Spatial variability in habitat temperature may drive patterns of selection between an invasive and native mussel species

Summary Coping with environmental stress may involve combinations of behavioral and physiological responses. We examined potential interactions between adult mussels’ simple behavioral repertoire – opening/closing of the shell valves – and thermal stress physiology in common-gardened individuals of three Mytilus congeners found on the West Coast of North America, two of which are native species (M. californianus and M. trossulus) and one an invasive from the Mediterranean (M. galloprovincialis). We first continuously monitored valve behavior over three consecutive days on which body temperatures were gradually increased, either in air or in seawater. A temperature threshold effect was evident between 25°C and 33°C in several behavioral measures. Mussels tended to spend much less time with the valves in a sealed position following exposure to 33°C body temperature, especially when exposed in air. This behavior could not be explained by decreases in adductor muscle glycogen (stores of this metabolic fuel actually increased in some scenarios), impacts of forced valve sealing on long-term survival (none observed in a second experiment), or loss of contractile function in the adductor muscles (individuals exhibited as many or more valve adduction movements following elevated body temperature as in controls). We hypothesize that this reduced propensity to seal the valves following thermal extremes represents avoidance of hypoxia-reoxygenation cycles and concomitant oxidative stress. We further conjecture that prolonged valve gaping following episodes of elevated body temperature may have important ecological consequences by affecting species interactions. We then examined survival over a 90-d period following exposure to elevated body temperature and/or emersion, observing ongoing mortality throughout this monitoring period. Survival varied significantly among species (M. trossulus had lowest survival) and among experimental contexts (survival was lowest after experiencing elevated body temperature in seawater). Surprisingly, we observed no cumulative impact on survival of three days relative to one day of exposure to elevated body temperature. The delayed mortality and context-specific outcomes we observed have important implications for design of future experiments and for interpretation of field distribution patterns of these species. Ultimately, variation in the catalog of physiological and behavioral capacities among closely related or sympatric species is likely to complicate prediction of the ecological consequences of global change and species invasions.

Section: Discussionsupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Behavior and survival ofMytiluscongeners following episodes of elevated body temperature in air and seawater

Dowd

Somero

2012

“…Therefore, abiotic factors, such as temperature and salinity, are likely to play a role in setting biogeographic range limits (Tomanek, 2008). Indeed, where M. trossulus and M. galloprovincialis co-occur in central California, M. galloprovincialis out-competes the native species at sites that are warmer and saltier (Braby and Somero, 2006b;Schneider, 2008;Schneider and Helmuth, 2007). In addition, M. trossulus, M. edulis and M. galloprovincialis maintain a greater scope for growth at cold, cool and warm temperatures, respectively (Fly and Hilbish, 2013).…”

Section: Thermal Responses In Mytilus Trossulus Versus Mytilus Gallopmentioning

confidence: 99%

“…M. californianus has a broad latitudinal range that extends along the eastern Pacific from Baja California to Alaska (Seed, 1992), where it characteristically inhabits wave-exposed sites of the rocky intertidal zone, although it can also be found in subtidal habitats as well. The blue mussels can also be found at wave-exposed sites (Seed, 1992), but in the eastern North Pacific they tend to be more prevalent in protected habitats, such as bays and estuaries (Braby and Somero, 2006b;Lockwood and Somero, 2011a;Schneider and Helmuth, 2007). The biogeographic range of the blue mussels extends across several continents (Hilbish et al, 2000;McDonald and Koehn, 1988;Seed, 1992).…”

Section: Introductionmentioning

confidence: 99%

The environmentally tuned transcriptomes ofMytilusmussels

Lockwood

Connor

Gracey

2015

Transcriptomics is a powerful tool for elucidating the molecular mechanisms that underlie the ability of organisms to survive and thrive in dynamic and changing environments. Here, we review the major contributions in this field, and we focus on studies of mussels in the genus Mytilus, which are well-established models for the study of ecological physiology in fluctuating environments. Our review is organized into four main sections. First, we illustrate how the abiotic forces of the intertidal environment drive the rhythmic coupling of gene expression to diel and tidal cycles in Mytilus californianus. Second, we discuss the challenges and pitfalls of conducting transcriptomic studies in field-acclimatized animals. Third, we examine the link between transcriptomic responses to environmental stress and biogeographic distributions in blue mussels, Mytilus trossulus and Mytilus galloprovincialis. Fourth, we present a comparison of transcriptomic datasets and identify 175 genes that share common responses to heat stress across Mytilus species. Taken together, these studies demonstrate that transcriptomics can provide an informative snapshot of the physiological state of an organism within an environmental context. In a comparative framework, transcriptomics can reveal how natural selection has shaped patterns of transcriptional regulation that may ultimately influence biogeography.

“…the Pacific Decadal Oscillation, the main hybrid zone ranges roughly from Monterey Bay to San Francisco Bay, with small numbers of M. galloprovincialis hybrids found further north to Humboldt Bay (Braby and Somero, 2006a;Hilbish et al, 2010). Field surveys indicate that the distribution within the hybrid zone is determined by both temperature and salinity (Braby and Somero, 2006a;Schneider and Helmuth, 2007). Salinity seems to play a crucial role because M. trossulus occurs at sites with higher freshwater input that are warm enough to normally favor occurrence of the more warm-adapted M. galloprovincialis (Braby and Somero, 2006a).…”

Section: Introductionmentioning

confidence: 99%

Proteomics of hyposaline stress in blue mussel congeners (genusMytilus): implications for biogeographic range limits in response to climate change

Tomanek

Zuzow

Hitt

et al. 2012

SUMMARYClimate change is affecting speciesʼ physiology, pushing environmental tolerance limits and shifting distribution ranges. In addition to temperature and ocean acidification, increasing levels of hyposaline stress due to extreme precipitation events and freshwater runoff may be driving some of the reported recent range shifts in marine organisms. Using two-dimensional gel electrophoresis and tandem mass spectrometry, we characterized the proteomic responses of the cold-adapted blue mussel Mytilus trossulus, a native to the Pacific coast of North America, and the warm-adapted M. galloprovincialis, a Mediterranean invader that has replaced the native from the southern part of its range, but may be limited from expanding north due to hyposaline stress. After exposing laboratory-acclimated mussels for 4h to two different experimental treatments of hyposaline conditions and one control treatment (24.5, 29.8 and 35.0psu, respectively) followed by a 0 and 24h recovery at ambient salinity (35psu), we detected changes in the abundance of molecular chaperones of the endoplasmic reticulum (ER), indicating protein unfolding, during stress exposure. Other common responses included changes in small GTPases of the Ras superfamily during recovery, which suggests a role for vesicle transport, and cytoskeletal adjustments associated with cell volume, as indicated by cytoskeletal elements such as actin, tubulin, intermediate filaments and several actin-binding regulatory proteins. Changes of proteins involved in energy metabolism and scavenging of reactive oxygen species suggest a reduction in overall energy metabolism during recovery. Principal component analyses of protein abundances suggest that M. trossulus is able to respond to a greater hyposaline challenge (24.5psu) than M. galloprovincialis (29.8psu), as shown by changing abundances of proteins involved in protein chaperoning, vesicle transport, cytoskeletal adjustments by actin-regulatory proteins, energy metabolism and oxidative stress. While proteins involved in energy metabolism were lower in M. trossulus during recovery from hyposaline stress, M. galloprovincialis showed higher abundances of those proteins at 29.8psu, suggesting an energetic constraint in the invader but not the native congener. Both species showed lower levels of oxidative stress proteins during recovery. In addition, oxidative stress proteins associated with protein synthesis and folding in the ER showed lower levels during recovery in M. galloprovincialis, in parallel with ER chaperones, indicating a reduction in protein synthesis. These differences may enable the native M. trossulus to cope with greater hyposaline stress in the northern part of its range, as well as to outcompete M. galloprovincialis in the southern part of M. trossulusʼ range, thereby preventing M. galloprovincialis from expanding further north. Supplementary material available online at