the physiology of global change: linking patterns to

MA04CH03-Somero ARI 3 November 2011 13:35

The Physiology of GlobalChange: Linking Patternsto MechanismsGeorge N. SomeroDepartment of Biology, Hopkins Marine Station, Stanford University, Pacific Grove,California 93950; email: [email protected]

Annu. Rev. Mar. Sci. 2012. 4:39–61

First published online as a Review in Advance onJuly 29, 2011

The Annual Review of Marine Science is online atmarine.annualreviews.org

This article’s doi:10.1146/annurev-marine-120710-100935

Copyright c© 2012 by Annual Reviews.All rights reserved

1941-1405/12/0115-0039$20.00

Keywords

adaptation, aerobic metabolism, biogeography, climate change, salinity,temperature

Abstract

Global change includes alterations in ocean temperature, oxygen availability,salinity, and pH, abiotic variables with strong and interacting influences onthe physiology of all taxa. Physiological stresses resulting from changes inthese four variables may cause broad biogeographic shifts as well as localizedchanges in distribution in mosaic habitats. To elucidate these causal linkages,I address the following questions: What types of physiological limitations canalter species’ distributions and, in cases of extreme stress, cause extinctions?Which species are most threatened by these physiological challenges—andwhy? How do contents of genomes establish capacities to respond to globalchange, notably in the case of species that have evolved in highly stablehabitats? How fully can phenotypic acclimatization offset abiotic stress? Canphysiological measurements, including new molecular (“-omic”) approaches,provide indices of the degree of sublethal stress an organism experiences?And can physiological evolution keep pace with global change?

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INTRODUCTION: THE SCOPE OF PHYSIOLOGICAL ANALYSISAND ITS UTILITY IN STUDY OF GLOBAL CHANGE

A common pattern manifested in the historical development of different fields of biology is a pro-gression from the descriptive or phenomenological level of study, which typically is characteristicof a nascent field of investigation, to the mechanistic level, where the phenomena under investiga-tion are explained in a cause-effect, reductionist manner. Global change biology can be viewed inthis context. Many studies of marine and terrestrial ecosystems have documented shifts in species’distribution patterns—at broad biogeographic scales and within mosaic habitats where environ-mental conditions vary over small distances—that correlate with changes in one or more abioticfactors, temperature in particular. Thus, we have a wealth of phenomena that beg for explanationin terms of underlying causal mechanisms. These mechanisms are apt to be complex and involveinteractions among oceanographic, climatological, and ecological factors, as well as direct envi-ronmental effects on the physiological systems that are the focus of this review. However, throughappropriate experimental design, it should be possible to tease apart direct effects of abiotic factorson physiological systems from these other determinants of where organisms are found and howwell they perform in their changing habitats. Scott Doney (2010) has phrased this challenge well:“. . . more detailed biochemical, systems biology, and genomic studies are required to explain mech-anistically the responses of cells and organisms to external perturbation, supplementing what haveoften been to date more phenomenological findings. Genomic and physiological research shouldbe embedded in large-scale ecological and biogeochemical spatial surveys. . . .” This review high-lights the strengths and the limitations of physiological approaches for addressing this challenge.

The term physiology is essentially synonymous with function. The science of physiology ex-plains how organisms work (Schmidt-Nielsen 1972) and how these workings are influenced—during individuals’ lifetimes and over long evolutionary periods—by the changing environmentsin which organisms live. In this review I address physiological issues of relevance to the studyof global change in a broad manner by examining function at several levels of biological or-ganization: whole-organism activity, organ-level function, cellular-level processes, biochemicalreactions, and genomic-level phenomena, including genome content, adaptive variation in gene(protein) sequence, and regulation of gene expression. All of these levels of function are sensitiveto alterations in the abiotic factors being altered by global change. The abilities of these diversefunctions to acclimatize and evolutionarily adapt to change thus may determine the survival of aspecies in its changing environment.

The type of multilevel and multi-time-frame analysis developed in the following sections offersseveral potential means for advancing our understanding of biological responses to global change.First, by examining responses of numerous physiological systems of different species to changesin an abiotic factor like temperature or salinity, it may be possible to identify the types of lethaland sublethal stresses that account for observed changes in distribution patterns. These insights,in turn, may help us to predict future distributional shifts on biogeographic and local scales.

Second, through comparative studies of different taxa from a variety of ecosystems, it may bepossible to characterize relative vulnerabilities of species and entire ecosystems to global change.How, for example, do ecosystems from different latitudes differ in their vulnerabilities to risingtemperatures? How does stability of the environment over long-term evolutionary history affectvulnerability of organisms (and ecosystems) to rapid change in abiotic factors like temperatureor oxygen availability? Can relative sensitivities of native and invasive species to environmentalchange provide insights into the success that invasive species may enjoy in a changing world?

Third, physiological studies can characterize capacities of organisms to acclimatize to environ-mental change. Adaptive phenotypic plasticity may be crucial in allowing a species to withstand

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environmental change in the short run, before evolutionary adaptation is possible. Some speciesare eurytolerant and can thrive under widely different abiotic conditions; others are strikinglystenotolerant and survive over only very narrow ranges of abiotic factors. Genomic analyses arebeginning to provide insights into the differences in genomic content that differentiate steno- andeurytolerant species. These data, in turn, are providing a firmer basis for predictions about relativesensitivities of species to changing abiotic conditions.

Fourth, physiological approaches may enable diagnoses of the “state of health” of naturalpopulations exposed to changes in abiotic conditions. New approaches that employ “-omic” tech-nologies (genomics, transcriptomics, and proteomics) are yielding insights into the nature ofsublethal stress at the cellular level. These approaches have begun to identify thresholds of stressat which different physiological systems begin to experience serious limitations, and to describehow increasing levels of stress elicit a tiered stress response that reflects severity of perturbation.

Fifth, molecular-level studies are shedding light on an important—yet largely unanswered—question about global change: Can adaptive genetic change occur at a rate that allows organ-isms’ physiological functions to keep up with ongoing changes in abiotic factors like temperature(Hoffmann & Sgro 2011)?

If effectively integrated with research on broader ecological and oceanographic phenomena,physiological studies focused on these five related questions have the potential to assist marinescientists in understanding the basic mechanisms underlying observed global-change-correlatedalterations in marine ecosystems and provide a stronger mechanistic foundation for predictingthese ecosystems’ future status in a changing ocean (Somero 2010, 2011).

BIOGEOGRAPHIC SHIFTS IN WARMING SEAS AND SEASHORES

Distributional Changes with Temperature

Because of the strong emphasis that global change scientists have given to the consequences ofrising temperatures, the most extensive data sets for developing linkages between distributionalchanges and underlying physiological mechanisms are those in which temperature is the abioticfactor of focus. Numerous analyses have documented how biogeographic patterning in open oceanand intertidal habitats is changing in concert with rising water and air temperatures. In the NorthAtlantic, planktonic copepod species have exhibited a northward range shift of approximately 10◦

latitude since the 1960s (Beaugrand et al. 2002). In the North Sea, large temperature-correlatedshifts in biogeographic patterning have been documented for demersal fishes: 87% of the speciesstudied exhibited extensions of their northern range limits, and approximately half of the northernspecies either migrated to deeper depths or contracted the southern limits of their biogeographicranges (Perry et al. 2005).

Intertidal ecosystems have shown especially pronounced and rapid biogeographic changes(Barry et al. 1995, Helmuth et al. 2006). For some species, estimated rates of biogeographic shiftshave been as high as 49–540 km per decade ( Jones et al. 2009, 2010). These latitudinal shiftsare several times greater than those reported in a variety of terrestrial ecosystems (Parmesan &Yohe 2003, Root et al. 2003). Furthermore, within a single rocky intertidal ecosystem, a mosaicof abiotic conditions exists, such that, over spatial scales of meters or less, a range of thermalconditions are found that may exceed those found over wide ranges of latitude or predicted tooccur over many decades of further global warming (Helmuth et al. 2010, Denny et al. 2011).Thus, intertidal ecosystems prove to be excellent study systems for evaluating climate change(Somero 2002; Harley et al. 2006; Helmuth et al. 2006, 2010; Helmuth 2009), and they will serveas a major focal point of this review.

www.annualreviews.org • Physiology of Global Change 41

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Challenges of Demonstrating Causation Behind Correlation

These extensive data on shifting distributions of marine organisms would seem to provide a strongbasis for concluding that temperature is the key driver of changing biogeographic- and local-scalepatterning. However, these data do not, in the absence of physiological analysis, tell us whetherthese temperature-correlated patterns are due to direct effects of temperature on the workings oforganisms or instead derive from ecological or oceanographic factors. The potential complexitiesof these varied interactions are suggested by studies of sea star (Pisaster ochraceus) predation onMytilus mussels in rocky intertidal habitats, which found that increases in temperature stronglyaffected rates of predation (Sanford 1999, Pincebourde et al. 2008). These effects on feedingbehavior could have major influences on ecosystem structure. For example, if increased heatstress due to global change were to increase predation, then the extent of mussel beds couldpotentially decrease. This effect could cause changes in occurrence or abundance of dozens tohundreds of other species that live among mussels, even if many or all of these other species arenot directly challenged by rising temperature per se. A further illustration of the complexities ofteasing apart the direct effects of temperature from broader ecological interactions is illustrated byGenner et al. (2004), who showed that populations of a species of fish exhibited different responsesto rising temperatures in different parts of the species’ biogeographic range. Additionally, somebiogeographic shifts may merely be consequences of altered current patterns, which alter supply oforganisms, notably larval stages, and thus change ecosystem composition. Increased precipitationleading to reduced salinity in estuarine habitats may, in some cases, be more important in governinglocal distributions than changes in temperatures (Braby & Somero 2006a,b). Thus, to establishcause-effect linkages between changes in one or more abiotic factors and alterations in a species’physiological status and distribution pattern, researchers must take great care in their experimentaldesigns. A first challenge is to identify study systems where such causal analyses seem most feasible.

Below, I build an analysis of the physiology of global change largely around two case studies,which examine sets of species for which detailed, multilevel analyses of the effects of abiotic stresson physiological systems have been performed. I focus strongly on differently adapted congenericspecies, where evolved differences in environmental optima and tolerance limits can be readilydiscerned owing to the absence of confounding effects of phylogeny (Hochachka & Somero 2002).These studies can offer at least tentative answers to the five overarching questions raised in theintroduction. After presenting each case study, I widen the focus of analysis to examine the degreeto which conclusions based on the principal case study species can be generalized to widely differentmarine taxa and ecosystems.

Note that, despite their ecological importance and “poster child” status in analysis of globalchange in the marine realm, I have elected not to focus strongly on coral reef systems. This choiceis based in part on the large amount of attention they already have received (for an overview, seeHoegh-Guldberg et al. 2007), but was made primarily because the potential to conduct a thorough,multilevel, reductionist analysis is considerably more limited than in the two case studies I havechosen. Likewise, I chose not to focus on ocean acidification, which has recently been reviewedextensively (e.g., Doney et al. 2009, Hofmann et al. 2010) and is a topic where, again, the type ofreductionist analysis I attempt here would be premature.

CASE STUDY 1: CONGENERS OF MUSSELS (GENUS MYTILUS)

Distribution Patterns: Biogeographic- and Local-Scale Effects

One of the most informative study systems for examining causal linkages between changes in abioticenvironmental factors—especially air and water temperatures (and, for some species, salinity as

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well)—and shifts in distribution patterns over different temporal and spatial scales comprises fourcongeners of mussels in the genus Mytilus. Below, I first review recent studies of biogeographic- andlocal-scale changes in distributions of blue mussel congeners (the Mytilus edulis complex). Then,I use a reductionist approach to characterize interspecific variations in physiological systems thatmay be responsible, at least in part, for these striking distributional changes.

On the East Coast of the United States, the dominant blue mussel, Mytilus edulis, has contractedits southern range by approximately 350 km during the past half century, a northward shift insouthern range limit of approximately 7.5 km per year ( Jones et al. 2009, 2010). During thisperiod, water and air temperatures in the species’ coastal habitats have risen substantially. Mortalityis largely due to failure of adult mussels to survive peak temperatures in summer. In cooler seasonslarval recruitment continues at many southern sites where virtually complete mortality occursamong adults in summer. At sites where adults persist into summer, their vertical distributionsin the field are truncated such that only low-intertidal or subtidal animals survive. The thresholdtemperature at which repeated, consecutive exposures to heating lead to high levels of mortalityappears to be 32◦C. Tolerance of chronically high temperatures is even lower. Chapple et al.(1998) reported that, whereas survival times of M. edulis at 28.5◦C varied with season, peaking inlate summer and early autumn, maximal survival at this temperature never exceeded ∼10 days.The relative importance of air and water temperatures in mortality showed latitudinal variation.At more northern sites, water temperatures never reached lethal levels, and all temperature-related mortality appeared to be driven by high air temperatures. At southern sites, high watertemperatures explained most mortality.

On the West Coast of the United States, two other blue mussel congeners occur, and bothhave exhibited changes in biogeographic range over the past several decades. The native blue mus-sel, Mytilus trossulus, which formerly occurred along most of the West Coast of North America,has been displaced by a more heat-tolerant invasive congener from the Mediterranean, Mytilusgalloprovincialis, southward from Monterey Bay (∼37◦N) (Rawson et al. 1999). This species re-placement began sometime in the mid-twentieth century, but was not discovered until allozymestudies were performed on what were thought at the time to be different populations of M. edulis,the blue mussel congener that, in fact, is absent from the West Coast (McDonald & Koehn 1988).The poleward movement of M. galloprovincialis has recently shown a reversal in concert with acooling phase of the Pacific Decadal Oscillation (PDO) (Hilbish et al. 2010). Over approximatelyone decade, M. galloprovincialis has become rare or absent at sites over the northern 200 km of itsrange. The difference in sea surface temperature between warm and cold phases of the PDO issmall, approximately 1◦C. Hilbish et al. (2010) conjectured that even this seemingly minor decreasein temperature during the cold phase of the PDO may be sufficient to retard larval development ofthe more warm-adapted invasive species, such that recruitment is handicapped in northern waters.Study of the thermal physiology of larval stages of these congeners is clearly needed, to ascertainwhether the different thermal sensitivities of adults, as discussed below, characterize earlier lifestages as well.

In addition to temperature-related shifts in distribution over latitudinal scales, West Coastblue mussels exhibit complex patterning related to temperature and salinity among sites in theSan Francisco and Monterey Bays, where the species co-occur and hybridize (Braby & Somero2006a). The percentage of M. galloprovincialis at a site is positively correlated with ambient salinity(Braby & Somero 2006a), an indication that factors in addition to water temperature may influencethe distribution of these two species. Within a single site, fine-scale differences in distributionthat reflect variations in temperature due to vertical position and exposure to the sun have beenreported (Schneider & Helmuth 2007, Elliott et al. 2008, Helmuth et al. 2010). M. trossulus is moreabundant in shaded intertidal habitats than in sun-exposed habitats, where M. galloprovincialis is


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more abundant. These fine-scale differences in relative abundances of native and invasive mussels,observed over distances of meters or less, predict that in habitats where a complex mosaic of abioticconditions exists, global change will lead to localized, species-specific shifts in distribution andabundance.

Will such a species replacement over a wide latitudinal range or at the local level have anysignificant ecological effect, or is this just a case of like replacing like? Whereas these two speciesmay be cryptic in terms of morphology, they are distinctly different in many ecologically relevantways. M. galloprovincialis is characteristically more robust in terms of growth and survivorshiprelative to its native congener and reaches much larger sizes (Braby & Somero 2006a, Elliottet al. 2008, Shinen & Morgan 2009). The invasive species is a strong interference competitorthat restricts movement and impedes feeding performances of the native blue mussel as well asthe native ribbed mussel, Mytilus californianus (Shinen & Morgan 2009). Thus, in addition tohaving several physiological traits that confer an advantage over the native blue mussel at highertemperatures (Lockwood & Somero 2011a), once established at a site, M. galloprovincialis exploitsbehavioral characteristics that further enable it to outcompete native congeners. It is noteworthythat M. galloprovincialis is the only congener of blue mussel that is a successful invasive species.Its ability to outcompete native blue mussels at numerous sites around the globe raises concernsabout widespread ecosystem change due to this single invasive species. Thus, understanding howabiotic factors like temperature and salinity govern the success of M. galloprovincialis may help usto predict and even control the further spread of this species.

Physiology: Cardiac Function

Increases in metabolic rate in ectotherms as temperature rises lead to challenges in providingsufficient oxygen to cells to allow aerobic scope to be maintained, to provide blood-borne substratesto fuel metabolism, and to remove metabolic end products, notably those that affect cellular andblood pH. The interactions between temperature, oxygen availability in the ambient water, andcirculatory performance illustrate the types of complex stress challenges faced by marine speciesbecause of global change. In analyses of climate change effects on aquatic species in particular,limitations in cardiac function that influence aerobic metabolic capacity have been a central focus,notably in the case of fishes (for review, see Portner & Farrell 2008, Farrell 2009, Portner 2010).However, as shown below, cardiac function in a wide variety of marine taxa may be one of theweak links in the physiological chain as global change progresses.

Mytilus. Although mussels have relatively greater abilities to rely on anaerobic production ofadenosine triphosphate (ATP) than more active taxa such as fishes, the broad biogeographicchanges and fine-scale distribution effects at a single intertidal site observed for the three bluemussel congeners may find partial explanation in terms of the temperature sensitivities of thespecies’ cardiac performance.

Heart rate rises with increasing body temperature up to a critical temperature termed theCTmax (also called the Hcrit), at which point further rise in temperature leads to a rapid reductionin heart rate (Braby & Somero 2006b). CTmax differs among the three blue mussel congeners,and for a given congener it varies with thermal acclimation. The relationship between CTmax andhabitat temperature for M. edulis suggests that truncation of the species’ southern range limit couldbe a reflection of limitations in cardiac performance. By 32◦C, a temperature at which high adultmortality is observed ( Jones et al. 2009, 2010), CTmax for heart function has already been exceededby several degrees. Thus, for 14◦C-acclimated M. edulis, CTmax is 25.50 ± 0.99◦C, and for 21◦C-acclimated specimens, CTmax is 28.50 ± 0.51◦C (Braby & Somero 2006b). How much further

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CTmax might increase through acclimation to even higher temperatures is not known. It has beenreported that M. edulis cannot be acclimated to temperatures above 28.5◦C (Chapple et al. 1998),and if the increase in CTmax were linear with acclimation temperature, rising approximately 0.4◦Cper degree Celsius increase in acclimation temperature (Braby & Somero 2006b), the potentialCTmax for cardiac function in 28◦C-acclimated mussels would still be below 32◦C. Thus, it isreasonable to conjecture that shortfalls in cardiac function contribute to establishing upper thermaltolerance limits of adult M. edulis and, thereby, help set the species’ southern latitudinal limit andits patterning within local habitats where a thermal mosaic pattern occurs.

Differences in tolerance of heart function to elevated temperatures also may account in part forthe biogeographic changes observed in native and invasive blue mussels on the U.S. West Coast.For specimens acclimated to 14◦C, CTmax is 23.70 ± 0.80◦C for the native species and 28.30 ±1.08◦C for the invasive (Braby & Somero 2006b). Acclimation to 21◦C increases CTmax to 26.00 ±0.59◦C and 30.70 ± 1.04◦C in the native and invasive species, respectively. Cardiac performanceat temperatures in the upper range of habitat temperatures measured in the zone where the nativeand invasive species co-occur thus would be superior in the invasive species. The competitivesuccess of M. galloprovincialis at high temperatures may be indicative of a common pattern—albeitone due to a variety of underlying mechanisms—in which rising ocean temperatures will enhancespecies invasions in the marine environment (Stachowicz et al. 2002, Geller et al. 2010, Sorte et al.2011b).

Crustacea. The importance of cardiac thermal sensitivity in setting distribution limits is likelyto vary among taxa, in part because species differ in ability to survive at temperatures above theCTmax of heart function. Mussels can withstand temperatures above CTmax if exposure times arelimited (Braby & Somero 2006b), as can some marine snails (Stenseng et al. 2005). However,in porcelain crabs (genus Petrolisthes), body temperatures above CTmax are acutely lethal, and norecovery occurs when temperatures are reduced below CTmax (Stillman & Somero 1996; Stillman2002, 2003).

The cardiac CTmax relationships discovered for congeners of Petrolisthes from different latitudesand different heights in the intertidal zone reveal important aspects of how thermal sensitivitymay differ within a genus (Stillman & Somero 2000). The most warm-adapted species (thosefrom low latitudes or highest vertical position in the intertidal zone) have CTmax values closer tocurrent maximal habitat temperatures than cold-adapted congeners (those from high latitudes orlower vertical positions). Additionally, the most warm-adapted species exhibit the least ability toacclimate to higher temperatures (Stillman 2002, 2003). Thus—perhaps counterintuitively—themost heat-tolerant species are in greatest danger from further increases in habitat temperaturedue to global change.

Snails. The differences in relative sensitivity to rising temperatures observed among Petrolisthescongeners are mirrored in interspecific differences in snails of the genus Chlorostoma (formerlyTegula) found at different heights in the intertidal zone. The species occurring highest in theintertidal zone, C. funebralis, exhibits greater heat tolerance (Tomanek & Somero 1999, Tomanek2002) and sustains heart function at higher temperatures than the low-intertidal and subtidalcongeners C. brunnea and C. montereyi (Stenseng et al. 2005). However, cardiac CTmax values ofC. funebralis are near the current upper body temperatures the species experiences, and CTmax

exhibits little acclimatory capacity. For the low-intertidal and subtidal congeners, CTmax valuesare several degrees above the species’ highest body temperatures and could be elevated by severaldegrees during warm acclimation.


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Fishes. Limitations in oxygen delivery under heat stress are likely to play especially critical rolesfor marine and freshwater fish, which lack the abilities to rely on anaerobic ATP production that arefound in many invertebrates, including mussels and snails (Hochachka & Somero 2002, Portner &Farrell 2008, Farrell 2009). Reductions in oxygen delivery at high temperatures may compromiseaerobic scope and, therefore, fishes’ capacities for locomotion in such critical contexts as predator-prey interactions and migrations. In the case of anadromous species like salmon, limitations incardiac performance may reduce their abilities to migrate successfully from colder marine watersto warmer riverine habitats where spawning occurs (Farrell et al. 2008, Farrell 2009). As rivertemperatures rise because of climate change, this challenge may increase and lead to limitationsin reproduction by some salmon populations.

Studies of tropical reef fish have shown that elevation in water temperature of only 2◦C–3◦Cabove current peak summer temperatures led to an almost 50% reduction in aerobic scope (Nilssonet al. 2009) and a significant reduction in growth rate (Munday et al. 2008). These data on tropicalfishes provide a further example of how close to the edge tropical ectotherms, both marine andterrestrial (Deutsch et al. 2008, Dillon et al. 2010), may be poised vis-a-vis threats from globalwarming.

Physiology: Stress-Induced Changes in Gene Expression

A primary determinant of a species’ ability to cope with changes in its environment is its comple-ment of protein-coding genes and gene regulatory elements needed for repairing stress-inducedcellular damage and generating adaptive phenotypic plasticity. Genomic (-omic) methods, broadlydefined to include studies of genome content and sequence, transcriptomics [messenger RNA(mRNA) populations in cells], and proteomics [protein populations in cells and their states of post-translational modification (PTM)] are yielding new insights into both the normal (nonstressed)status of cells and the influences of different types and intensities of abiotic stress on cellular phys-iology. Studies of stress-induced changes in gene and protein expression have elucidated a corecellular stress response that is exhibited by all taxa in response to a wide range of abiotic stresses,including changes in temperature, oxygen concentration, reactive oxygen species (ROS), salinity,and pH (Kultz 2005). With the development of -omic methods for studying this ubiquitous re-sponse, there is an unprecedented opportunity for marine scientists to develop multidimensionalbiomarkers for characterizing the states of natural populations of essentially all species, underconditions of different types and intensity of abiotic stress.

The development of DNA microarrays (gene chips) for Mytilus and other marine species hasenabled investigation of changes in expression patterns of thousands of genes as a consequence ofvariation in temperature (Gracey et al. 2004, Buckley et al. 2006, Lockwood et al. 2010), oxygenavailability (Gracey et al. 2001), and salinity (Evans & Somero 2008, Lockwood & Somero 2011b).These gene expression data provide insights into several of the central questions addressed by thisreview, including the following: At what point does stress first reach a threshold at which stress-related gene expression occurs? How does the pattern of expression of these genes—the typesof genes being transcribed and their levels of expression—vary with intensity of stress? Howdo these different threshold stress levels compare with ambient conditions found in the field,and how frequently are different classes of stress-induced genes switched on? Can interspecificvariation in gene expression provide insights into the relative effects of global change on differentspecies? How does recent acclimation or acclimatization history affect the threshold temperaturesat which stress-related genes are expressed? And how do exposures to different types of stress—e.g.,temperature and salinity—compare in terms of transcriptional responses?

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Mytilus. Studies of gene expression in field-acclimatized M. californianus have revealed complexpatterns of transcriptional changes related to specimens’ height of occurrence in the intertidalzone, exposure to solar heating during emersion, and periodicity of stress linked with the tidal cycle(Gracey et al. 2008). Figure 1a illustrates how induction of mRNA for the molecular chaperoneheat-shock protein 70 (Hsp70) varies with temperature for mussels found at a high, sun-exposedsite (Figure 1b). When body temperature rose to ∼28◦C, mRNA for Hsp70 increased significantly(∼twofold) relative to values measured at temperatures below the induction threshold (<28◦C).At ∼32◦C and ∼37.5◦C, Hsp70 messages increased ∼fourfold and ∼sixfold, respectively. Duringthis same period, no induction of Hsp70 mRNA was observed in mussels from the low, moreshaded collection site (Figure 1b), where body temperatures never exceeded ∼23◦C.

Much as the level of induction of Hsp70 mRNA changed with intensity of thermal stress,so did the types of stress-related genes that exhibited enhanced expression. A battery of genesrelated to proteolytic activity and suppression of the cell cycle were switched on only underthe highest level of heat stress, ∼37.5◦C (Figure 1a). This temperature is close to the upperincipient lethal temperature (LT50) measured for this species, 38.2◦C (Denny et al. 2011). Thesedata indicate that, as temperatures rose to approximately 28◦C, sufficient protein damage hadoccurred to require production of molecular chaperones to refold reversibly denatured proteins.However, as temperatures rose above ∼32◦C, protein damage was so severe that removal ofdamaged proteins by proteolytic processes (proteasomal activity) was required. Upregulation ofgenes linked to suppression of the cell cycle is suggestive of a cessation of growth (cell proliferation)under conditions of extreme stress.

The roles of vertical zonation and orientation to the sun in governing the degree of stressare evident from these data. Low-site mussels collected from a rock surface with low direct sunexposure and more time of immersion exhibited markedly lower levels of stress-induced geneexpression than high-site specimens over the same series of tidal cycles (Figure 1b). Costs relatedto recovery from stress-induced damage to the cell thus are likely to differ substantially over shortdistances in the thermally mosaic intertidal zone. Stress-related costs correlated with verticalposition and solar exposure are likely to explain in part the reduced growth and reproductiveeffort in higher-occurring mussels, which, as filter feeders during periods of immersion, also havereduced total feeding time (Petes et al. 2008).

Combining data on microhabitat thermal conditions and gene expression can provide an under-standing of the frequency with which different types of stress-induced changes in gene expressionoccur in the field. Figure 1c shows annual temperature variation at a site near the high site usedin the Gracey et al. (2008) study. Induction of heat-shock proteins is likely to occur on many days(denoted as moderate stress), whereas on only approximately 6 days did mussel body temperaturesreach the level that would trigger the more extreme stress responses noted at temperatures above∼37◦C (denoted as severe). If warming trends continue as climate change models predict, theremay be an increase in the number of days per year that intertidal organisms encounter levels ofstress that cause severe cellular damage and suppression of cell division. The resulting increasesin damage repair costs may so alter energy budgets as to necessitate concomitant reductions ingrowth rate and reproductive output. Further exploitation of microarray analyses in studies offield populations will shed further light on climate-related reallocations of cellular energy budgetsand shifts in physiological performance that have major ecological significance.

DNA microarray studies with blue mussels have provided insights into the types of interspecificvariations in gene expression that may contribute to differences in thermal tolerance among closelyrelated species. An oligonucleotide gene chip was used to compare transcriptional responses torising temperature and falling salinity in M. galloprovincialis and M. trossulus (Lockwood et al.2010, Lockwood & Somero 2011b). Of the 4,488 genes represented on the microarray used in


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Citrate synthaseMalate dehydrogenaseIsocitrate dehydrogenase

Cyclin Bγ-tubulinPolo kinase

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Thioredoxin domain-containing protein 4 precursor

Heat-shock protein HSP90-alpha

Heat-shock protein HSP90-alpha (HSP86)

Peptidyl-prolyl cis-trans isomerase B precursor

Heat-shock protein SSB

T-complex protein 1, beta subunit

Heat-shock 60 kDa protein, mitochondrial precursor

T-complex protein 1, epsilon subunit

T-complex protein 1, delta subunit

Gene expression level

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the acute heat-stress study, 1,531 showed changes in expression that were highly similar in bothcongeners, and 96 showed species-specific changes in expression (Lockwood et al. 2010). Thus,only a minor fraction of temperature-related gene regulatory responses differed between the cold-and warm-adapted species. Among the genes that exhibited interspecific differences were thosefor heat-shock proteins and the proteasome. Surprisingly, among the 21 genes on the array thatencoded Hsp proteins, only genes encoding a low-molecular-mass chaperone, Hsp24, showed aspecies-specific induction pattern (stronger induction in the invasive species). Another significantdifference between the native and invasive congeners was in expression of genes encoding eightproteins of the proteasomal complex. Induction of these genes commenced at 28◦C in M. trossulusand increased greatly at 32◦C. In M. galloprovincialis, no induction occurred at 28◦C and only minorinduction was noted at 32◦C. This difference in expression of proteasomal protein genes couldreflect interspecific differences in protein thermal stability, as suggested by the discovery of higherlevels of ubiquitinated (proteasome-targeted) proteins in M. trossulus than in M. galloprovincialisexposed to similar thermal conditions (Hofmann & Somero 1996). The increased levels of mRNAfor heat-shock proteins and proteins of the proteasome are paired with elevated levels of theproteins themselves (Tomanek & Zuzow 2010), a clear example of tight coordination betweenadjustments in the transcriptome and the proteome during stress (for a review of environmentalproteomics, see Tomanek 2011).

Global change may entail increases in precipitation as well as temperature, and for this reasonestuarine species in particular may be exposed to increasing hypo-osmotic stress. Through theuse of a microarray platform similar to that used in the study of acute thermal stress, the effectsof an acute reduction in salinity were examined on M. trossulus and M. galloprovincialis (Lockwood& Somero 2011b). A total of 117 genes showed significant changes in expression in both species,but only 12 genes showed interspecific differences in expression. As suggested by studies of geneexpression under acute heat stress, differences between species in environmentally driven generegulation events may involve but a minor fraction of genes and proteins.

A set of 45 genes showed significant changes in expression under both acute heat stress andhypo-osmotic stress. However, for the large majority of these genes, responses to heat andhypo-osmotic stresses were in opposite direction, notably for genes encoding proteins involvedin transmembrane movement of ions and organic solutes. Thus, the effects on gene expression

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−Figure 1Changes in gene expression in Mytilus californianus from low and high sites in the rocky intertidal zone at China Point (Hopkins MarineStation). (a) (Upper left panel ) Changes in expression of the gene encoding heat-shock protein 70 (Hsp70) across four tidal cycles at thehigh site (shown in right panel ), during which mussel body temperatures ranged from ∼13◦C to ∼37.5◦C. (Lower left panel ) Changes inexpression in high-site mussels of several genes encoding proteins associated with protein breakdown (proteolysis), including ubiquitin,sequestosomal protein, T-complex proteins, and amino acid transporters. (Right panel ) Tidal height (blue) and mussel bodytemperatures (red ) over four tidal cycles at the high site. Black arrows denote midnight on each day. (b) Contrasting levels ofstress-related gene expression in populations of M. californianus from adjacent low and high sites that differ in vertical position (tidalheight) and orientation to the sun. (Inset) Heat maps show temporal variation in gene expression for the group of genes listed in the textbox to the right. Each horizontal band represents a different gene, and each column is a different sampling time. Strong upregulation ofthe stress-related genes occurred in high-site mussels (right-hand heat map, rich in red, indicative of upregulation of gene expression),but minimal expression change was found in low-site mussels (left-hand heat map, rich in blue). (c) Mussel body temperatures over thecourse of 400 days in 2003–2004 at a site similar to the high site shown in panel b. Moderate stress temperatures are defined as those atwhich transcription of the gene encoding Hsp70 was induced; severe stress temperatures are defined as those at which transcription ofgenes associated with proteolysis and suppression of cell division was induced. (d ) Rhythmic expression patterns of eight genesassociated with aerobic adenosine triphosphate (ATP) production [tricarboxylic acid (TCA) cycle] and nine genes encoding proteins ofcell division (mitosis) in high-site mussels. Note the similar periodicities but opposite phases of expression of these two sets of genes.Panels a, b, and d are based on data in Gracey et al. (2008); panel c data are courtesy of Dr. Brian Helmuth.


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of simultaneous change in two or more abiotic factors may be additive or counteracting. Furthermicroarray studies with marine species will provide insights into the cellular-level effects ofmultiple stressors and help define the complex biological impacts of global change.

Fishes. DNA microarray studies of marine fishes have revealed a tiered response to increasingthermal stress consistent with the patterns seen in Mytilus congeners. In the long-jawed mudsuckerGillichthys mirabilis, a eurytolerant estuarine goby that withstands exceptionally wide ranges oftemperature and salinity, effects of acute thermal stress on gene expression were examined inspecimens acclimated to 9◦C, 19◦C, and 28◦C (Logan & Somero 2011). For all acclimation groupsa sequential pattern of induction of stress-related genes was observed, and induction temperaturesfor different sets of stress-induced changes in expression increased by approximately 2◦C foreach 10◦C increase in acclimation temperature. As in the case of Mytilus congeners, expressionof molecular chaperones like Hsp70 was an initial response to rising temperature and viewed asan indicator of low-to-moderate thermal stress. At slightly higher temperature, genes encodingproteins involved in proteolysis were induced, and at the highest stress temperatures, genes linkedto suppression of cell division were strongly upregulated. The latter finding again suggests thatsublethal thermal stress may lead to a rechanneling of energy flow in cells toward repair processesand away from growth (cellular proliferation). Acute heat stress also elevated mRNA for proteinsinvolved in ion transport (Logan & Somero 2010, 2011). This observation is consistent withrising costs for ionic and osmotic regulation at higher temperatures, and is another indication ofthe complex effects that multiple abiotic stresses arising from global change may have on cellularphysiology, especially energy budgets.

Transcriptomic and proteomic biomarkers: potentials and caveats. The insights beinggained from transcriptomic and proteomic studies about the types of damage that occur withincreasing levels of stress are facilitating development of biomarkers that will be helpful in di-agnosing the physiological status (e.g., capacity for growth) of natural populations. However,although the utility of -omic methods for gauging the status of field populations is likely to beconsiderable, important caveats must be taken into account when these methods are employed forthis purpose. One is the fine-scale variation in stress-related gene expression found over distancesof meters or less. This fine-spatial-scale variation raises a warning about use of microarrays tocharacterize populations over wide latitudinal ranges unless the specific thermal characteristicsof the sampling sites are also determined (Place et al. 2008). A second caveat arises from thetypes of temporal variation in gene expression found in the Gracey et al. (2008) field study ofM. californianus (Figure 1a,d) and in a recent study of corals (Levy et al. 2011). Gene expressionin field-acclimatized M. californianus exhibited a strong cyclical patterning, with genes associatedwith aerobic processes having a similar periodicity but opposite phase from genes associated withbiosynthetic events like DNA synthesis and cell division. Generation of greater amounts of ROSat high temperatures (Abele et al. 2002) is a potentially important aspect of heat stress. ROS maydamage a variety of cellular components, including DNA, so reducing use of oxygen during peri-ods of DNA synthesis may be adaptive. In M. californianus, this periodicity was much stronger inspecimens from the high site than in those from the low site, consistent with greater ROS pro-duction at higher body temperatures. The circadian gene expression patterns found in coral-algalsymbioses also may reflect temporal separation of oxidative (ROS-generating) and biosyntheticactivities (Levy et al. 2011). Experiments that apply gene chip technology in evaluating the physio-logical status of natural populations must incorporate these types of spatial and temporal variationsin gene expression and metabolism into their design. For intertidal species, the interplay between

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endogenous circadian rhythms in gene expression and periodicities in expression driven by tidalcycles must also be taken into account.

A final caveat to consider in the context of using -omic biomarkers is that changes at one -omiclevel do not map one on one with changes at another level. Thus, changes in the transcriptomedo not provide either a full qualitative or quantitative picture of changes in the proteome (Feder& Walser 2005, Tomanek 2011). And, as has long been appreciated by physiologists, the proteinpool of the cell does not, in and of itself, reveal the types and amounts of metabolic flux takingplace in the cell.

Physiology: Posttranslational Modification of Proteins

Another tier of regulation, PTM of proteins, is beginning to be examined in the stress responsesof marine species. Responses involving PTM can occur more rapidly than responses involvingtranscriptional control of gene expression, because PTM events involve covalent alterations (suchas reversible phosphorylation) of preexisting proteins. Many of the initial responses to environ-mental change involve covalent modulation of key regulatory proteins that control downstreamevents in regulatory cascades. Even though common sets of genes or metabolic events may be reg-ulated in different species in response to stress, initiating these responses falls to the activities ofupstream regulators controlled by PTM. Analyses of the sensors, signal transducers, and effectorsinvolved in stress regulatory networks suggest that a large fraction of the interspecific variation inthese complex networks lies in the sensing and signal transduction components of the system thatfunction in the initial period of the stress response (Singh et al. 2008). Thus, evolved differencesin sensing and signal-transducing elements in stress regulatory systems may be of major relevancein setting environmental tolerance limits.

How closely related species with different environmental tolerance ranges differ in terms ofPTM responses that initiate regulatory cascades is only now being elucidated. In Mytilus congeners,the three species found on the West Coast of North America exhibited significant differences inthe PTM reactions (phosphorylations) of several regulatory proteins in response to thermal andosmotic stress (Evans & Somero 2010). Though preliminary, these data are consistent with theconjecture that interspecific differences in regulatory responses reliant on PTM may be criticalevolved differences that govern different species’ responses to abiotic stress, such as the stressthresholds sufficient for initiating acclimatization. Differences among species in PTM-relatedresponses may be closely integrated with interspecific differences in transcriptional responses, suchthat the requisite changes in gene expression and protein function in response to environmentalchange involve a species-specific hierarchy of regulation. Adaptive variation at the level of PTMcontrol may play an important role in positioning species for success or failure in the context ofglobal change and thus is a subject meriting additional examination.

Physiology: Adaptive Variation in Protein Stability and Function

The discovery that genes encoding proteins involved in molecular chaperoning and proteolysisincrease expression at temperatures well within a species’ normal temperature range reflects afundamental property of almost all proteins, their marginal stability (Fields 2001, Hochachka &Somero 2002). Protein function almost invariably involves a change in conformation to enable thebinding, catalytic, and reversible assembly events associated with protein function to occur. Therequirement that proteins have sufficient structural flexibility to allow optimal function at normalcell temperatures renders proteins susceptible to perturbation from increasing temperature, whichtends to make protein structure more labile. Therefore, paired with the need for proteins to possess


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marginal stability is the need for repair systems (molecular chaperones) and degradation systems(the proteasome) that can be activated to refold heat-damaged proteins or, when damage exceedslimits of repair, to remove the proteins from the cell.

Evolutionary processes lead to a fine-tuning of protein structural stability to ensure that func-tion is optimized at the temperatures the cell normally experiences (Fields 2001, Hochachka &Somero 2002). Orthologous proteins from organisms evolutionarily adapted to different tempera-tures commonly exhibit differences in thermal stability such that an ortholog from a cold-adaptedspecies is more thermally labile than an ortholog from a warm-adapted species (Fields 2001,Somero 2004). These adaptive differences in structural stability lead to a strong conservationamong species, at normal cellular temperatures, in functional properties such as substrate bindingthat rely on an appropriate balance between stability and flexibility (Fields 2001).

In the context of climate change, it is pertinent to ask the following questions about theimportance of temperature-adaptive changes in proteins. First, how much temperature changeis sufficient to perturb the structure and, thereby, the functions of a protein to the extent thatselection will favor a compensatory evolutionary change in sequence? Second, are all types ofproteins equally sensitive to temperature, or are some proteins much weaker links in the large chainof protein-based processes? Third, how much change in sequence is needed to restore structuraland functional properties to values that are appropriate for the new thermal conditions? Fourth,are there hot spots in protein structure where adaptive change is localized? These questions, to agreater or lesser degree, have obvious bearing on the answer to a fifth and most critical question:Can adaptive evolution of proteins occur at a rate that will enable organisms to keep up with theeffects of a warming world?

Answers to some of these questions have come from studies of congeneric marine invertebratesand fishes that have evolved under different thermal conditions. Mytilus congeners have againprovided instructive lessons. Orthologs of the enzyme cytosolic malate dehydrogenase (cMDH)from M. trossulus and M. galloprovincialis exhibit different thermal responses in accord with theevolutionary histories of the species. cMDH of M. galloprovincialis is capable of sustaining optimalsubstrate binding at higher temperatures than the ortholog of its more cold-adapted congener,M. trossulus (Fields et al. 2006). Only two differences occur in the 334 amino acid sequence of thecMDHs of these two species. Only one of these substitutions is nonconservative and found at alocation that influences conformational flexibility. Site-directed mutagenesis experiments showedthat this one sequence difference accounted for the temperature-adaptive differences in function.

The finding that a single amino acid substitution in a region that influences conformational flex-ibility can achieve adaptive change has been reported in other studies of marine animal congeners,including limpets of the genus Lottia (Dong & Somero 2009) and fishes of the genera Sphyraena(barracudas) (Holland et al. 1997) and Chromis (damselfish) ( Johns & Somero 2004). Differences inevolutionary temperature of 3◦C–5◦C seem adequate to favor these adaptive changes in sequence(Holland et al. 1997). Thus, temperature increases of the magnitude predicted by climate changemodels are likely to favor selection for adaptive change in at least some types of proteins.

The extent to which different families of proteins are likely to be affected by rising temper-atures is an area demanding further exploration. The adaptive patterns discussed above were allobserved in enzymes undergoing large conformational changes during function. In contrast, astructural protein, skeletal muscle actin, showed no sequence variation among vertebrates adaptedto temperatures between −1.9◦C (Antarctic fish) and ∼43◦C (a thermophilic lizard) (Ream et al.2003). Thus, different families of proteins may have widely varying requirements for adapting toa warming world.

Of importance in the context of how rapidly protein evolution can occur in the face of globalchange is the amount of adaptive allelic variation present in natural populations. Allelic variation

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maintained by balancing selection may give a species substantial potential for adapting to changein temperature and other abiotic factors (e.g., Powers et al. 1993, Reusch et al. 2005). The roleof local adaptation in developing genetically distinct species populations having different ther-mal tolerances may also be important in a species’ response to climate change (for reviews, seeSanford & Kelly 2011, Sorte et al. 2011a). However, a recent study of 18 populations of the widelydistributed tide pool copepod Tigriopus californicus from sites separated by up to 17◦ of latitudeshowed that, whereas substantial local adaptation to temperature exists, there appears to be onlylimited capacity for these isolated populations to cope with further increases in temperature (Kellyet al. 2011). These and other genetically focused questions, including those of population size andgeneration time, demand much additional investigation for development of predictions about ratesof adaptation in the face of global change.

CASE STUDY 2: EXTREME STENOTHERMSOF THE SOUTHERN OCEAN

Examination of the types of genetic changes that are required for adapting physiological systemsto new environmental conditions must be paired with analyses of how contents of genomes changewhen selection is relaxed. Notably, for ectotherms that evolve for many millions of years in stableenvironments, some of the genetic information needed to respond appropriately to environmentalchange may have been lost through what is termed DNA decay (Harrison & Gerstein 2002).Lack of adequate purifying selection can lead to several types of losses from the genome. First,loss of protein-coding genes can occur when selection for retaining the genes’ products is lost.These losses may be virtually impossible to reverse. Second, disruption of open reading framesby point mutations can lead to loss of the corresponding protein. If disruption is due to only oneor a few nucleotide changes, reversal of this type of DNA decay may be feasible. Third, geneticpolymorphism (allelic variation) can be lost from populations, limiting their abilities to respond toenvironmental change in cases where the allelic variants lost are protein isoforms that are fit for thechanged environment. Fourth, regulatory regions of DNA may become dysfunctional, therebyreducing the organism’s ability to respond to changes in temperature or other environmentalfactors through appropriate transcriptional regulation. A fifth type of lesion, which might betermed translational decay, involves failure to translate certain mRNAs that, although transcribedappropriately, fail to generate protein products.

The challenges that these forms of DNA decay present in the context of global change in themarine realm are perhaps best illustrated by stenothermal ectotherms of the Southern Ocean.Many of the contemporary species of fishes and invertebrates of the Southern Ocean belongto lineages that have evolved for approximately 14 million years in waters noted for their lowand stable temperatures and high and stable levels of dissolved oxygen (Eastman 1993, Portneret al. 2006). Evolution under these conditions has been marked by a suite of adaptations to near-freezing temperatures, including development of protein and glycoprotein antifreezes as well asstructural and enzymatic proteins that function well in extreme cold (Fields & Somero 1998,Cheng & Detrich 2007, Portner et al. 2006). However, paired with these evolutionary gains area set of behavioral, physiological, and genetic losses that confer on these species an extreme levelof stenothermy. Heat death is common when temperature increases acutely beyond 4◦C–6◦C(Somero & DeVries 1967, Peck et al. 2009a), and acclimation ability (increase in heat tolerance)may also be very limited (Podrabsky & Somero 2006, Peck et al. 2009a). For a variety of Antarcticfishes and invertebrates, the upper temperature limit for survival after one month of acclimationranges between approximately 1◦C and 6◦C and averages only 3.3◦C (Peck et al. 2009a). Thermaltolerance is related to body size within a species and to activity level among species, with more active


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species exhibiting higher thermal tolerance (Peck et al. 2009a). Thus, climate change is predicted tohave sharply differential effects among different-sized individuals and among species with differentlevels of activity. One of the most telling findings is that for a species of Antarctic brittle star(Ophionotus victoriae), acclimation to 2◦C—a temperature <0.5◦C above current maximal summertemperatures in waters of the western Antarctic Peninsula (WAP)—is not possible (Peck et al.2009b). Behavioral impairment at temperatures only slightly above 0◦C has also been observed:For example, the Antarctic scallop Adamussium colbecki loses its swimming ability near 2◦C (Pecket al. 2004). The current rate of increase in sea surface temperature near the WAP (3.4◦C percentury) would seem to place stenothermal ectotherms dwelling in shallow or intertidal regionsof the WAP in danger of extinction (Schofield et al. 2010, Shevenell et al. 2011). In concert withfuture loss of endemic stenothermal species, entry of cold-adapted species from lower latitudesis already occurring in the rapidly warming marine ecosystems of the WAP (Schofield et al.2010). Ecosystems of the Southern Ocean, notably in the Antarctic Peninsula region, are thustrue canaries in the coal mine of global change.

Among the mechanisms responsible for the stenothermy of Southern Ocean ectotherms are thetypes of DNA (and translational) decay discussed above. Loss of an entire protein-coding gene, thatfor the β-subunit of hemoglobin (Hb), has occurred in the notothenioid family Channichthyidae,the white-blooded icefish (Cocca et al. 1997). A portion of the 5′ region of the gene for theα-subunit has been lost as well. These would appear to be irreversible lesions. Some speciesof Channichthyidae have lost the ability to produce myoglobin (Mb) as well. Loss of Mb hasoccurred at least three times in this lineage and involves two distinct mechanisms (Sidell et al.1997). Although all Channichthyidae species have retained the gene for Mb, some have disruptedreading frames. Others transcribe mRNA for Mb but fail to translate it into protein (Sidell et al.1997). Losses of Hb and Mb are likely to position channichthyids in challenging circumstancesas the Southern Ocean continues to warm. Warming will elevate metabolic rates and lower theconcentration of dissolved oxygen that is available to support aerobic metabolism, rendering fisheswithout oxygen transport proteins especially vulnerable to stress. A study by Beers & Sidell (2011)showed that these Hb-free fish had significantly lower tolerance of acute heat stress than Hb-containing members of Notothenioidei.

Another category of DNA decay that has been discovered in notothenioids as well as severalinvertebrate species is loss of the heat-shock response (HSR) (Hofmann et al. 2000, Clark & Peck2009). In the nototheniid fish Trematomus bernacchii, acute heat stress failed to induce synthesisof any size class of Hsp (Hofmann et al. 2000) or to increase transcription of any mRNAs forHsp proteins (except for the cochaperone Hsp40) (Buckley & Somero 2009). Loss of the HSRdoes not reflect loss of genes encoding molecular chaperones; these proteins are needed for nor-mal protein folding and compartmentalization in the cell, and notothenioids exhibit a normalsuite of molecular chaperones for these functions (Buckley & Somero 2009). What is lackingin notothenioids of the Southern Ocean [but not in their cold-temperate relatives from NewZealand (Hofmann et al. 2005)] is the ability to upregulate Hsp-encoding genes in response tothermal stress. These regulatory lesions could have a number of negative physiological effectsas ocean temperatures rise. Loss of the HSR may impair cells’ abilities to reverse heat-induceddamage to the proteome, should constitutively expressed levels of molecular chaperones proveinadequate for this function. More broadly, lack of the HSR may impair a number of cellularregulatory processes controlled in part by Hsp proteins. For example, the complex regulatorycircuitry that controls programmed cell death (apoptosis) incorporates Hsp70 and other molec-ular chaperones, which temporarily block apoptosis until the cell has had the opportunity torepair stress-induced damage, whether from heat or other chemical or physical stresses (Beere2004).

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DNA microarray analysis provides further evidence for impairment of temperature-regulatedgene expression in Trematomus bernacchii (Buckley & Somero 2009). Although a number of genesexhibit changes in expression in response to acute heat stress, the amount of change in mRNA con-centration is generally muted relative to the fold changes seen in similar thermal stress experimentsinvolving temperate eurythermal fish (Gracey et al. 2004, Podrabsky & Somero 2004, Buckley et al.2006). Notothenioids’ transcriptional machinery may have lost the types of responsiveness—inboth the qualitative and quantitative senses of that term—needed to cope with rising temperatures.Such loss of regulatory ability may be a critical factor in establishing the remarkable degree ofstenothermy found in ectotherms of the Southern Ocean.

Similar concerns about the adequacy of genetic resources for coping with climate change havebeen raised for tropical marine and terrestrial ectotherms (Stillman 2002, Merila 2009). Like ec-totherms of the Southern Ocean, tropical ectotherms commonly exhibit narrow environmentaltolerance ranges, live close to their upper temperature limits, and possess limited ability to accli-mate to higher temperatures (Stillman 2002, Deutsch et al. 2008, Tewksbury et al. 2008). Thus,these warm-adapted species have been viewed as especially likely to be challenged strongly byclimate change. The vulnerability of reef-building corals to even slight increases in water tem-perature is perhaps the most familiar example of dangers faced by tropical marine species underclimate change (Hoegh-Guldberg et al. 2007, Hoegh-Guldberg & Bruno 2010). DNA decay hasbeen suggested as playing a role in some of these instances of tropical stenotolerance, althoughmany of the strongest data come from studies of terrestrial species. For instance, among certaintropical congeners of Drosophila, highly specialized species adapted to a narrow range of habitatconditions lack sufficient genetic variation to cope satisfactorily with changes in temperature andwater availability (Kellermann et al. 2009). Thus, despite their very different physical environ-ments, the evolutionary histories of stenotolerant species under the stable physical conditions oftropical regions and the Southern Ocean have led to losses of genetic capacities that are likely tomake these species especially vulnerable to global change.

SUMMARY POINTS

1. Physiological analyses at the whole-organism, organ, cellular, protein, and genomic levelsare identifying aspects of acutely lethal and sublethal stress resulting from environmen-tal change that may affect biogeographic patterning and local distributions in mosaichabitats.

2. Species differ widely in terms of the threats they face from global change. Ectothermsthat have evolved in thermally stable habitats in the tropics and Southern Ocean maybe especially vulnerable to climate change because of the proximity of their upper ther-mal tolerance limits to current ambient temperatures and their limited capacities foracclimatization.

3. The amounts of adaptive variation in proteins and gene regulatory elements that dis-tinguish differently adapted species are being revealed through genomic and proteomicanalyses of congeneric species adapted to different abiotic conditions. Temperature-adaptive change in proteins may require but a single amino acid substitution, a findingwith implications for rates of evolution in a changing world.

4. Transcriptomic and proteomic analyses are revealing a tiered response to different inten-sities of abiotic stress, facilitating development of biomarkers for gauging stress exposureunder field conditions.


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5. Temperature and salinity stress elicit contrasting shifts in gene regulatory responses,illustrating the complexities of adaptation to co-occurring, multiple stressors associatedwith global change.

FUTURE ISSUES

1. Further development and judicious exploitation of -omic technologies for gauging theeffects of environmental change on physiological systems of marine species will helpto better clarify how individual stressors and interactions among several stressors asso-ciated with global change are impacting organismal function. In particular, these newapproaches may provide important new insights into how stress alters energy allocationamong processes for damage repair, growth, and reproductive output.

2. Genomic studies that focus on the genetic resources of marine species, including theamount of adaptive variation present in genomes, may allow predictions about the capac-ities of different species to cope with global change. Genomic analyses may also provideinsights into the extent to which adaptive change, especially to alterations in temperature,has occurred among different families of proteins. This genetic information may provideimportant new perspectives on how much evolutionary change is needed to cope withenvironmental alteration and, thereby, generate an improved basis for predicting howrapidly adaptive evolution can occur in response to global change.

3. Physiological studies, broadly defined, will be helpful to ecologists and biologicaloceanographers for developing models that can predict the biogeographic- and fine-scale distribution patterns of species and, thereby, ecosystem structures in a changingworld.

DISCLOSURE STATEMENT

The author is not aware of any affiliations, memberships, funding, or financial holdings that mightbe perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

I thank Drs. J. Beers, W.W. Dowd, and B. Lockwood for their helpful suggestions in developingthis review. I also acknowledge many stimulating and helpful discussions with the late Dr. BruceSidell that helped frame my thoughts about the issues treated in this review.

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MA04-FrontMatter ARI 16 November 2011 9:36

Annual Review ofMarine Science

Volume 4, 2012 Contents

A Conversation with Karl K. TurekianKarl K. Turekian and J. Kirk Cochran � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Climate Change Impacts on Marine EcosystemsScott C. Doney, Mary Ruckelshaus, J. Emmett Duffy, James P. Barry, Francis Chan,

Chad A. English, Heather M. Galindo, Jacqueline M. Grebmeier, Anne B. Hollowed,Nancy Knowlton, Jeffrey Polovina, Nancy N. Rabalais, William J. Sydeman,and Lynne D. Talley � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �11

The Physiology of Global Change: Linking Patterns to MechanismsGeorge N. Somero � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �39

Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic SeasJacqueline M. Grebmeier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �63

Understanding Continental Margin Biodiversity: A New ImperativeLisa A. Levin and Myriam Sibuet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �79

Nutrient Ratios as a Tracer and Driver of Ocean BiogeochemistryCurtis Deutsch and Thomas Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 113

Progress in Understanding Harmful Algal Blooms: Paradigm Shiftsand New Technologies for Research, Monitoring, and ManagementDonald M. Anderson, Allan D. Cembella, and Gustaaf M. Hallegraeff � � � � � � � � � � � � � � � � 143

Thin Phytoplankton Layers: Characteristics, Mechanisms,and ConsequencesWilliam M. Durham and Roman Stocker � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 177

Jellyfish and Ctenophore Blooms Coincide with Human Proliferationsand Environmental PerturbationsJennifer E. Purcell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Benthic Foraminiferal Biogeography: Controls on Global DistributionPatterns in Deep-Water SettingsAndrew J. Gooday and Frans J. Jorissen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 237

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MA04-FrontMatter ARI 16 November 2011 9:36

Plankton and Particle Size and Packaging: From Determining OpticalProperties to Driving the Biological PumpL. Stemmann and E. Boss � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 263

Overturning in the North AtlanticM. Susan Lozier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 291

The Wind- and Wave-Driven Inner-Shelf CirculationSteven J. Lentz and Melanie R. Fewings � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 317

Serpentinite Mud Volcanism: Observations, Processes,and ImplicationsPatricia Fryer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Marine MicrogelsPedro Verdugo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

The Fate of Terrestrial Organic Carbon in the Marine EnvironmentNeal E. Blair and Robert C. Aller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 401

Marine Viruses: Truth or DareMya Breitbart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 425

The Rare Bacterial BiosphereCarlos Pedros-Alio � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 449

Marine Protistan DiversityDavid A. Caron, Peter D. Countway, Adriane C. Jones, Diane Y. Kim,

and Astrid Schnetzer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 467

Marine Fungi: Their Ecology and Molecular DiversityThomas A. Richards, Meredith D.M. Jones, Guy Leonard, and David Bass � � � � � � � � � � � � 495

Genomic Insights into Bacterial DMSP TransformationsMary Ann Moran, Chris R. Reisch, Ronald P. Kiene, and William B. Whitman � � � � � � 523

Errata

An online log of corrections to Annual Review of Marine Science articles may be found athttp://marine.annualreviews.org/errata.shtml

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the physiology of global change: linking patterns to

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