and Pacific populations. During 10-min trials, males and females from different oceans often attacked and then avoided each other, and they never paired to mate. Nor did they pair to mate in longer, 36-h trials. One Pacific and one Atlantic population were compared for tolerance to cold temperature. Pacific individuals were less able to tolerate cold water than Atlantic individuals. Two Atlantic populations studied had karyotypes with 11 pairs of small acrocentric chromosomes (2n=22), while the two Pacific populations had nine pairs of large metacentric or submetacentric chromosomes (2n=18). Such extreme dissimilarity in karyotype was not expected considering the similarity in morphology, habitat, and reproductive mode. Results suggest strongly that the Atlantic and Pacific populations have been allopatric for a long time, and are different species.

Keywords

Habitat Type Sexual Selection Polychaete Marine Invertebrate Reproductive Mode 
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.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Agresti, A. (1984). Analysis of ordinal categorical data. John Wiley & Sons, New YorkGoogle Scholar
  2. Ahearn, J. N. (1980). Evolution of behavioral reproductive isolation in a laboratory stock ofDrosophila silvestris. Experientia 36: 63–64Google Scholar
  3. Akesson, B. (1977). Crossbreeding and geographic races: Experiments with the polychaete genusOphryotrocha. Mikrofauna Meeresbod. 61: 11–18Google Scholar
  4. Akesson, B. (1984). Speciation in the genusOphryotrocha (Polychaeta, Dorvilleidae). In: Fischer, A., Pfannenstiel, H.-D. (eds.) Polychaete reproduction. Fortschritte der Zoologie, Band 29. Fischer-Verlag, Stuttgart/New York, p. 299–316Google Scholar
  5. Ament, A. S. (1978). Geographic variation in relation to life history in three species of the marine gastropod genusCrepidula. Ph. D. Thesis, Univ. Pennsylvania, Philadelphia, PennsylvaniaGoogle Scholar
  6. Bailey-Brock, J. H. (1984). Ecology of the tube-building polychaeteDiopatra leuckarti Kinberg, 1865 (Onuphidae) in Hawaii: community structure, and sediment stabilizing properties. Zool. J. Linn. Soc. 80: 191–199Google Scholar
  7. Barnard, J. L. Reish, D (1959). Ecology of Amphipoda and Polychaeta of Newport Bay, California. Occ. Pap. Allan Hancock Fdn 21: 1–106Google Scholar
  8. Berger, E. M. (1973). Gene-enzyme variation in three sympatric species ofLittorina. Biol. Bull. mar. biol. Lab., Woods Hole 145: 83–90Google Scholar
  9. Berger, E. M. (1977). Gene-enzyme variation three sympatric species ofLittorina. II. The Roscoff population, with a note on the origin of North AmericanL. littorea. Biol. Bull. mar. biol. Lab., Woods Hole 153: 255–264Google Scholar
  10. Berkeley E, Berkeley, C. (1953).Micronereis nanaimonensis n. sp.: with some notes on its life history. J. Fish. Res. Bd Can. 10: 85–95Google Scholar
  11. Boilly-Marer, Y., Lassalle, B. (1980). Electrophysiological responses of the central nervous system in the presence of homospecific and heterospecific sex pheromones inNereis (Annelida Polychaeta). J. exp. Zool. 213: 33–39Google Scholar
  12. Boilly-Marer, Y., Lhomme, M. F. (1986). Sex pheromones in the marine annelidPlatynereis dumerilii Aud. and M. Edw. In: Porches, M., Andries, J.C., Dhainaut, A. (eds.) Advances in invertebrate reproduction, 4. Elsevier, AmsterdamGoogle Scholar
  13. Borowsky, B. (1984). Effects of receptive females' secretions on some male reproductive behaviors in the amphipod crustaceanMicrodeutopus gryllotalpa. Mar. Biol. 84: 183–187Google Scholar
  14. Cardé, R. T. (1986). The role of pheromones in reproductive isolation and speciation of insects. In: Huettel, M. D. (ed.) Evolutionary genetics of invertebrate behavior. Plenum Press, New YorkGoogle Scholar
  15. Carillo, E. B.-G., Miller, C. B., Wiebe, P. H. (1974). Failure of interbreeding between Atlantic and Pacific populations of the marine Calanoid CopepodAcartia clausi Giesbrecht. Limnol. Oceanogr. 19: 452–458Google Scholar
  16. Carlton, J. T. (1985). Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr. mar. Biol. A. Rev. 23: 313–371Google Scholar
  17. Carlton, J. T. (1987). Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bull. mar. Sci. 41(2): 452–465Google Scholar
  18. Christensen, B. (1980). Animal cytogenetics. In: John, B., Bauer, H., Kayano, H., Levan, A., White, M. (eds.) Vol. 2: Annelida. Gebrüder Borntraeger, Berlin, StuttgartGoogle Scholar
  19. Clark, R. B. (1959). The tubicolous habit and the fighting reactions of the polychaeteNereis pelagica. Anim. Behav. 7: 85–90Google Scholar
  20. Clark, R. B. (1961). The origin and formation of the heteronereis. Biol. Rev. 36: 199–236Google Scholar
  21. Clark, R. B. (1977). Reproduction, speciation and polychaete taxonomy. In: Reish, D. J., Fauchald, K. (eds.) Essays on polychaetous annelids in memory of Dr Olga Hartman. Allan Hancock Foundation, Univ. So. California, Los Angeles, CaliforniaGoogle Scholar
  22. Coyne, J. A., Orr, H. A. (1989). Patterns of speciation inDrosophila. Evolution 43: 362–381Google Scholar
  23. Cram, A., Evans, S. M. (1980). Stability and lability in the evolution of behaviour in nereid polychaetes. Anim. Behav. 28: 483–490Google Scholar
  24. Darwin, C. (1874). The descent of man, and selection in relation to sex, 2nd ed. John Murray, LondonGoogle Scholar
  25. Dauer, D. M., Ewing, R. M., Sourbeer, J. W., Harlan, W. T., Stokes, T. L. (1982). Nocturnal movements of the macrobenthos of the Layfayette River, Virginia. Int. Revue ges. Hydrobiol. 67: 761–775Google Scholar
  26. Dawley, E. M. (1987). Species discrimination between hybridizing and non-hybridizing terrestrial salamanders. Copeia 4: 924–931Google Scholar
  27. Day, J. (1973). New Polychaeta from Beaufort, with a key to all species recorded from North Carolina. NOAA Tech. Report NMFS, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Washington, DC, circ-375Google Scholar
  28. Dennert, H. G., Dennert, A. L., Kant, P., Pinkster, S., Stock, J. H. (1969). Upstream and downstream migrations in relation to the reproductive cycle and to environmental factors in the amphipod,Gammarus zaddachi. Bijdr. Dierk. 39: 11–43Google Scholar
  29. Devaney, D., Eldredge, L. G. (eds) (1987). Reef and shore fauna of Hawaii. Section 2: Platyhelminthes through Phoronida, Section 3: Sipuncula through Annelida. Bishop Museum Special Publication 64(2&3). Bishop Museum Press, Honolulu, HawaiiGoogle Scholar
  30. Dobzhansky, T. (1940). Speciation as a stage in evolutionary divergence. Amer Nat. 74: 312–321Google Scholar
  31. Ehlers, E. (1868). Die Borstenwurmer (Annelida, Chaetopoda) nach systematischen und anatomischen Untersuchungen dargestellt. Part 2. Wilhelm Engelmann, Leipzig, p. 269–748Google Scholar
  32. Evans, S. M. (1971). Behavior in polychaetes. Q. Rev. Biol. 46: 379–405Google Scholar
  33. Fauvel, P. (1923). Polychètes Errantes. Faune de France, 5. Federation Francaise de Sociétés de Sciences Naturelles, ParisGoogle Scholar
  34. Fisher, R. A. (1930). The genetical theory of natural selection. Oxford Univ. Press, OxfordGoogle Scholar
  35. Grassle, J. P., Gelfman, C. E., Mills, S. W. (1987). Karyotypes ofCapitella sibling species, and of several species in the related generaCapitellides andCapitomastus (Polychaeta). Bull. biol. Soc. Wash. 7: 77–88Google Scholar
  36. Grassle, J. P., Grassle, J. F. (1976). Sibling species in the marine pollution indicatorCapitella (Polychaeta). Science, N.Y. 192: 567–569Google Scholar
  37. Green, R. H., Hobson, K. D. (1970). Spatial and temporal variation in a temperate intertidal community, with special emphasis onGemma gemma (Pelecypoda: Mollusca). Ecology 51: 999–1011Google Scholar
  38. Guérin, J. P., Kerambrun, P. (1984). Role of reproductive characters in the taxonomy of spionids and elements of speciation in the “Malacoceros fuliginosus complex”. In: Fischer, A., Pfannenstiel, H.-D. (eds.) Polychaete reproduction. Fortschritte der Zoologie, Band 29. Fischer, Stuttgart/New York, p. 317–333Google Scholar
  39. Herpin, R (1923). Éthologie et développement deNereis (Neanthes) caudata delle Chiaje. C.r. hebd. Séanc. Acad. Sci., Paris 177: 542–544Google Scholar
  40. Herpin, R. (1926). Recherches biologiques sur la reproduction et le développement de quelques annélids polychètes. Soc. Sci. l'ouest Fr., Nantes, Bull. Ser. 4.5: 1–250Google Scholar
  41. Highsmith, R. C. (1985). Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Mar. Ecol. Prog. Ser. 25: 169–179Google Scholar
  42. Hilbish, T. J. (1985). Demographic and temporal structure of an allele frequency cline in the musselMytilus edulis. Mar. Biol. 86: 163–171Google Scholar
  43. Ibarzábal, D. (1986). Poliquetos de Punta del Este, Isla de la Juventud. 1. Familias Nereidae, Glyceridae, y Goniadidae, Poeyana Inst. biol. Mabuna (Ser. B) 309: 1–16Google Scholar
  44. Janson, K. (1987). Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol. J. Linn. Soc. 30: 245–256Google Scholar
  45. Kimura, M., Weiss, G. H. (1964). The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49: 561–576Google Scholar
  46. Kirkpatrick, M. (1982). Sexual selection and the evolution of female choice. Evolution 36: 1–12Google Scholar
  47. Kligerman, A.D., Bloom, S.E. (1977). Rapid chromosome preparation from solid tissues of fishes. J. Fish. Res. Bd Can. 34: 266–269Google Scholar
  48. 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
  49. Koehn, R. K. (1983). The biochemical and physiological bases of aminopeptidase-1 (Lap) polymorphism inMytilus edulis. In: King, C. E., Dawson, P.S. (eds.) Population biology: retrospect and prospect. Columbia Univ. Press, New YorkGoogle Scholar
  50. Koehn, R. K., Hall, J. G., Innis, D. J., Zera, A. J. (1984). Genetic differentiation ofMytilus edulis in eastern North America. Mar. Biol. 79: 117–126Google Scholar
  51. Kristensen, E. (1988). Factors influencing the distribution of nereid polychaetes in Danish coastal waters. Ophelia 29: 127–140Google Scholar
  52. Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78: 3721–3725Google Scholar
  53. Lande, R. (1982). Rapid origin of sexual isolation and character divergence in a cline. Evolution 36: 213–223Google Scholar
  54. Lessios, H. A. (1984). Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution 38: 1144–1148Google Scholar
  55. Mayr, E. (1963). Animal species and evolution. Belknap Press, Harvard Univ. Press, Cambridge, MAGoogle Scholar
  56. McGurk, D. J., Frost, J., Eisenbraun, E., Vick, K., Drew, W. A., Young, J. (1966). Volatile compounds in ants: identification of 4-methyl-3-heptanone from Pogonomyrmex ants. J. Insect. Physiol. 12: 1435–1441Google Scholar
  57. McLain, D. K., Rai, K. S., Rao, P. N. (1985). Ethological divergence in allopatry and asymmetrical isolation in the South PacificAedes scutellaris subgroup. Evolution 39: 998–1108Google Scholar
  58. Moore, J. P. (1903). Descriptions of two new species of polychaeta from Woods Hole, Massachusetts. Proc. Acad. Nat. Sci. USA 55: 720–726Google Scholar
  59. Nelson, W. G. (1986). Benthic infaunal sampling in vicinity of Sand Island Ocean Outfall, O'Ahu, Hawaii. Special Report 6: 20: 86. Water Resources Research Center, Univ. Hawaii at Manoa, Honolulu, HawaiiGoogle Scholar
  60. Paterson, H. E. H. (1985). The recognition concept of species. In: Vrba, E.S. (ed.) Species and speciation. Transvaal Museum Monograph No. 4, Pretoria, South AfricaGoogle Scholar
  61. Pesch, G. G., Pesch, C. E. (1980). Chromosome complement of the marine wormNeanthes arenaceodentata (Polychaeta: Annelida). Can J. Fish quat. Sciences 37: 286–288Google Scholar
  62. Pesch, G. G., Pesch, C. E., Mueller, C. (1988). Chromosome complements from two populations of the marine wormNeanthes arenaceodentata (Annelida: Polychaeta). Ophelia 28: 163–167Google Scholar
  63. Pettibone, M. H. (1963). Marine polychaete worms of the New England Region. 1. Aphroditidae through Trochochaetidae. Smithsonian Inst. Bull. 227, part 1, Washington, DCGoogle Scholar
  64. Phelan, P. L., Baker, T. C. (1987). Evolution of male pheromones in moths: reproductive isolation through sexual selection? Science, N.Y. 235: 205–207Google Scholar
  65. Read, G. B. (1980). A new species ofNereis (Polychaeta: Nereididae) from Wellington, New Zealand, Rock Shores. J. R. Soc. N.Z. 10: 185–193Google Scholar
  66. Reish, D. J. (1957). The life history of the polychaete annelidNeanthes caudata (delle Chiaje) including a summary of development in the family Nereidae. Pacif. Sci. 11: 216–228Google Scholar
  67. Reish, D. J. (1963). A quantitative study of the benthic polychaetous annelids of Bahia de San Quintin, Baja California. Pacif. Nat. 3: 399–436Google Scholar
  68. Reish, D. J. (1968). The polychaetous Annelids of the Marshall Islands. Pacif. Sci. 22: 208–231Google Scholar
  69. Reish, D. J., Alosi, M.C. (1968). Aggressive behavior in the polychaetous annelid family Nereidae. Bull. South. Calif. Acad. Sci. 67: 21–28Google Scholar
  70. Rice, S. A., Simon, J. L. (1980). Intraspecific variation in the pollution indicator polychaetePolydora ligni (Spionidae). Ophelia 19: 79–115Google Scholar
  71. Ridley, M. 1978. Paternal care. Anim. Behav. 26: 904–932Google Scholar
  72. Roe, P. 1975. Aspects of life history and of territorial behavior in young individuals ofPlatynereis bicanaliculata andNereis vexillosa (Annelida, Polychaeta). Pacif. Sci. 29: 341–348Google Scholar
  73. Rubinoff, R. W., Rubinoff I. (1971). Geographic and reproductive isolation in Atlantic and Pacific populations of PanamanianBathygobius. Evolution 25: 88–97Google Scholar
  74. Snyder, T. P., Gooch, J. L. (1973). Genetic differentiation inLittorina saxatilis (Gastropoda). Mar. Biol. 22: 177–182Google Scholar
  75. Solignac, M. (1981). Isolating mechanisms and modalities of speciation in theJaera albifrons species complex (Crustacea, Isopoda). Syst. Zool. 30: 387–405Google Scholar
  76. Starczak, V. R. (1984). Sexual selection and intrasexual aggression in the marine polychaeteNereis (Neanthes) acuminata. Ph.D. thesis, Univ. of Connecticut, Storrs, ConnecticutGoogle Scholar
  77. Todd, C. D., Havenhand, J. N., Thorpe, J. P. (1988). Genetic differentiation, pelagic larval transport and gene flow between local populations of the intertidal marine molluscAdalaria proxima (Alder & Hancock). Funct. Ecol. 2: 441–451Google Scholar
  78. Trivers, R. L. (1978). Parental investment and sexual selection. In: Clutton-Brock, T. H., Harvey, P. H. (eds.) Reading in sociobiology. Freeman, San FranciscoGoogle Scholar
  79. Uebelacker, J. M., Johnson, P. G. (eds.) (1984). Taxonomic guide to the polychaetes of the northern Gulf of Mexico. Final report to minerals management Service, 7 vols. Alabama, Vittor, B. A. and AssocGoogle Scholar
  80. Volkman, B. (1977). Geographic and reproductive isolation in the genusTisbe (Copepoda, Harpacticoida). Mikrofauna Meeresbod. 61: 313–314Google Scholar
  81. Weinberg, J. R., Starczak, V. R. (1988). Morphological differences and low dispersal between local populations of the tropical beach isopodExcirolana braziliensis. Bull. mar. Sci. 42: 296–309Google Scholar
  82. Weinberg, J. R., Starczak, V. R. (1989). Morphological divergence of Eastern Pacific and Caribbean isopods: effects of a land barrier and the Panama Canal. Mar. Biol. 103: 143–152Google Scholar
  83. West-Eberhard, M. J. (1983). Sexual selection, social competition, and speciation. Q. Rev. Biol. 58: 155–183Google Scholar
  84. Wilson, E. O. (1975). Sociobiology. Belknap Press, Cambridge, MAGoogle Scholar
  85. Wright, S. (1943). Isolation by distance. Genetics 28: 114–138Google Scholar
  86. Zeeck, E., Hardege, J., Bartels-Hardege, H., Wesselmann, G. (1988). Sex pheromone in a marine polychaete: determination of the chemical structure. J. exp. Zool. 246: 285–292Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • J. R. Weinberg
    • 1
  • V. R. Starczak
    • 1
  • C. Mueller
    • 2
  • G. C. Pesch
    • 2
  • S. M. Lindsay
    • 3
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.U.S. Environmental Protection AgencyNarrangansettUSA
  3. 3.Department of Biological SciencesUniversity of South CarolinaColumbiaUSA

Personalised recommendations