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Rapid Cold-Hardening of Drosophila Melaivogaster (Diptera: Drosophilidae) During Ecologically Based Thermoperiodic Cycles

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Rapid Cold-Hardening of Drosophila Melaivogaster (Diptera: Drosophilidae) During Ecologically Based Thermoperiodic Cycles The Joumal of Erpcrintental Biology" 3t1-1.1659-1666 (2(Xll ) 1659 Pnnted in Crert Brrtrin {OThe Comprn! of Bioiogists Linrtcd l(X) I JEBl.l l8 RAPID COLD-HARDENINGOF DROSOPHILAMELAIVOGASTER (DIPTERA: DROSOPHILIDAE)DURING ECOLOGICALLY BASEDTHERMOPERIODIC CYCLES JONATHAN D. KELTYX ANDRICHARD E. LEE JN Departmento.f Zoology,212 Pearson Hall, Mictni Universir:^,Oxfnrd, OH 45056, USA *Presentaddress:TheUniversityoiChicago.Departnentof OrganismalBiotogyandAnatomy. l027E.57thStreet.Chicago, IL60637,USA (e-mail: j-kelty @ uchicago.edu) Accepted 7 Februart'; published ort WWW 5 April 2001 summary In contrast to most studies of rapid cold-hardening, in critical thermal minima (CI*i") decreasedby 1.9"C. Cold which abrupt transfers to low temperatures are used to hardiness increased with the number of thermoperiods to induce an acclimatory response.the primary objectives of which flies were exposed; i.e. flies exposed to six this study were to determine (i) whether rapid cold- thermoperiods were more cold-tolerant than those exposed hardening was induced during the cooling phase of to two. Endogenous levels of Hsp70 and carbohydrate an ecologically based thermoperiod, (ii) whether the cryoprotectants were unchanged in rapidly cold-hardened protection afforded vvas Iost during warming or adults compared rvith controls held at a constant 23 "C. ln contributed to increased cold-toleranceduring subsequent nature, rapid cold-hardening probably affords subtle cycles and (iii) whether the major thermally inducible benefits during short-term cooling, such as allorving D. stress protein (Hsp70) or carbohl'drate cryoprotectants melanogasterto remain active at lower temperatures than contributed to the protection afforded by rapid cold- they otherwise could. hardening. During the cooling phaseof a single ecologically based thermoperiod, the tolerance of Drosopltila melanogastertoth at-7"C increasedfrom 5+5 96survival Kev w,ords:acclimation. cold shock, cold tolerance. crvoprotectant. to 62.5t7.3 7o (means + s.E.\,l.,l{=40-60), lvhile their Hsp70.heat-shock protein. Drosophila nrclarutgctster. Introduction In contrastto most studiesof acciimation.which examine heniolymphincreases b), approximately300% (Chen et al.. phenornenainduced over prolongedexposures lasting days. 1987).On a time scalesimilar to that of rapidcolcl-hardening rveeksor evenmonths. a numberof studiesduring the past l5 (i.e. u'ithin minutes),l-righ temperatures elicit the svnthesisof years have be_gunto examinerelatively lapid processesof heat-shockproteins (Burton et al.. 1988:Goto and Kimura. acciimationto low and high temperature(for reviews,see 1998:Feder and Hotmann.1999). These proteins presumably Federand Krebs. 1997:Deniinger and Lee, 1998:Denlinger protectagainst thermal injury b;"acting as rnolecular chaperones. and Yocum. 1998). Upon exposureto rnoderatelylow minimizing the aggre-sationof non-native proteins and temperature.diverse insect speciesexhibit a rapid cold- promotingthe degradationand removalof both non-naiiveand hardeningresponse. ,,vhich within periodsof minutesto hours aggregatedproteins from thecell (Federand Hofmann.1999). enhancestheir cold-tolerance(Chen et al.. 1987;Lee et al.. Within an organism. a varietl, of therntal protective 1987:Coulson and Bale. 1990;Coulson and Bale. 1992:Kelty mechanismsmay act in svnchronv to prevent cellular and Lee. 1999).For example,prior exposureof housefly darnage(Feder and Hofmann. 1999).Substantial evidence (fuIttscttdoryestica) pupae to 0'C lor 90min increasedtheir denonstratesthat sugarsand poiyols botli serve protective sun'ival lblloiving treatmentlor 2 h at -7 "C from 0 7oto above rolesat lorvtemperatures and heip to stabilizenrenrbrane lipids 80Vc (Coulsonand Bale. 1990). Similarly, insectscan andcellular proteins at high temperature(Kim andLec. 1993: acclimaterapidly to irightemperature (Milkman. 1963: Levins. Ramoset al.. 1997).Siniilarlv. exposure to low temperaturc 1969:Chen et al.. 1991;Krebs and Feder. 1997). inducesthe explessionof stresspl-oteins, but onlv uponreturn The phl,siologicalrnechanisms underlvrng rapid acciimation to liigher tenlperatures.and high tempcrilturcsi.rock rncrelses to iow and high temperatureremarn poorlv understood.ln the toleranceof insectsto lorv ternperatul'cs(Burton ct al.. prepu'ationfbr rvinter,insects accurnuiate low-molecular-mass 1988:jopiin et rl.. 1990;Nunamaker et rl.. 1996:Yiangou et polyirvdriculcohols and sugarslDenlinger aud Lee. 1998). al.. 1997:Coto and Kirnura.l9c)8; Goto ct al.. 1998t.Thus. Sirrrilarly. during lapid cold-hardeningin Surt:ttltltuqu commolrelenreuts rnav underliea toicrancco1' lou, and high cra,;sipolpis.the givceroi concentrationwithin the pupal Iemperatufes. 1660 J. D. KslrY ,rNoR. E. LeEJn As a tirst stepin determiningthe ecological signiliclnce of the capacityfor rapidrcclimation to low or high temperature. we recentlydemonstrated that rvhenD. tnelutogttJterwere cooledat slower.and thus more natural. rates they exhibitedI signiticantly greater cold-rolerancethan did flies cooled (Kelty 1999). When cooied at at higher fates and Lee. i) ecologicallyrelevant rates (e.g.0.05"Cmin-r). flies not only exhibitedhigher rates of survivalat sub-zerotemperatures than = - IO their more rapidly cooled counterparts,but rapid cold- ! hardening provided them with proiection at I I "C. a temperaturethat flies llre more likely to encounterin nature thanthe near 0 "C exposuresused to elicitrapid cold-hardening in most previous studies.Furthermore. the fact that D. ntelurLogastercooled at slowerrates entered a stateof cold torpor (i.e. reachedtheir criticalthermai minimum or CTmin) et lower temperaturesthan those cooled at higher rates l6:00 l9:00 2l:00 0l:00 04:00 07:00 l0:00 ll:00 l6:00 provides strong evidencethat rapid cold-hardeningcould Time of day (h) beneht this speciesat the temperatul'esthev are likely to Fig. 1. The 2,1h thermopenodto rvhich Dntsctl.thilrtrnelunoqaster encoullterin nature. were exposed. Arrows representthe points at rvhich flies were the presentstudy. we investigatedrapid acclimationto In removedand their cold-toierance(assessed as survival atter I h at low temperaturesin D. melunogtLslerduring an ecologicallv -7'C and as CZ'nin)or heat-tolerance(assessed as sunival alter I h based thermoperiod. The cooiing phase of a single at i8 or l9"C) determined.The upper bar shows the l2h: l2h thermoperiodinduced substantialprotection against cold- light:darkphotoperiod. with the hlled region representingthe dark shock injurv. much of which r.vasretained during the rvarmin-Q period.CGriu, critical thermalminimum. phase of the thermoperiod.The increasedcold-tolerance appearedto be not only a tunction of the phase of the thermoperiodfiom which aduitswere removed. but was also shadedD. meltuutgctslerhabitat at lliami University's Ecology dependenton the numberot thennoperiodsto r.vhichthey had Research Center (Oxlbrd, OH. USA) during the spring, been exposed;flies exposedto multiplethermopenods were sul1rmerand autumn of 1996. These data lvere used to program substantiallvmore tolerantof low temperaturesthan flies an incubator to cycle beiween 9 " and l3'C ttver a period of exposedto a singlethermoperiod. 2-lh tFig. l); similar thermoperiodslrequently occulred during mid-spring and mid-autumn. The incubator was set to il photoperiodof l2h:i2h L:D. with the lights turned on at Nlaterials and methods 09:00h. lnsectreurttt? We first determinedwhether D. rneltmo,gasrarcold-hardened Drosoplilo rneltutogaster(Oregon-R strain) were reared rapidlv during the cooling phase of the programmed 'C undera long-davphotoperiod (15 h:9 h L:D) ct 23 in halt- thermoperiodand whether hardening rvas lost during warming. pint milk bottles containing DrosopliLtt medium (corn Flies rvere lightly anesthetizedrvith COt and transt'enedin rneal.molasses, yeast. agar) as tood and es a substratumtbr groupsof l0 into giassculture tubes (12x75mmt contlining oviposition.Nervll, emergecl adults were removed tiom bottles approximately0.3 ml of Drosophila medium and a t'ew -qrains daily and transt'erredto tresh medium on which they rvere of live velst.These flies were then allowed to recoverat 23'C allor.vedto teedand lay eg-rstbr 9 days.Within 8 h of eclosion' lor at lelst 6h. Afier recovery,flies rvere ti) kept at l3 "C tbr the llies rvere lightly anesthetizedwith CO:, segregatedby up to 6 davs,(ii) transt-enedto the thermoperiod(beginning at genderrnd transf'enedinto liesh bottlescontaining Drosopltila 23"C) for 0-6 days.(iii) keptat 16'C lbr up to 6 daysor (iv) rnedium.This enableclus to studv vilgin flies and cxamine rnaintainedat l3'C for txe clr hve additionaldays then potentialdit'ferences in the capacitvoi Inale and t-emaieD. subjectedto all or partof thethermoperiod. As outlinedbelow. tnelutoqttster-to cold-hardenrapidlv. Because age ma1'eft'ect the thernraltolerances of D. melunsester subjectedto the this capacitytCzcjka and Lce. 1990).all tliesrvere I davsold thermoperiodwere assessedat the times and temperatures lt the l'reginningtrf e'achexperiment. cxcept where the effect irrdicatedin Fig. 1.The thermaltolerances of D. rnelunoqasrer oC of agervas examined. heldat constantl6 or l3 wereassessed everv 1l-24h. 'f he rmtt p er i ttd e.rpe ri tn ent s Sun'ivuLut lott' untl li.qlt remperatures To deterntrnewhat thermoperioda tiuit lly is likelv to As an index of overall cold-hardiness.we assessedthe experiencein nature.a computerizeddata-accltrisition svstern caplcitv of D. rnelanogusterto survive I h tlf exposure to (CarnpbellScicntiflc. modei CRl0) rvas used to record
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