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Evolution As a Critical Component of Plankton Dynamics

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Evolution As a Critical Component of Plankton Dynamics Received 7November 2002 Accepted 9January 2003 Publishedonline 31March 2003 Evolutionas a criticalcomponent of plankton dynamics GregorF. Fussmann 1,2* ,Stephen P.Ellner 2 and NelsonG. HairstonJr 2 1Institut fu¨rBiochemieund Biologie,Universita ¨tPotsdam,Maulbeerallee 2, D-14469 Potsdam, Germany 2Departmentof Ecology and EvolutionaryBiology, Corson Hall, Cornell University, Ithaca,NY 14853,USA Microevolution is typically ignored asa factor directly affecting ongoing population dynamics.We show herethat density-dependentnatural selectionhas adirectand measurable effecton aplanktonic predator– prey interaction.We kept populations of Brachionuscalyciflorus ,amonogonontrotifer that exhibits cyclical parthenogenesis,in continuousflow-through cultures(chemostats) for more than 900 days.Initially, femalesfrequently produced male offspring,especially at high population densities.We observed rapid evolution,however, towards low propensity toreproduce sexually, andby 750 days,reproduction had becomeentirely asexual. There wasstrong selectionfavouring asexual reproductionbecause, under the turbulentchemostat regime, males wereunable to mate with females,produced no offspring,and so had zerofitness. In replicated chemostatexperiments wefound that this evolutionary processdirectly influ- encedthe population dynamics.We observed very specificbut reproducible plankton dynamicswhich are explained well by amathematical model that explicitly includesevolution. This model accountsfor both asexual andsexual reproductionand treats thepropensity toreproduce sexually asa quantitative trait underselection. We suggest that asimilar amalgam ofecological andevolutionary mechanismsmay drive thedynamics of rapidly reproducing organisms in thewild. Keywords: Brachionuscalyciflorus ;chemostat;clonal selection;cyclical parthenogenesis; evolutionary dynamics;rapid evolution 1. INTRODUCTION The life cyclebegins whendiploid amictic femaleshatch from diploid diapausing eggs.Rapid clonal propagation of Population dynamicsand evolutionary dynamicsare often thesediploid femalescharacterizes theamictic phase.The treatedas separate fieldsthat require differentapproaches sexual phaseis initiated whenamictic (parthenogenetic) andmethodologies both in experimental andtheoretical femalesproduce mictic female offspring.Mictic females studies.In particular, thetwo dynamic processestra- producehaploid eggs that developinto haploid males if ditionally have beenbelieved tooperate ondifferent time- unfertilized.Fertilized mictic eggs,however, develop into scales,that is population dynamicsare rapid while evol- diapausing eggs that canundergo extended periods of dor- ution’s progress is slow(e.g. Khibnik &Kondrashov mancy.Amictic femaleshatching from diapausing eggs 1997). In many cases,however, evolutionary change can initiate another phaseof parthenogenetic reproduction, occurat rates comparable tothe rates at which theabun- and so on. dancesof populations andcommunities change anda High population densityof conspecifics has beenexper- growing numberof studies have demonstratedrapid evol- imentally establishedas an intrinsic stimulusfor thepro- utionat ecologically relevant time-scales(Thompson ductionof mictic eggs in B.calyciflorus (Gilbert 1963, 1998; Hairston et al. 1999; Hendry et al. 2000; Cousyn et 2002). Gilbert’s (1963) resultssuggest that therate of al. 2001; Reznick& Ghalambor 2001; Stockwell et al. mictic female productionis proportional tothedensity of 2003). In this study,we show how clonal selection femalesand that therotifers obtain information about the operating ona fundamentallife-history trait (thepro- currentpopulation densityvia theconcentration of oneor ductionof amictic versusmictic offspring) affectsthe several chemical substancesthat accumulatewhen rotifer dynamicsof plankton populations.We report resultsfrom densityincreases. This is consistentwith observationsof experimental populations ofcyclically parthenogenetic natural populations ofrotifers wherethe onset of mixis is rotifers whosedynamics can be accurately describedby a gradual andthe population consistsof mictic andamictic mathematical model (Fussmann et al. 2000). These femalescoexisting in variable fractions(Aparici et al. dynamicswere shaped by evolutionary change,so much 2001). sothat they couldonly becorrectly predictedwhen evol- Sexual reproductionof monogonont rotifers resultsin utionwas explicitly includedin themodel. theproduction of diapausing eggs,an essentialadaptation Brachionuscalyciflorus Pallas is amonogonontrotifer that ensuressurvival in thetime-varying environmentsthe speciesthat exhibits cyclical parthenogenesisin thewild; plankton inhabit. At thestart ofanewseason, genetic vari- apopulation persiststhrough time with phasesof amictic ance—represented by differentclones— is routinely re- (ameiotic) andmictic (sexual) reproductionfollowing one establishedthrough emergencefrom thedormant egg another in aseasonalpattern (e.g.Serra &King 1999). bank (Go´mez &Carvalho 2000). Recently,Gilbert (2002) performed crowdingexperiments with astrain of B.calyciflorus anddetected significant clonal variation in *Authorfor correspondence ([email protected]). thepropensity toproduce mictic femalesin responseto Proc.R. Soc.Lond. B (2003) 270, 1015–1022 1015 Ó 2003 TheRoyal Society DOI10.1098/ rspb.2003.2335 1016G. F.Fussmann andothers Evolution andplankton dynamics thecrowding stimulus. From theseobservations, and (b) Mictic andamictic rotifers becauseplanktonic rotifers typically undergomany gener- Forour study itwas crucialto be ableto distinguishbetween ationsof asexual reproductionduring aseasonalcycle, we micticand amictic B.calyciflorus . While male B.calyciflorus are suspectclonal selectionto have animportant, naturally considerablysmaller and morphologicallydifferent from recurring impact onthe population dynamicsof theseani- females,there are no morphologicaldifferences between mictic mals. In ourexperiments, mating ofmale andfemale roti- and amicticfemales. However, females produce any of three ferswas prevented by turbulencein theculture vessels. types of egg that canbe easily distinguished during routine This extreme conditionenabled us to study the effect of microscopicinspection: large, soft-cased subitaneous eggs clonal selectionagainst sexon the rotifer population (amicticeggs that hatch immediately,produced by amictic dynamicswithout any confoundingeffects of recombi- females),small soft-cased ‘male’ eggs (unfertilizedmictic eggs nation. that hatch immediately,produced by micticfemales), or large, Wefoundthat, after ca.2years,the propensity torepro- hard-cased diapausing eggs (fertilizedmictic eggs that go ducesexually had disappeared entirely from therotifer through aperiodof dormancy,produced by micticfemales). population. The rate at which this happenedwas Thus, for allegg-carrying femalesit was straightforward to especially high whenthe chemostat cultures initially determinewhether they weremictic or amictic. For those reachedlarge population size(including male production femalesin asamplethat werenot carryingeggs, we assumedthe by somegenotypes), and then, as the algal resourcewas sameratio of micticto amicticindividuals as found for the egg- depleted,decreased rapidly, thusproducing conditionsfor carryingfemales. The proportion of micticfemales among all strong natural selection.We combined replicated com- females p (‘micticratio ’;table 1)was estimatedas munity experiments andmathematical modelling todem- M 1 N [M /(M 1 A )] onstratethat theobserved dynamics were unlikely toresult pˆ = e e e e e , (2.1) M 1 N 1 A from population interaction alone butthat evolution of e e e therotifer population towardsasexual reproductionwas a where Me, Ae, and Ne arethe numbersof femaleswith mictic, critical componentof the dynamic process. amictic,and no eggs inasample,respectively. (c) Quantitativetrait (QT) model for mixis 2. METHODS evolution (a) Experiments andextra-experimental The QTmodel we propose hereis an extensionof amodel observations (F2Kmodel; Fussmann et al. 2000)we have previouslyused to Femalesof the rotifer B.calyciflorus werecollected from Mil- predictsuccessfully the dynamicsof nutrientsand interacting waukee Harbor, Lake Michigan,USA (courtesy of M.Boraas) populations of algae and rotifersin the chemostat system. The and axeniccultures were established using the unicellulargreen F2Kmodel is adoubleMonod model (Nisbet et al. 1983) that alga Chlorellavulgaris Beij.(UTEX no. 26) as food.We cultured doesnot allowfor mixis.It couldthus beexpected to produce these two speciestogether inflow-through culturesystems quantitatively accuratepredictions only for periodswhen rotifer (380ml glass chemostats) at 25 ± 0.3 °C,constant illumination reproductionwas almost exclusivelyamictic. Because our at 120 ± 20 m E m2 2 s2 1 (wide-spectrumfluorescent lamps) and experimentfell into a periodof extensivemictic reproduction useda culturemedium that containednitrogen at aconcen- and becausethere was evidencein the data for selectionagainst tration that limitedalgal growth (80 –514 m mol l2 1), plus non- mixis,we amendedthe F2Kmodel to includemictic females limitingconcentrations of other nutrientsand tracemetals: P, and evolutionof aQTrelated to mixis(bold type indicates S,B,Ca, K, Na, Mg,Cl, Fe, I, Li, V, Mn,Co, Cu, Zn, Se, these amendments): Rb, Sr,Mo; we addedvitamins B , B ,and biotinto ensure 1 12 dN the long-termsurvival of B.calyciflorus .Sterileair was bubbled = d(N 2 N) 2 F (N)C, dt i C through the chemostat vesselsto prevent CO limitationof the 2 dC 1
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