Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 21:75–79

    Google Scholar 

  • Berman J, Carlton JT (1991) Marine invasion processes—interactions between native and introduced marsh snails. J Exp Mar Biol Ecol 150:267–281

    Article  Google Scholar 

  • 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 148:1249–1262

    Article  Google Scholar 

  • 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 209:2554–2566

    Article  Google Scholar 

  • 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 300:189–215

    Article  Google Scholar 

  • Byers JE (2000a) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239

    Article  Google Scholar 

  • Byers JE (2000b) Differential susceptibility to hypoxia aids estuarine invasion. Mar Ecol Prog Ser 203:123–132

    Article  CAS  Google Scholar 

  • 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 209:656–667

    Article  CAS  Google Scholar 

  • Geller JB (1999) Decline of a native mussel masked by sibling species invasion. Conserv Biol 13:661–664

    Article  Google Scholar 

  • 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 119:243–249

    Article  CAS  Google Scholar 

  • Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428

    Article  CAS  Google Scholar 

  • 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 5:547–556

    Article  Google Scholar 

  • 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 42:1239

    Article  Google Scholar 

  • Harger JRE (1968) The role of behavioral traits in influencing the distribution of two species of sea mussel, Mytilus edulis and Mytilus californianus. Veliger 11:45–49

    Google Scholar 

  • 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 48:1498–1508

    Article  Google Scholar 

  • Hawkins AJS (1991) Protein-turnover—a functional appraisal. Funct Ecol 5:222–233

    Article  Google Scholar 

  • Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Hockey PAR, Schurink CV (1992) The invasive biology of the mussel Mytilus galloprovincialis on the Southern African coast. Trans R Soc South Afr 48:123–139

    Article  Google Scholar 

  • 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 198:1509–1518

    CAS  PubMed  Google Scholar 

  • 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 126:65–75

    Article  CAS  Google Scholar 

  • 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 189:370–375

    Article  CAS  Google Scholar 

  • 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 304:31–44

    Article  Google Scholar 

  • Lee SYM, Morton B (1985) The introduction of the Mediterranean mussel Mytilus galloprovincialis into Hong Kong. Malacol Rev 18:107–109

    Google Scholar 

  • 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 146:93–102

    Article  Google Scholar 

  • 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 22:423–430

    Google Scholar 

  • McDonald JH, Koehn RK (1988) The mussels Mytilus galloprovincialis and Mytilus trossulus on the Pacific coast of North-America. Mar Biol 99:111–118

    Article  Google Scholar 

  • Place SP, Hofmann GE (2005) Function and expression of the molecular chaperone HSP70 in Antarctic fishes. FASEB J 19:A214

    Google Scholar 

  • 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–R436

    Article  CAS  Google Scholar 

  • 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 451:145–176

    Article  Google Scholar 

  • 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 124:245–250

    Article  Google Scholar 

  • 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 134:201–211

    Article  Google Scholar 

  • 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 conference

  • 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 192:309–320

    Article  CAS  Google Scholar 

  • Sarver SK, Foltz DW (1993) Genetic population-structure of a species complex of blue mussels (Mytilus spp). Mar Biol 117:105–112

    Article  Google Scholar 

  • 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 339:157–167

    Article  Google Scholar 

  • Schurink CV, Griffiths CL (1993) Factors affecting relative rates of growth in 4 South-African mussel species. Aquaculture 109:257–273

    Article  Google Scholar 

  • Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68

    Article  CAS  Google Scholar 

  • 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 177:857–866

    Article  CAS  Google Scholar 

  • 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 202:2925–2936

    CAS  PubMed  Google Scholar 

  • Wonham MJ (2004) Mini-review: distribution of the Mediterranean mussel Mytilus galloprovincialis (Bivalvia: Mytilidae) and hybrids in the Northeast Pacific. J Shellfish Res 23:535–543

    Google Scholar 

  • Yamada SB, Mansour RA (1987) Growth-inhibition of native Littorina saxatilis (Olivi) by introduced L Littorea (L). J Exp Mar Biol Ecol 105:187–196

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, 93101-9610, USA

    Jessica M. Dutton & Gretchen E. Hofmann

  2. Marine Science Institute, University of California, Santa Barbara, CA, 93106-6150, USA

    Gretchen E. Hofmann

Authors
  1. Jessica M. Dutton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gretchen E. Hofmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jessica M. Dutton.

Additional information

Communicated by H.O. Pörtner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dutton, J.M., Hofmann, G.E. Spatial and temporal variation in distribution and protein ubiquitination for Mytilus congeners in the California hybrid zone. Mar Biol 154, 1067–1075 (2008). https://doi.org/10.1007/s00227-008-1000-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-1000-5

Keywords

Search

Navigation