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EMBO reports VOL 9 | NO 1 | 2008 ©2008 EurOpEaN MOLEcuLar BiOLOgy OrgaNizatiON10

viewpoint viewpoint

Complexity in biology Exceeding the limits of reductionism and determinism using complexity theory

Fulvio Mazzocchi

t

he lme m of senf esehs o ndesnd he nl wold. inode o heve hs ol, Wesen

sene hs eled on dffeen onvesees, nldn smlfon, boh nems of nlss nd exlnon. as heBsh nl hlosohe S is Newon(1643–1727) , “th s eve o befond n he sml, nd no n he ml-l nd onfson of hns.” in w,exmles of smlfon nlde sndeled models, sh s ‘efe sheeolln down smooh lne n vm’;ondn exemens n sl on-olled envonmen sh s he lboo;nlsn omlex ssems b ednhem o he ndvdl s; nd enellb sn lne nd deemns oneof how he wold, nldn lfe, woks.

the Fenh hlosohe nd mhem-n rené Deses (1596–1650) ws hefs o node edonsm o Wesenhnkn nd hlosoh. aodn o hsvew, he wold n be eded s lok-wok mehnsm; o ndesnd , one needonl nvese he s nd hen essem-ble eh omonen o eee he whole.Deses’ wok ws exnded b Newon(1643–1727) nd lmel lmned nhe Principia Mathematica n 1687—one of

he mos nflenl sene books eve w-en—n whh Newon fhe dvned hede of ‘lokwok nvese’.

Sne he me of Newon, lsslmehns hs been eded s he fond-on of senf eseh. Senss, nld-n boloss, hve doed he Newonnoh boh he onolol level—nems of he oneon of he wold ndhe hns of whh s mde—nd heesemolol level—n ems of heoh o ndesndn hose hns. theNewonn esemolo, n f, ses h

senf knowlede hs o ovde n obje-ve eesenon of he exenl wold. thewold’s en omlex n be esolved

b nlss nd edn henomen ohe smles omonens. “One o hvedone h, [he evolon of henomen]wll n o o be efel el, eves-ble nd edble, whle he knowledeo ned wll meel be efleon of he-exsn ode” (Helhen et al , 2007).

Eve sne Newon fomled he fslws of v, he onel model of hehsl wold hd sessfll desbedhe she, movemens nd ons of heobjes whn . B s hsss beno exloe esell he om nd sb-om elms n he el weneh en-, he obsevons beme llmennless. the new dsovees eqed dm shf nd new nellelfmewok o ndesnd evens he sb-om level, whh evenll esled nqnm hss.

as mn of he molel boloss n he1950s me fom hss, s no ssnh he exended s lssl oho he sd of lvn onsms. Molelbolo, wh some exeons (Wesehoff & plsson, 2004), hs lel doed edons vew o exln bolol ss-ems odn o he hsl nd hemloees of he ndvdl omonens.as Fns ck (1916–2004) , “thelme m of he moden movemen nbolo s o exln ll bolo n emsof hss nd hems” (ck, 1966). in

de ose, edonsm oved o be nexemel owefl nll mehodolond enbled senss o nlse mn

bs molel nd elll oesses.

Noneheless, boloss mh be ehnhe lms of hs oh. Dese he beseffos, senss e f fom wnnn hew on ne, own lel o he omlexne of boh he dsese nd he hmnonsm. the hmn bn s omlex,nonlne ssem h defes ll edonsnd deemns ems o ndesnd (Sne, 2007). On mo level, eossemsnd hmn soees esen he sme hl-lene. Wh s needed s new oh osd hese ssems. comlex heo novde new onel ools h wll nev-bl qeson mn of he ssmons of Newonn sene.

comlex ssems exs dffeen

levels of onon h nefom he sbom elm o nd-

vdl onsms o whole olons ndbeond. the nlde, fo exmle, mole-les, ells, onsms, eossems ndhmn soees. Dese he dffeenes,hese ll she ommon fees, sh semeen oees. in ddon, ndom-ness nd ode e boh elevn fo hebehvo of he ovell ssem. the e,n f, nehe fed b omlee dee-mnsm, sh s he henomen h envesed b Newonn mehns, no

Since the time of Newton,classical mechanics has beenregarded as the foundation of scientific research

Complex systems exist atdifferent levels of organizationthat range from the subatomicrealm to individual organisms to whole populations and beyond

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science & society viewpoint

b ol ndomness, sh s he sbjesof ssl mehns (Helhen et al ,2007). comlex ssems exs on he ‘edeof hos’. the mh show el nd e-dble behvo, b he n ndeosdden mssve nd sohs hnes nesonse o wh seem lke mno modf-ons. the meho of he ‘befl effe’—wheeb snle befl ben s wnsn se som—desbes, fo exmle,he deendene of omlex ssem on snl ondons.

i s heefoe mon o nlsehow he lon of omlex heon ffe he sd of bolol ss-ems, n he elm of molel bolo,oo. ths dssson s mnl onened

wh he mlons h hese noonshve fo edonsm nd deemnsm.redonsm n l n be dsn-shed no hee es: onolol ed-onsm, whh ssmes h evehn hexss n ne s onsed b smllse of mve elemens h behve n el nd edble mnne; ese-molol edonsm, whh es hfndmenl ones, lws nd heoes of ven level of onon n be devedfom ones, lws nd heoes en-n o lowe level; nd mehodolol

edonsm, whh lms h omlexhenomen o ssems n nd shold bendesood b mens of nlsn hendvdl s.

an nesn nmbe of sensse h he edons ohn no lone oe wh boh he

enomos mon of nfomon h omesfom he so-lled ‘-oms’ senes ndehnoloes—enoms, oeoms, me-boloms nd so on—nd he sonshnomlex h he evel. the ssmonh omlex bolol ssems n be om-leel exlned b Deses’ lokwokmodel hs been eeedl qesoned. ashe Beln bolos M Vn reenmoel

ommened, move w “fom he ed-ons vewon nd oolse s hh -o fo boh bolol nd bomedleseh” (Vn reenmoel, 2004).

Fs, he edons oh s noble o nlse nd oel on fohe emeen oees h he-e omlex ssems. the geek hlo-sohe asole (384–322 bc) hd leddesbed emeene n hs eseMetaphysics s, “the whole s moe hnhe sm of s s.” ths, he whole ssemn nehe be eded no deded fom

he qles of s ndvdl s; vewnow held n ve of senf feldsnn fom hss o soolo.

Bolol onsms show emeenoees h se fom neons bohmon he omonens nd wh exe-nl fos. Fo exmle, he oees of oen e no eqvlen o he sm of he oees of eh mno d. poense ble o sefll lse hem-l eon, eone n nen o movelon nohe oen olme no onlbese he mno ds e ned n sef ode, b lso bese he hee- dmensonl se nd fnon eddonll deemned b exenl fos.

the noon of emeene s lso sso-

ed wh he de h he nl woldonsss of hehl levels of on-on h ne fom sbom leso moleles, eossems nd beond(De Hn, 2006). Eh level s boh h-eed nd ovened b emeen lws hdo no e he lowe levels of on-on. ths mles h, n ode o exln hefees nd behvo of whole ssem,we eqe heo h oees he o-esondn hehl level. Fo nsne,emeen henomen h o he levelof he onsm nno be fll exlned

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b heoes h desbe evens he levelof ells o momoleles. Howeve, heee lso vos enel fees nd h-ess—desbed n hs le—h e-mee ll levels of onon nd hllow he sd of bolol ssems n hefmewok of omlex sene.

ths hehl onon ees‘downwd son’ (De Hn, 2006).Whle he behvo of he whole s, o some

deee, onsned b he oees of s omonens—‘wd son’—hebehvos of s omonens e lso on-sned o en exen b he oeesof he ssem. the behvo of ell, foexmle, s onolled boh b he oeesof s momoleles nd b he oeesof he on of whh s . the wholes no onl moe hn he sm of s s, blso less hn he sm of s s besesome oees of he s n be nhb-ed b he onon of he whole. Fomn esemolol on of vew, hs mensh s no enoh o nlse eh nd-vdl (edonsm), no s enoho nlse he ssem s whole (holsm).a new model of senf nveson ondesnd omlex ssems wold eqeshfn he eseve fom he whole o hes nd bk n (Mon, 1990).

Seond, edonsm fvos heemovl of n obje of sd fom snoml onex. Exemenl esls

obned nde ven l ond-ons o fom l model—sh s mose, in vitro ell les o ome

models—e ofen exoled o moeomlex sons nd hhe onsmssh s hmns. B hs exolon s bes debble nd wos msledn oeven hdos. the fle of mn om-sn d nddes n lnl esehshows h s no lws ossble o ns-fe esls fom me o even mes ohmns (Hoobn, 2003).

Moe enell, he se of n heobje of sd n n fl, onolled ndsmlfed exemenl son, even f s done fo hes oses, s no nel

nd hs s e— seves he essenl lnkbeween he obje nd he nl onex owhh belons. phenomen nd oeesh o onl n he lvn envonmenbeome obsed nd skew he esls. Feldobsevons of hmnees, fo exmle,hve shown h hese nmls hve enomlex behvos h nno be obsevedn n fl sen b onl n he nlenvonmen (goodll, 1986).

thd, edonsm s lso loselssoed wh deemnsm—heone h eve henomenon

n ne s omleel deemned b e-exsn ses, os bese of neess,nd h eh l se odes nqe effe nd ve ves. ths, nll,lso ssns he de of edbl. “When

o e ble o ed he develomen of ssem fom some edefned ondon, heno hve esblshed deemns elonbeween he elemens whh onse hessem” (Emmehe et al , 1997). Noneheless,omlex bolol ssems nno be fllndesood on el deemns bss.in f, he ofen show nonlne behvo (De Hn, 2006).

as pointed out bove, the individulcomponents in complex systems intect inmnifold wys, including highly dynmicegultoy nd feedbck mechnisms(Vn regenmotel, 2004). Within this fme-wok, single cuse cn poduce multiplend unpedictble effects nd even smll fluc-tutions cn hve unexpected consequences.Line csul explntions—tht conceiveelity s line succession of elementyevents fom cuse to effect—e theefoepossibly unble to descibe how complexsystems behve (Kellenbege, 2004).

Neveheless, mn molel bolo-ss sll fvo smle models wh exl-nons bsed on few ndvdl fos.Fo exmle, knoko exemens—whh e wdel sed o deemne he

fnonl ole of ene—oveemhsehe ole of snle ene nd e of lmedse fo ndesndn omlex ene ne-woks. as me of f, mn knokoexemens hve no o nexeed effesbese n ven ene od s onl of omlex newok.

in ddon, ohe henomen n sehese nfoeseen fndns sh s eneedndn—he esene of dleenes n he enome—nd ene leoo,whh n led o sevel henoes bsedon he sme enoe (Mone, 2001).

Bolo, when bsed on edonsm nddeemnsm, seems o lk ssem es-eve h old nlse he neon of he mn fos h nflene he behvoof ssem (Vn reenmoel, 2004).

Foh, o bee ndesnd omlexbolol ssems nd he dvebehvo, we need o onsde he

henomenon of self-onon , whhnooes mn of he des menonedbove. Self-onn ssems sonn-eosl ne he omonens nd heneons no dve ses whemeen oees. Sh ses e bleo ee new nd modf exsn seeso d o hnn envonmenl ond-ons (coffe, 1998). comlex bololssems, n f, exs he ‘ede of hos’

whee, odn o Kffmn (1993), hee ble o heve mxmm fness. Self-onon seems o ke le dffe-en levels of bolol onon: s enel nle n he onon of heell self (Msel, 2001); n he esonse of bel olones o hemo sbses;nd n he bn, whh eones self olen fom exeene (coffe, 1998).

as menoned befoe, don s slssoed wh self-onon. Whlehe le s n nel fee of he ssemself, he fome shfs he eseve o heelonsh beween he ssem nd heenvonmen. Wheve he esse fom heexenl envonmen, omlex ssems—

hoh dnm vons n he deee of neons beween he ndvdl omo-nens h fom he newoks—n djs ndeone hemselves n new eqlbmn esonse o exenl evens. Of ose,fles n nd do o, neveheless,don seems o be he le he hnhe exeon (Helhen et al , 2007).

Whle n bo he Dwnnmeho of he onsm dn o senvonmen, he amen evolonbolos rhd Lewonn showed how hsde s bsed on dhoom beween nsde

…the reductionist approach isnot able to analyse and properlyaccount for the emergentproperties that characterizecomplex systems

An epistemological rethink isneeded to instigate a paradigmshift from the Newtonian model

that has dominated science,to an appraisal of complexitythat includes both holism andreductionism…




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nd osde, whh dseds he ole of heonsm n eonsn s envonmen(Lewonn, 2000). in f, onsms ne-he evolve n solon no sml d o‘exenl’ fos. On he on, he eo nd modf he envonmen od-n o he own needs. Boh onsm ndenvonmen heefoe ndeo onn-os oess of ml neon, whhLewonn emed o-don. a bolo-l ssem s onsned b s envonmen,b lso hnes s envonmen. ths demh be led b nlo, lhoh whdffeen mlons, o dffeen levelsof onon nldn, fo exmle, hemolel nd he elll levels (gle& Dhel, 2007).

in hs fmewok, seems h bol-

o, nd somehow sene s whole,needs o eonsde he noon of ‘n-

l lws’. reen develomens n evol-on bolo ses eln he deof deemns (esve) lw b non-esve lw h js ovdes nmbe of onsns. Moe hn lldeemnn he develomen of onsmso ohe omlex ssems, sh lws—f sonended—he delm he fmewok nwhh he o. in ohe wods, he ‘lws onsn’ esblshes he ‘les of heme’. i defnes esed feld of oss-bles, whn whh omlex ssemsdevelo, b who mosn nqew of ndeon hs oess. Ohemes shold be onsdeed, sh s heole of onnenes nd of hne, ndhe w n whh he ‘les’ se hesend del wh he exsn les (ce,1986). i seems h enewed nd moefsnn vson of ne emees whmh moe oom fo vbl.

Of ose, mn boloss ewell we of he omlex of lvnssems, b he do no exend hselon o esl of how oefom sene. “When one sehesfo he ‘lws of omlex’, one sllhes omlex s knd of wonbehnd he h loomove, h whhodes lws. a hbd ws fomedbeween he nles of donlsene nd he dvnes owds s

heefe. all, one vods he fnd-menl oblem of omlex, whh sesemolol, onve, dm.to some exen, one eones omlex,b b deomlexfn . in hs w, hebeh s oened, hen one es o lo :he dm of lssl sene emns,onl fssed.” (Mon, 2007).

an esemolol ehnk s needed

o nse dm shf fom heNewonn model h hs domned s-ene, o n sl of omlex hnldes boh holsm nd edonsm,nd whh elxes deemnsm n fvo of eonn nedbl s nns oomlex ssems. Moeove, hs ‘omlexdm’ eqes s o develo ‘knowl-ede of knowlede’ nd ndesnd s oss-bles nd lms. Sene shold no onlonne o develo moe efned menso nlse s sbjes, b lso nveses own oh o enen knowlede(Mon, 1990).

ths ses he mon qeson of heole of he obseve. clssl senehs develoed b elmnn sbje-

v n ode o ee objeve knowlede,b omlex heo hs enoded heobseve s n nns omonen n heoess of hen knowlede nd e-fomn eseh. the fmos nennle fomled b he gemn hssWene Hesenbe (1901–1976) shows howhe ‘obseve modfes he obsevon’. thsles no onl o qnm hss, b, b

exenson, n lso hve l elevnen he felds of boheml nd bololexemenon. as he Swss hss ndbolos Edd Kellenbee (1920–2004)woe, “fo he sb-moso wold of oms nd moleles, mens h he hs-l oees of ssem—fo exmle, sene—e nen; n l, heseoees deend on he e of obsevonh s efomed on h ssem, defned bhe exemenl se-. in he fshonblefeld of nno-boehnolo, whh exmnesbolol ses he level of oms,

hese elonshs e del elevn. Even le sle, he neons beween nexemenl se- nd bolol meve se o modfons oo; fo exmle,blehn dn floesene moso ohe eleon-bem-nded leon—shs bnn o bonon—of semen.”(Kellenbee, 2004).

Bodl sekn, he enodonof he obseve hs foseed enewedde of knowlede. insed of sehnfo one fndmenl on of obsevon,senss need o exloe dffeen onsof vew—whh n be vos n bld-n onve nvese—when desbno exlnn ven henomenon (ce,1986). Dffeen eseves n, n f,omlemen eh ohe nd llow sensso qe moe omlee knowlede of

he henomenon.

One of he mos fndmenl elon-shs whn hs fmewok s beween hessem nd s envonmen—he dsn-on beween on of vew h s whnhe ssem nd one h s exenl o hessem. these wo ons of vew e e-dble nd omlemen. the emeefom nd e defned wh ese o onenohe. the Fenh sens Hen aln,one of he fs who ed o defne om-lex n bolo, nvesed bololonon fom he eseve of nfo-mon heo. He sesed h, n he-hl ssem, he exenl obseve nbe he hhe ononl level (aln,1979). in exlnn he ole of ‘nose’, hesessed how s ‘menn’ deends on heobsevonl eseves: ledn ese-vel o deese o o n nese nnfomon onen “whehe one s ne-

esed n he nfomon nsmed n hehnnel o n he nfomon nsmed ohe obseve fom whole ssem n whhhe hnnel s of edndn omm-non newok” (aln, 1974). Fo exm-le, ell wold o sess nose n sommnon hws s mh ledo nexeed nd ossbl deleeoseffes, b n obseve hhe level—n on o he onsm—wold ednose s fo h neses vblnd heefoe ovell fness—ovded hhe ell s no klled.

…the reintroduction of theobserver has fostered a renewed

idea of knowledge

…key notions such asemergence, nonlinearity andself-organization alreadyoffer conceptual tools that cancontribute to transform andimprove science

Any constraint can also be anopportunity that, if exploited,allows new possibilities to arise




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anew heoel fmewok sholdheefoe be ble o nee dffe-en levels of ode whle llown

hem o mnn he dsnveness. Sh fmewok shold be onded on one of he ke ones of omlex hnkn, unitasmultiplex, odn o whh s ossbleo eseve dsnon mon wh s on-need nd o onne who edon(Mon, 1990).

ths fmewok needs o exend o heonon of knowlede. Eh domn of knowlede shold no be vewed s losedssem— vew h fmens knowlede.Eh e shold nsed e n bode oje fo he develomen of s-ene ble of esevn dves—ehfeld hs s own sef fees—b lsoensn he neon of he dffeen s

no one ommon fmewok.Bolo n heefoe be eded s

dslne wh sbdslnes h e-n o dffeen levels of onon(Emmehe et al , 1997). i needs, of ose,s own vobl nd ssem of one-lon, nd emns l ndeend-en of hems nd hss. ye, hesme me, needs o ‘ommne’ whhem, s well s wh ohe dslnesdevoed o he sd of ssems hhelevels, sh s eolo.

a esen, he mlfeed ‘om-lex dm’ onsss moe of nfed w of hnkn he hn

fnshed bod of knowlede. possblelons o he dffeen domns of knowlede need o be fhe nvesed.Noneheless, ke noons sh s eme-ene, nonlne nd self-ononled offe onel ools h nonbe o nsfom nd move s-ene. Novel ohes nd seledfelds of knowlede e led eme-n. Fo exmle, newok bolo (alm &akn, 2003; Bbs & Olv, 2004) kes

dvne of he f h dvese omlexnewoks, nldn bolol newoks,

seem o she sml ononl -ens. Some senss hve lso sessedhow sh hne n hve beneflonseqenes no onl he heoellevel, b lso n bomedl eseh shs d dsove nd vne develomen(Vn reenmoel, 2004).

Fhemoe, he esemolol sdeof omlex offes senss hne oefle on he hess nd lms of he senf oh o enen knowl-ede. Follown he noon of he obseve,senss shold be moe we h sen-f knowlede s lws develoed whnhe bond of ven onsns. ye, hsshold no be lmn fo. an on-sn n lso be n oon h, f exloed, llows new ossbles o se.Senss old heefoe qe moe

omlee knowlede of ven henom-enon f he exloe fom dffeen on-ve ‘hoons’, sh s ons of obsevon dffeen hehl levels, whh bve of he vosness, ooee ndomlemen eh ohe.

rEFErENcESalm E, akn ap (2003) Bolol newoks. Curr

Opin Struct Biol 13: 193–202aln H (1974) On foml defnon of

onon. J Theor Biol 45: 295–304aln H (1979) Entre le Cristal et la Fumée. ps,

Fne: Édons d SelBbs aL, Olv zN (2004) Newok bolo:

ndesndn he ell’s fnonl onon.Nat Rev Genet 5: 101–113ce M (1986) Il Vincolo e la Possibilità. Mln,

il: Felnellcoffe DS (1998) Self-onon, omlex

nd hos: he new bolo fo medne. NatMed 4: 882–885

ck FHc (1966) Of Molecules and Man. Sele,uSa: unves of Wshnon pess

De Hn J (2006) How emeene ses. Ecol Compl 3: 293–301

Emmehe c, Køe S, Sjenfel F (1997) Exlnnemeene: owds n onolo of levels.

Journal for General Philosophy of Science 28: 83–119

gle N, Dhel J (2007) coevolon whn ndbeween enes. in Gene and Protein Evolution.

Genome Dynamics, JN Volff (ed), vol 3, 1–12. Bsel, Swelnd: Ke

goodll J (1986) The Chimpanzees of Gombe:Patterns of Behaviour. cmbde, Ma, uSa:Belkn

Helhen F, clles p, geshenson c (2007)comlex nd hlosoh. in Complexity,Science and Society, J Bo, r gee (eds).Oxfod, uK: rdlffe (n ess)

Hoobn DF (2003) Moden bomedl eseh:n nenll self-onssen nvese wh lleon wh medl el? Nat Rev DrugDiscov 2: 151–154

Kffmn Sa (1993) The Origin of Order:Self-Organization and Selection in Evolution.Oxfod, uK: Oxfod unves pess

Kellenbee E (2004) the evolon of molelbolo. EMBO Rep 5: 546–549

Lewonn rc (2000) The Triple Helix. Gene,Organism and Environment. cmbde, Ma,uSa: Hvd unves pess

Msel t (2001) the one of self-ononn elll hee. J Cell Biol 155: 181–186

Mone M (2001) The Misunderstood Gene.

cmbde, Ma, uSa: Hvd unves pessMon E (1990) Introduction á la PenséeComplexe. ps, Fne: ESF Éde

Mon E (2007) resed omlex, enelomlex. in Worldviews, Science and Us:Philosophy and Complexity, c geshenson,D aes, B Edmonds (eds), 5–29. Snoe:Wold Senf

Sne W (2007) undesndn he bn. EMBORep 8: S16–S19

Vn reenmoel MHV (2004) redonsm ndomlex n molel bolo. EMBO Rep 5: 1016–1020

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Fulvio Mazzocchi is at the Institute forAtmospheric Pollution of CNR, Monterotondo(Rome), Italy.

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