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.
Similar content being viewed by others
Literature cited
Agresti, A. (1984). Analysis of ordinal categorical data. John Wiley & Sons, New York
Ahearn, J. N. (1980). Evolution of behavioral reproductive isolation in a laboratory stock ofDrosophila silvestris. Experientia 36: 63–64
Akesson, B. (1977). Crossbreeding and geographic races: Experiments with the polychaete genusOphryotrocha. Mikrofauna Meeresbod. 61: 11–18
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. 299–316
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, Pennsylvania
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: 191–199
Barnard, J. L. Reish, D (1959). Ecology of Amphipoda and Polychaeta of Newport Bay, California. Occ. Pap. Allan Hancock Fdn 21: 1–106
Berger, E. M. (1973). Gene-enzyme variation in three sympatric species ofLittorina. Biol. Bull. mar. biol. Lab., Woods Hole 145: 83–90
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: 255–264
Berkeley E, Berkeley, C. (1953).Micronereis nanaimonensis n. sp.: with some notes on its life history. J. Fish. Res. Bd Can. 10: 85–95
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: 33–39
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, Amsterdam
Borowsky, B. (1984). Effects of receptive females' secretions on some male reproductive behaviors in the amphipod crustaceanMicrodeutopus gryllotalpa. Mar. Biol. 84: 183–187
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 York
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: 452–458
Carlton, J. T. (1985). Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr. mar. Biol. A. Rev. 23: 313–371
Carlton, J. T. (1987). Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bull. mar. Sci. 41(2): 452–465
Christensen, B. (1980). Animal cytogenetics. In: John, B., Bauer, H., Kayano, H., Levan, A., White, M. (eds.) Vol. 2: Annelida. Gebrüder Borntraeger, Berlin, Stuttgart
Clark, R. B. (1959). The tubicolous habit and the fighting reactions of the polychaeteNereis pelagica. Anim. Behav. 7: 85–90
Clark, R. B. (1961). The origin and formation of the heteronereis. Biol. Rev. 36: 199–236
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, California
Coyne, J. A., Orr, H. A. (1989). Patterns of speciation inDrosophila. Evolution 43: 362–381
Cram, A., Evans, S. M. (1980). Stability and lability in the evolution of behaviour in nereid polychaetes. Anim. Behav. 28: 483–490
Darwin, C. (1874). The descent of man, and selection in relation to sex, 2nd ed. John Murray, London
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: 761–775
Dawley, E. M. (1987). Species discrimination between hybridizing and non-hybridizing terrestrial salamanders. Copeia 4: 924–931
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-375
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: 11–43
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, Hawaii
Dobzhansky, T. (1940). Speciation as a stage in evolutionary divergence. Amer Nat. 74: 312–321
Ehlers, E. (1868). Die Borstenwurmer (Annelida, Chaetopoda) nach systematischen und anatomischen Untersuchungen dargestellt. Part 2. Wilhelm Engelmann, Leipzig, p. 269–748
Evans, S. M. (1971). Behavior in polychaetes. Q. Rev. Biol. 46: 379–405
Fauvel, P. (1923). Polychètes Errantes. Faune de France, 5. Federation Francaise de Sociétés de Sciences Naturelles, Paris
Fisher, R. A. (1930). The genetical theory of natural selection. Oxford Univ. Press, Oxford
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: 77–88
Grassle, J. P., Grassle, J. F. (1976). Sibling species in the marine pollution indicatorCapitella (Polychaeta). Science, N.Y. 192: 567–569
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: 999–1011
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. 317–333
Herpin, R (1923). Éthologie et développement deNereis (Neanthes) caudata delle Chiaje. C.r. hebd. Séanc. Acad. Sci., Paris 177: 542–544
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: 1–250
Highsmith, R. C. (1985). Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Mar. Ecol. Prog. Ser. 25: 169–179
Hilbish, T. J. (1985). Demographic and temporal structure of an allele frequency cline in the musselMytilus edulis. Mar. Biol. 86: 163–171
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: 1–16
Janson, K. (1987). Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol. J. Linn. Soc. 30: 245–256
Kimura, M., Weiss, G. H. (1964). The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49: 561–576
Kirkpatrick, M. (1982). Sexual selection and the evolution of female choice. Evolution 36: 1–12
Kligerman, A.D., Bloom, S.E. (1977). Rapid chromosome preparation from solid tissues of fishes. J. Fish. Res. Bd Can. 34: 266–269
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: 213–223
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 York
Koehn, R. K., Hall, J. G., Innis, D. J., Zera, A. J. (1984). Genetic differentiation ofMytilus edulis in eastern North America. Mar. Biol. 79: 117–126
Kristensen, E. (1988). Factors influencing the distribution of nereid polychaetes in Danish coastal waters. Ophelia 29: 127–140
Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78: 3721–3725
Lande, R. (1982). Rapid origin of sexual isolation and character divergence in a cline. Evolution 36: 213–223
Lessios, H. A. (1984). Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution 38: 1144–1148
Mayr, E. (1963). Animal species and evolution. Belknap Press, Harvard Univ. Press, Cambridge, MA
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: 1435–1441
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: 998–1108
Moore, J. P. (1903). Descriptions of two new species of polychaeta from Woods Hole, Massachusetts. Proc. Acad. Nat. Sci. USA 55: 720–726
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, Hawaii
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 Africa
Pesch, G. G., Pesch, C. E. (1980). Chromosome complement of the marine wormNeanthes arenaceodentata (Polychaeta: Annelida). Can J. Fish quat. Sciences 37: 286–288
Pesch, G. G., Pesch, C. E., Mueller, C. (1988). Chromosome complements from two populations of the marine wormNeanthes arenaceodentata (Annelida: Polychaeta). Ophelia 28: 163–167
Pettibone, M. H. (1963). Marine polychaete worms of the New England Region. 1. Aphroditidae through Trochochaetidae. Smithsonian Inst. Bull. 227, part 1, Washington, DC
Phelan, P. L., Baker, T. C. (1987). Evolution of male pheromones in moths: reproductive isolation through sexual selection? Science, N.Y. 235: 205–207
Read, G. B. (1980). A new species ofNereis (Polychaeta: Nereididae) from Wellington, New Zealand, Rock Shores. J. R. Soc. N.Z. 10: 185–193
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: 216–228
Reish, D. J. (1963). A quantitative study of the benthic polychaetous annelids of Bahia de San Quintin, Baja California. Pacif. Nat. 3: 399–436
Reish, D. J. (1968). The polychaetous Annelids of the Marshall Islands. Pacif. Sci. 22: 208–231
Reish, D. J., Alosi, M.C. (1968). Aggressive behavior in the polychaetous annelid family Nereidae. Bull. South. Calif. Acad. Sci. 67: 21–28
Rice, S. A., Simon, J. L. (1980). Intraspecific variation in the pollution indicator polychaetePolydora ligni (Spionidae). Ophelia 19: 79–115
Ridley, M. 1978. Paternal care. Anim. Behav. 26: 904–932
Roe, P. 1975. Aspects of life history and of territorial behavior in young individuals ofPlatynereis bicanaliculata andNereis vexillosa (Annelida, Polychaeta). Pacif. Sci. 29: 341–348
Rubinoff, R. W., Rubinoff I. (1971). Geographic and reproductive isolation in Atlantic and Pacific populations of PanamanianBathygobius. Evolution 25: 88–97
Snyder, T. P., Gooch, J. L. (1973). Genetic differentiation inLittorina saxatilis (Gastropoda). Mar. Biol. 22: 177–182
Solignac, M. (1981). Isolating mechanisms and modalities of speciation in theJaera albifrons species complex (Crustacea, Isopoda). Syst. Zool. 30: 387–405
Starczak, V. R. (1984). Sexual selection and intrasexual aggression in the marine polychaeteNereis (Neanthes) acuminata. Ph.D. thesis, Univ. of Connecticut, Storrs, Connecticut
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: 441–451
Trivers, R. L. (1978). Parental investment and sexual selection. In: Clutton-Brock, T. H., Harvey, P. H. (eds.) Reading in sociobiology. Freeman, San Francisco
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 Assoc
Volkman, B. (1977). Geographic and reproductive isolation in the genusTisbe (Copepoda, Harpacticoida). Mikrofauna Meeresbod. 61: 313–314
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: 296–309
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: 143–152
West-Eberhard, M. J. (1983). Sexual selection, social competition, and speciation. Q. Rev. Biol. 58: 155–183
Wilson, E. O. (1975). Sociobiology. Belknap Press, Cambridge, MA
Wright, S. (1943). Isolation by distance. Genetics 28: 114–138
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: 285–292
Author information
Authors and Affiliations
Additional information
Communicated by J. Grassle, Woods Hole
Rights and permissions
About this article
Cite this article
Weinberg, J.R., Starczak, V.R., Mueller, C. et al. Divergence between populations of a monogamous polychaete with male parental care: Premating isolation and chromosome variation. Mar. Biol. 107, 205–213 (1990). https://doi.org/10.1007/BF01319819
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01319819