Advertisement

Marine Biology

, Volume 154, Issue 6, pp 1067–1075 | Cite as

Spatial and temporal variation in distribution and protein ubiquitination for Mytilus congeners in the California hybrid zone

  • Jessica M. Dutton
  • Gretchen E. Hofmann
Original Paper

Abstract

Along the west coast of North America, the invasive mussel Mytilus galloprovincialis and a native congener M. trossulus overlap in range and compete for habitat in an extensive hybrid zone along central California. The two species have been shown to exhibit differential abiotic tolerances in laboratory studies, yet little is known about how such tolerances affect spatial and temporal patterns of geographic distribution, particularly in areas of competition. We examined distributions of the two congeners and their hybrids in neighboring intertidal and subtidal habitats in Bodega Bay, CA over 2 years, and compared shell length and seasonal ubiquitin (Ub) conjugates to estimate protein turnover and physiological stress for the species at each site. The two species were spatially segregated, with M. galloprovincialis dominating the subtidal habitat, and M. trossulus constituting a majority of the intertidal mussel population. Hybrid individuals appeared in low numbers at both sites. For each habitat, there was no statistical difference between shell lengths of M. galloprovincialis and hybrids but M. trossulus mussels were statistically smaller than the other two. In regards to physiological performance, ubiquitin conjugate values showed different seasonal cycles for the two species, suggesting different periods of peak environmental stress. The highest levels of Ub-conjugated proteins were observed in winter for M. galloprovincialis and in summer for M. trossulus, consistent with the respective range edges for their distributions since Bodega Bay is near the northern range edge of the invader and the southern edge of the native species. These findings suggest that future assessments of Mytilus populations along the California coast may need to consider vertical distributions and seasonal cycles as part of monitoring and research activities.

Keywords

Shell Length Hybrid Zone Intertidal Habitat Mussel Species Subtidal Habitat 
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.

Notes

Acknowledgments

The authors would like to thank S. Henkel and L. Hammond for field assistance, and Drs. S. Gaines, B. Kinlan and C. Osovitz for assistance with statistical analyses. This work was partially supported by a Mildred E. Mathias Graduate Research Grant through the University of California Natural Reserve System (awarded to JMD). We also thank the Bodega Marine Reserve for access to facilities and housing. During the preparation of this manuscript, the authors were supported by the NOAA Nancy Foster Scholarship Program (awarded to JMD) and the US National Science Foundation (NSF grant OCE-0425107, awarded to GEH). This is contribution number 293 from PISCO, the Partnership for Interdisciplinary Studies of Coastal Oceans funded primarily by the Gordon and Betty Moore Foundation and David and Lucile Packard Foundation. The experiments contained herein comply with the current laws of the United States, in which they were performed.

References

  1. Anderson AS, Bilodeau AL, Gilg MR, Hilbish TJ (2002) Routes of introduction of the Mediterranean mussel (Mytilus galloprovincialis) to Puget Sound and Hood Canal. J Shellfish Res 21:75–79Google Scholar
  2. Berman J, Carlton JT (1991) Marine invasion processes—interactions between native and introduced marsh snails. J Exp Mar Biol Ecol 150:267–281CrossRefGoogle Scholar
  3. Braby CE, Somero GN (2006a) Ecological gradients and relative abundance of native (Mytilus trossulus) and invasive (Mytilus galloprovincialis) blue mussels in the California hybrid zone. Mar Biol 148:1249–1262CrossRefGoogle Scholar
  4. Braby CE, Somero GN (2006b) Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J Exp Biol 209:2554–2566CrossRefGoogle Scholar
  5. Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215CrossRefGoogle Scholar
  6. Byers JE (2000a) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239CrossRefGoogle Scholar
  7. Byers JE (2000b) Differential susceptibility to hypoxia aids estuarine invasion. Mar Ecol Prog Ser 203:123–132CrossRefGoogle Scholar
  8. Fields PA, Rudomin EL, Somero GN (2006) Temperature sensitivities of cytosolic malate dehydrogenases from native and invasive species of marine mussels (genus Mytilus): sequence-function linkages and correlations with biogeographic distribution. J Exp Biol 209:656–667CrossRefGoogle Scholar
  9. Geller JB (1999) Decline of a native mussel masked by sibling species invasion. Conserv Biol 13:661–664CrossRefGoogle Scholar
  10. Geller JB, Carlton JT, Powers DA (1994) PCR based detection of Mtdna haplotypes of native and invading mussels on the Northeastern Pacific coast—latitudinal pattern of invasion. Mar Biol 119:243–249CrossRefGoogle Scholar
  11. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428CrossRefGoogle Scholar
  12. Griffiths CL, Hockey PAR (1987) A model describing the interactive roles of predation, competition and tidal elevation in structuring mussel populations. South Afr J Mar Sci Suid Afrikaanse Tydskrif Vir Seewetenskap 5:547–556CrossRefGoogle Scholar
  13. Halpin PM, Menge BA, Hofmann GE (2002) Fine-scale temporal and spatial variation in the heat shock response of mussels in nature. Integr Comp Biol 42:1239CrossRefGoogle Scholar
  14. Harger JRE (1968) The role of behavioral traits in influencing the distribution of two species of sea mussel, Mytilus edulis and Mytilus californianus. Veliger 11:45–49Google Scholar
  15. Harley CDG, Helmuth BST (2003) Local- and regional-scale effects of wave exposure, thermal stress, and absolute versus effective shore level on patterns of intertidal zonation. Limnol Oceanogr 48:1498–1508CrossRefGoogle Scholar
  16. Hawkins AJS (1991) Protein-turnover—a functional appraisal. Funct Ecol 5:222–233CrossRefGoogle Scholar
  17. Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384CrossRefGoogle Scholar
  18. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
  19. Hockey PAR, Schurink CV (1992) The invasive biology of the mussel Mytilus galloprovincialis on the Southern African coast. Trans R Soc South Afr 48:123–139CrossRefGoogle Scholar
  20. Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures—seasonal-changes in levels of ubiquitin conjugates and Hsp70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518PubMedGoogle Scholar
  21. Hofmann GE, Somero GN (1996) Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: evidence from the heat shock response and protein ubiquitination. Mar Biol 126:65–75CrossRefGoogle Scholar
  22. Inoue K, Waite JH, Matsuoka M, Odo S, Harayama S (1995) Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. Biol Bull 189:370–375CrossRefGoogle Scholar
  23. Jewett EB, Hines AH, Ruiz GM (2005) Epifaunal disturbance by periodic low levels of dissolved oxygen: native vs invasive species response. Mar Ecol Prog Ser 304:31–44CrossRefGoogle Scholar
  24. Lee SYM, Morton B (1985) The introduction of the Mediterranean mussel Mytilus galloprovincialis into Hong Kong. Malacol Rev 18:107–109Google Scholar
  25. Martel C, Guarini JM, Blanchard G, Sauriau PG, Trichet C, Robert S, Garcia-Meunier P (2004) Invasion by the marine gastropod Ocinebrellus inornatus in France III. Comparison of biological traits with the resident species Ocenebra erinacea. Mar Biol 146:93–102CrossRefGoogle Scholar
  26. Matson SE, Davis JP, Chew KK (2003) Laboratory hybridization of the mussels, Mytilus trossulus and M. galloprovincialis: larval growth, survival and early development. J Shellfish Res 22:423–430Google Scholar
  27. McDonald JH, Koehn RK (1988) The mussels Mytilus galloprovincialis and Mytilus trossulus on the Pacific coast of North-America. Mar Biol 99:111–118CrossRefGoogle Scholar
  28. Place SP, Hofmann GE (2005) Function and expression of the molecular chaperone HSP70 in Antarctic fishes. FASEB J 19:A214Google Scholar
  29. Place SP, Zippay ML, Hofmann GE (2004) Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fishes. Am J Physiol Regul Integr Comp Physiol 287:R429–R436CrossRefGoogle Scholar
  30. Purcell JE, Shiganova TA, Decker MB, Houde ED (2001) The ctenophore Mnemiopsis in native and exotic habitats: US estuaries versus the Black Sea basin. Hydrobiologia 451:145–176CrossRefGoogle Scholar
  31. Rawson PD, Hilbish TJ (1995) Distribution of male and female lineages in populations of blue mussels, Mytilus trossulus and M. galloprovincialis, along the Pacific coast of North America. Mar Biol 124:245–250CrossRefGoogle Scholar
  32. Rawson PD, Agrawal V, Hilbish TJ (1999) Hybridization between the blue mussels Mytilus galloprovincialis and M. trossulus along the Pacific coast of North America: evidence for limited introgression. Mar Biol 134:201–211CrossRefGoogle Scholar
  33. Rensel MAE, Elliot J, Wimberger P (2005) Will the introduced mussel Mytilus galloprovincialis outcompete the native mussel M. trossulus in Puget Sound? A study of relative survival and growth rates among different habitats. In: Proceedings of the 2005 Puget Sound Georgia basin research conferenceGoogle Scholar
  34. Roberts DA, Hofmann GE, Somero GN (1997) Heat-shock protein expression in Mytilus californianus: Acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol Bull 192:309–320CrossRefGoogle Scholar
  35. Sarver SK, Foltz DW (1993) Genetic population-structure of a species complex of blue mussels (Mytilus spp). Mar Biol 117:105–112CrossRefGoogle Scholar
  36. Schneider KR, Helmuth B (2007) Spatial variability in habitat temperature may drive patterns of selection between an invasive and native mussel species. Mar Ecol Prog Ser 339:157–167CrossRefGoogle Scholar
  37. Schurink CV, Griffiths CL (1993) Factors affecting relative rates of growth in 4 South-African mussel species. Aquaculture 109:257–273CrossRefGoogle Scholar
  38. Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68CrossRefGoogle Scholar
  39. Todgham AEH, Hoaglund EA, Hofmann GE (2007) Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation in vivo. J Comp Physiol B 177:857–866CrossRefGoogle Scholar
  40. Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936PubMedGoogle Scholar
  41. Wonham MJ (2004) Mini-review: distribution of the Mediterranean mussel Mytilus galloprovincialis (Bivalvia: Mytilidae) and hybrids in the Northeast Pacific. J Shellfish Res 23:535–543Google Scholar
  42. Yamada SB, Mansour RA (1987) Growth-inhibition of native Littorina saxatilis (Olivi) by introduced L Littorea (L). J Exp Mar Biol Ecol 105:187–196CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Ecology, Evolution and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations