Advertisement

Journal of Chemical Ecology

, Volume 31, Issue 8, pp 1865–1876 | Cite as

Chemical Signal Mediated Premating Reproductive Isolation in a Marine Polychaete, Neanthes acuminata (Arenaceodentata)

  • R. Sutton
  • E. Bolton
  • H. D. Bartels-Hardege
  • M. Eswards
  • D. J. Reish
  • J. D. Hardege
Article

Abstract

Neanthes acuminata Ehlers (1868) is a monogamous coastal polychaete with male parental care and a high level of sexual selection. We measured the level of prezygotic isolation among allopatric populations of N. acuminata; from the East and West Coast of the USA, a population from Hawaii, and a laboratory culture originating from Los Angeles, CA. All populations were found to preferably mate with members of their own population. Individuals from populations from Atlantic vs. Pacific Ocean failed to pair and to mate, either during the 10 min or 48 hr experiments. Instead, individuals showed high levels of aggressive behavior. Experiments measuring the levels of interpopulation aggression, established that individuals can recognize and discriminate among different populations of N. acuminata on the basis of olfactory cues. Aggressive behavior was induced by exposure of animals to seawater “conditioned” by individuals from the other populations, thus demonstrating the role of olfaction in the detection of “home” populations. The aggressive display was stronger upon exposure to seawater conditioned with “unrelated” populations and especially between Pacific and Atlantic populations.

Key Words

Neanthes acuminata premating isolation sex pheromones pop-ulation variations in chemical cues 

Notes

Acknowledgments

We thank Dr. Jim Weinberg for kindly providing us with the Neanthes cultures and fruitful discussions, Dr. T. Breithaupt for help on statistics, and J. Duck and V. Swetez for assistance with the culture of the worms. The authors gratefully acknowledge funding for this work by the Royal Society and by the Marine Biological Laboratory, Woods Hole, through a summer research fellowship to J.D.H.

References

  1. Ayasse, M., Birnbaum, J., Tengö, , Doorn, A., Taghizadeh, T., Francke, W. 1999Caste- and colony specific chemical signals on eggs of the bumblebee Bombus terrestris L. (Hymenoptera: Apidae)Chemoecology9119126Google Scholar
  2. Bentley, M. G., Pacey, A. A. 1992Physiological and environmental control of reproduction in polychaetesOceanogr. Mar. Biol., Annu. Rev.30443481Google Scholar
  3. Boilly-Marer, Y., Lassalle, B. 1980Electrophysiological responses of the central nervous system in the presence of homospecific and heterospecific sex pheromones in Nereids (Annelida, Polychaeta)J. Exp. Zool.2133339Google Scholar
  4. Brannon, E. L., Quinn, T. P. 1990Field test of the pheromone hypothesis for homing by Pacific salmonJ. Chem. Ecol.16603609Google Scholar
  5. Breithaupt, T., Atema, J. 2000The timing of chemical signaling with urine in dominance fights of male lobsters (Homarus americanus)Behav. Ecol. Sociobiol.496778Google Scholar
  6. Breithaupt, T., Eger, P. 2002Urine makes the difference: chemical communication in fighting crayfish made visibleJ. Exp. Biol.20512211231Google Scholar
  7. Bull, M. C., Griffin, C. L., Lanham, E. J., Johnston, G. R. 2000Recognition of pheromones from group members in a gregarious lizard, Egernia stokesiiJ. Herpetol.349299Google Scholar
  8. Bushmann, P. J., Atema, J. 2000Chemically-mediated mate location and evaluation in the lobster, Homarus americanusJ. Chem. Ecol.26893900Google Scholar
  9. Caldwell, R. L. 1982Interspecific chemically mediated recognition in two competing stomatopodsMar. Behav. Physiol.8189197Google Scholar
  10. CardÉ, R. T. 1986Epilogue: behavioral mechanismsPayne, T. L.Birch, M. C.Kennedy, C. E. J. eds. Mechanisms in Insect OlfactionClarendon PressOxford175186Google Scholar
  11. Cooper, W. E.,Jr., Wyk, J. H., Mouton, P. L. E. F. N. 1999Discrimination between self-produced pheromones and those produced by individuals of the same sex in the lizard Cordylus cordylusJ. Chem. Ecol.25197208Google Scholar
  12. Day, J. 1973. New Polychaeta from Beaufort, with a key to all species recorded from North Carolina. NOAA Tech. Rpt., NMFS, NOAA, circ-375, Washington, DC, USA.Google Scholar
  13. Denny, M. W., Shibata, M. F. 1989Consequences of surf zone turbulence for settlement and external fertilizationAm. Nat.134859889Google Scholar
  14. Evenden, M. L., Spohn, B. G., Moore, A. J., Preziosi, R. F., Haynes, K. F. 2002Inheritance and evolution of male response to sex pheromone in Trichoplysia ni (Lepidoptera: Noctuidae)Chemoecology125359Google Scholar
  15. Gemeno, C., Moore, A. J., Preziosi, R. F., Haynes, K. F. 2001Quantitative genetics of signal evolution: A comparison of the pheromonal signal in two populations of the cabbage looper, Trichoplysia niBehav. Genet.31157165Google Scholar
  16. Hardege, J. D. 1999Nereidid polychaetes as model organism for marine chemical ecology: A reviewHydrobiologia402145161Google Scholar
  17. Hardege, J. D., Bartels-Hardege, H., Zeeck, E., Grimm, F. T. 1990Induction of swarming of Nereis succineaMar. Biol.104291295Google Scholar
  18. Hardege, J. D., Bartels-Hardege, H. D., Yu, Y., Zhu, M. Y., Wu, B. L., Zeeck, E. 1994Environmental control of reproduction of Perinereis nuntia var. brevicirrusJ. Mar. Biol. Assoc. U.K.74903918Google Scholar
  19. Hurst, J., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., Cavaggioni, A., Beynon, R. L. 2001Individual recognition in mice mediated by major urinary proteinsNature414631634Google Scholar
  20. Karavanich, C., Atema, J. 1998Individual recognition and memory in lobster dominanceAnim. Behav.5615531560Google Scholar
  21. McLaughlin, L. C., Walters, J., Atema, J., Wainwright, N. 1999Urinary protein concentration in connection with agonistic interactions in Homarus americanusBiol. Bull.197254255Google Scholar
  22. Nevison, C. M., Barnard, C. B., Beynon, R., Hurst, J. L. 2000The consequences of inbreeding for recognizing competitorsProc. R. Soc. Lond., Sect. B.267687694Google Scholar
  23. Palmer, C. A., Edmands, S. 2000Mate choice in the face of both inbreeding and outbreeding depression in the intertidal copepod Tigriopus californicusMar. Biol.136693698Google Scholar
  24. Pesch, G. G., Pesch, C. E., Müller, C. 1988Chromosome complements from two populations of the marine worm Neanthes arenaceodentata (Annelida, Polychaeta)Ophelia28163167Google Scholar
  25. Pettibone, M. H. 1963Marine polychaete worms of the New England region 1. Aphroditidae through TrochochaetidaeSmithsonian Inst. Bull., 227 part 1Washington, DC, USAGoogle Scholar
  26. Reish, D. J. 1957The life history of the polychaete Neanthes caudata (delle Chiaije) including a summary of the development in the family NereidaePac. Sci.11216228Google Scholar
  27. Reish, D. J. 1985The use of the polychaetous annelid Neanthes arenaceodentata as a laboratory experimental animalTethys.11335341Google Scholar
  28. Reish, D. J., Alosi, M. C. 1968Aggressive behavior in the polychaetous annelid family NereidaeBull. S. C. Acad. Sci.672128Google Scholar
  29. Reish, D. J., Stevens, G. C. 1969Uptake of organic material by aquatic invertebrates: V. The influence of age on the uptake of glycine-C14 by the polychaete Neanthes arenaceodentataMar. Biol.3352355Google Scholar
  30. Rodriguez-Trelles, F., Weinberg, J. R., Ayala, F. J. 1996Presumptive rapid speciation after a founder event in a laboratory population of Nereis: Allozyme electrophoretic evidence does not support the hypothesisEvolution50457461Google Scholar
  31. Rollmann, S. M., Houck, L. D., Feldhoff, R. C. 2000Population variation in salamander courtship pheromonesJ. Chem. Ecol.2627132724Google Scholar
  32. Solomon, D. J. 1973Evidence for pheromone influenced homing by migrating Atlantic salmon, Salmo salar (L.)Nature244231232Google Scholar
  33. Stanhope, M. J, Connelly, M. M., Hartwick, B. 1992Evolution of a crustacean chemical communication channel: behavioral and ecological genetic evidence for a habitat-modified, race-specific pheromoneJ. Chem. Ecol.1818711887Google Scholar
  34. Starczak, V. R. 1984. Sexual selection and intrasexual aggression in the marine polychaete Nereis (Neanthes) acuminata. Ph.D. dissertation. Univ. Connecticut, Storrs, CT, USA.Google Scholar
  35. Weinberg, J. R., Starczak, V. R., MÜller, C., Pesch, G. C., Lindsay, S. M. 1990Divergence between populations of a monogamous polychaete with male parental care: Premating isolation and chromosome variationsMar. Biol.107205213Google Scholar
  36. Weinberg, J. R., Starczak, V. R., Jörg, D. 1992Evidence for rapid speciation following a founder event in the laboratoryEvolution4612141220Google Scholar
  37. Yamazaki, K., Singer, A., Beauchamp, G. K. 1999Origin, function and chemistry of H-2 regulated odorantsGenetica104235240Google Scholar
  38. Zeeck, E., Harder, T., Beckmann, M., Müller, C. T. 1996Marine gamete-release pheromonesNature382214Google Scholar
  39. Zeeck, E., Müller, C. T., Beckmann, M., Hardege, J. D., Papke, U., Sinnwell, V., Schröder, F. C., Francke, W. 1998Cysteine–glutathione disulfide, the sperm-release pheromone of the marine polychaete Nereis succinea (Annelida: Polychaeta)Chemoecology83338Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • R. Sutton
    • 1
  • E. Bolton
    • 2
  • H. D. Bartels-Hardege
    • 2
  • M. Eswards
    • 2
  • D. J. Reish
    • 3
  • J. D. Hardege
    • 2
  1. 1.School of BiosciencesCardiff UniversityCardiffUK
  2. 2.Department of Biological SciencesHull UniversityHullUK
  3. 3.Department of Biological SciencesCalifornia State UniversityLong BeachUSA

Personalised recommendations