Omissions in the synthetic theory of evolution - SciELO Chile

The synthetic theory of evolution is considered the most unifying theory of life science. This theory is mainly based on neo-Darwinism, particularly on ...      ServiciosPersonalizados Revista SciELOAnalytics GoogleScholarH5M5() Articulo Inglés(pdf) ArticuloenXML Comocitaresteartículo SciELOAnalytics Traducciónautomática Indicadores CitadoporSciELO Accesos Linksrelacionados CitadoporGoogle Similaresen SciELO SimilaresenGoogle Compartir Otros Otros Permalink BiologicalResearch versión impresa ISSN0716-9760 Biol.Res. v.43 n.3 Santiago  2010 http://dx.doi.org/10.4067/S0716-97602010000300006  BiolRes43:299-306,2010ARTICLESOmissionsinthesynthetictheoryofevolution DanielFríasL.InstitutodeEntomología,UniversidadMetropolitanadeCienciasdelaEducación,CódigoPostal7760197,Santiago.Chile,E-mail:daniel.frias@umce.clABSTRACTTheSyntheticTheoryofEvolutionisthemostunifyingtheoryoflifescience.Thistheoryhasdominatedscientificthoughtinexplainingthemechanismsinvolvedinspeciation.However,therearesomeomissionsthathavedelayedtheunderstandingofsomeaspectsofthemechanismsoforganicevolution,principally:1)thebridgebetweensomaticandgerminalcells,especiallyinsomephylumofinvertebratesandvertebrates;2)horizontalgenetictransferencesandtheimportanceofvirusesinhostadaptationandevolution;3)theroleofnon-codingDNAandnon-transcriptionalgenes;4)homeoticevolutionandthelimitationsofgradualevolution;and5)excessiveemphasisonextrinsicbarrierstoanimalspeciation.Thispaperreviewseachofthesetopicsinanefforttocontributetoabettercomprehensionoforganicevolution.Molecularfindingssuggesttheneedforanewevolutionarysynthesis.Keyterms:Evolution,non-transcriptionalgenes,viruses,homeosis,epigénesis,imprinting,neo-Lamarckism,sympatricspeciation. INTRODUCTIONThesynthetictheoryofevolutionisconsideredthemostunifyingtheoryoflifescience.Thistheoryismainlybasedonneo-Darwinism,particularlyonMendelism,populationgenetics,mutations,naturalselection,gradualism,andthecentraldogmaofmolecularbiology.Thesearekeytopicstoexplaingenomechanges,speciationphenomena,andbiodiversity.Neo-DarwinismrootsarefoundinAugustWeissmann'stheoryofcontinuityofthegermplasm.Weismannestablishedthatorganismshavetwosetsofcells:somatoplasmandgermplasm.Inthelatter,thereareparticlesorbiospheresassociatedwithchromosomesresponsibleforthetransmissionofinheritedcharacters.Thus,Weismannlaidthefoundationsofchromosometheoryofinheritance.HerejectedLamarck'stheoryofacquiredcharacteristics,andchallengedalltheseideasofthenaturalselectiontheoryofCharlesDarwin.Thus,Neo-Darwinismemerged,byaddingWeismann'stheoryofthecontinuityofgermplasm(East,1929;Darlington,1937).TherediscoveryoftheprinciplesofMendelbyHugodeVries,CarlCorrensandErichVonTschermakstrengthenedNeo-Darwinism,andwiththecontributionsofFisher,Wright,Haldane,Dobzhasky,Mayr,Simpson,StebbinsandHuxley,"PopulationGenetics"and"TheSyntheticTheoryofEvolution"emerged.Sinceitsorigins,thistheoryhasdominatedthemindsandthoughtsofscientistsinexplainingthemechanismsinvolvedinthephenomenonofspeciation.However,importantomissionshavepreventedafullunderstandingoftheprocessesinvolvedinorganicevolution.Especially,thereislittleconsiderationregarding:1)thelackofabridgebetweensomaticandgerminaleukaryotecells,2)lateralgenetictransferencesperformedbyplasmidsandvirusesinthegenomeofeukaryotes,3)thelackofaholisticconceptofthegene,determinism,andgeneticreductionism,4)non-codingDNA,5)epigénesis,6)homeoticmutationsandthegeneticsofdevelopment,and7)sympatricspeciation.Thegoalofthisarticleistodiscussthesetopicstocontributetoabetterunderstandingofthemechanismsinvolvedinorganicevolution.TheabsenceofabridgebetweensomaticandgerminalcellsinsomephylumofinvertebratesandtheheredityofsomatoclonalvariationOneoftheassumptionsofpopulationgeneticsisthatgenesareverticallytransmittedtotheprogenyaccordingtothelawsofMendelianinheritance.Inthiscontext,andbasedonWeissmann'sbarriersbetweensomaticandgerminalcells,onlygeneticchangesthattakeplacewithingametesareinheritedbythenextgeneration.Nevertheless,inmanyinvertebrateorganismstherearenobarriersbetweensomaticandgerminalcells.Forexample,inthephylumporifera(seasponges)andcoelenterata(medusa)therearenodifferentiatedgerminallines.Sexualspongecellsoriginatefromacellulargroupdenominatedchoanocytesandarchaeocyteamoeboidsthathaveseveralfunctions,suchasobtaining,digesting,andtransportingfood,besidessexualandasexualreproduction.InthephylumEchinoderms,thereisagermlinewithlatedifferentiationduringembryonicdevelopment(StorerandUsinger1966;RuppertandBarnes1996).Thus,changesinthegeneticmaterialofsomaticcellscouldbeinheritedinthenextgenerationunderaneo-Lamarckianmodelofhereditybynaturalsomatoclonalvariation.Somatoclonalselectionfrequentlyoccursnaturallyinangiospermsthroughrhizomes,tubers,andstems(Hoffmann,1998).Althoughweknowagreatdealaboutnaturalcloning,thereisstillmuchtolearnaboutvegetativepropagationanditsevolutionaryimplications.Duetogreatadvancesingeneticengineeringandbiotechnology,themeaningofgeneticchangeshasbeenverifiedwithsomatoclonalcellsandsomaticembryogenesisthroughplantimprovement(Ahuja,1988;Mohanetal.,1988).Inaddition,thisoccursinmanyprimitivephylumofinvertebrates,suchasporifera,coelenterata,platyhelminthes,nemertinea,andbryozoa,byalternatingsexualandasexualreproduction;eitherbycelldispersion,transversalexcision,orbudding.Neworganismsmayarisethroughalltheseprocesses(StorerandUsinger,1966,RuppertandBarnes,1996).Thereisagreatregenerativepowerexistinginsomeofthesespecies,forexampletheplanarian(Turbellarian);anypieceofabodymaydevelopintoanewentirebeing(Legneretal.,1976).InachapterentitledTheHeredityofAcquiredCharactersofhisbookTheScientificBasisofEvolution(1943),ThomasH.Morganstated:"Itisnotknownifthenewworkinthefieldofgeneticsisamortalblowtotheolddoctrineoftheinheritanceofacquiredcharacteristics.Theolddoctrineheldthatamodificationofthebody'scells,producedduringdevelopmentorinadultstagesbyexternalagents,isinherited.Inotherwords:achangeinthecharacterofthesomaticcelldeterminesachangeinthegermcells."Morganthengaveargumentstoprovethefallacyoftheinheritanceofacquiredcharacteristics,usingstableheritabletraitsinDrosophila.Undoubtedly,manysuchargumentsaresolidandindisputable,butgenomicsequencingshowsthatthegenomeofmanyeukaryoticorganismshaveretrovirusgenesthathavefirstlyparasitizedsomaticcells.AccordingtoSteeleetal.,(1998)thebarrierbetweensomaticandgermcellscanbesortedthroughretrovirusandcouldberesponsibleforpaternaltransmissionofacquiredimmunologicaltolerance.Horizontalgenetictransferencesandtheimportanceofvirusesinthehost'sadaptationandorganicevolutionIntheclassicmodelsofpopulationgeneticsandheredity,smalleffectmutationsarethemostimportantcauseofevolutionarynoveltybywhichnaturalselectionacts.WithMcClintock'sdiscoveryoftransposableelementsinmaize,themechanismofvariabilitybecamemorehorizontal.Mobileelementsregulategeneticaction(McClintock,1950,1951)andcouldalsohaveevolutionaryimplicationsthroughtheinductionofhybriddysgenesisandsympatricspeciation(Syvanen,1984).SalvadorLuriain1959postulatedthattemperatebacterialvirusesmightplayaroleintheevolutionofthehost(Villarreal,1999).StebbinsandAyala(1986)providednewdataandamodernreinterpretationinordertoexpandtheSyntheticTheoryofEvolution.Inthatpublicationtheseauthorsaid:"Whennewgenesarisebyduplication,boththeoriginalandtheduplicatedgeneshavethetendencytobetransmittedcoupledtotheoffspringoftheorganismwheretheduplicationwasproduced.However,avariantofthisprocesshasbeendiscoveredthatconstitutesoneoftheways,apparentlycountlessoftheevolutionatthegeneticlevel.Occasionally,thegeneisfoundinaspeciesandtheduplicatedgeneispresentinadistantphylogeneticspecies.ThisphenomenoniscalledhorizontaltransferofDNAasitpassesfromonespeciestoanotherandco-existingwithit.Thishorizontalgenetictransmissionisopposedtoverticaltransmissionfromparentstochildrenthroughgametes.Therealmechanismsforhorizontalgenetransferareunknown.Probably,thevectorcouldbesmallring-shapedchainsofDNAcalledplasmid,capableoftransportinghereditarymaterialfromonecelltoanother."Withtheadventofgeneticengineering,wenowknowthatplasmidsandvirusesarevectorsintheframeworkofrecombinantDNAtechnology.TheimpactoftheselateraltransferencesbetweenbacteriaandprimitiveeukaryotesonorganicevolutionhasbeendetectedinthenewtreeoflifedescribedbyCarlR.Woese(1998).Accordingtothisnewtree,therearethreedomains:bacteria,archaea,andeukarya.Uniqueverticaltransferofgenesamongthesedomainsisnotconsistent.Itwasexpectedthateukarya,withtheexceptionofmitochondriaandchloroplastgenes,shouldhaveonlygenesfromarchaea.However,thisisnotthecase,becauseeukaryotesoftenhavegenesfrombacterialoriginthatarenotrelateduniquelytorespirationandphotosynthesis(Doolittle,2004).Horizontalgenetransferhasbeendescribedindetailincasesofbacterialtransformationmediatedbyviruses(restrictedandgeneralizedtransduction).Bacteriahaveobtainedasignificantproportionoftheirgeneticdiversitythroughtheacquisitionofsequencesfromdistantlyrelatedorganisms.Theselateraltransfershaveeffectivelychangedtheecologicalandpathogeniccharacterofbacterialspecies(Ochman,etal,2000,Bardarov,2002).Thehumangenomeshowsevidencethatgeneswerelaterallytransferredintothegenomefromprokaryoticorganisms.About40to113geneshavebeenfoundtobeexclusivelysharedbyhumansandbacteriaandareexamplesofadirecthorizontaltransferfrombacteriatothehumangenome(Salzbergetal.,2001,Villarreal2001).Inaddition,manytransposableelementsinthehumangenome,suchasLINES,SINES(longandshortinterspersedsequences),areclearlyrelatedtoendogenousretroviruses(ERV)embeddedinthehostgenome.Aswell,someDNApolymerasesfromeukaryoteshaveaviralorigin(Villarreal,2000,Villarreal2001).Humanchromosome21carries225protein-encodinggenes,butalsocarries2000ERVelements.About5%ofthehumangenomecontainsretroviralandrelatedsequences,similartoproportionsexhibitedbyotherspecies(PrakandKazazian,2000;Tristem,2000),whilealowerproportionofhuman,genome(about2%)containstructuralgenes.Aspartofthehostgeneticheritage,ERVaretransmissibletothenextgenerationinaMendelianmodel.Theirabundanceinanimalgenomesandtheirexpressioninprimarilygermcells,embryonictissueandcancercelllinesraisedthequestionoftheirbiologicalsignificance(Prudhommeetal.,2005).ThepresenceofERVinhumansandintheplacentaofothermammalshasbeenknownforthepast25years,butthesignificanceofthisobservationisstillnotfullyunderstood.ItisprobablythatancienttrophoblasticERVshadaroleintheevolutionanddivergenceofallplacentalmammals(Harris,1998).AllmammaliangenomeshavespecificanddistinctsetsofERVsandmuchgreaternumbersofdefectiveretroviralderivatives,suggestingthatmammaliangenomeswerecolonizedbyspecificlineagesofERVsoonafterplacentalspeciesradiatedfromoneanother.ThehumangenomeprojectindicatesthattherearethousandsofhumanERVsthatseemtocomprise24families.HumanshavebothancientandnewlyacquiredversionsofERVs,whichdistinguisheshumansfromcloseprimaterelatives.MammalsarephylogeneticallycongruentwiththeirERVs,whereasbirdsarenot.MostmammalsexpresstheircorrespondingERVsinplacentalandembryonictissues.Thisexpressionisneeded,possiblyforimmunesuppressionandothervitaldevelopmentalprocesses.ERVformspartoftheplacentalimmunosuppressivebarrierbetweenmotherandfetus,andtheirexpressionpreventstherejectionofthefetusbythematernalimmunesystem.Thishassolvedamajorproblemoflivebirth(viviparous)placentalmammals.Itcouldalsoplayaroleintheoriginofadaptiveimmunesystemsinanimals(Venableet.al,1995,Villarreal,1997,1999,2001,2003;Prudhomme,etal.2005).Therefore,theseERVviruseshaveasymbioticrelationshipwiththehost.AsimilarexampleofERVhasbeendescribedinDNAvirusesofparasiticwasps.MutualisticrelationshipswithpolydnavirushavebeendescribedinthefamiliesBraconidaeandIchneuminidae.TheDNAvirusisintegratedintotheparasitoidwasphostgenomeandseemstobethefirstdocumentedexampleofanintegrated,nonretroviralDNAvirusininsects,andverticallytransmittedasaprovirus(Fleming,1991).Thesevirusesareformedonlyincalyxcellsintheovaryofthewasp(WylerandLanzrein,2003).Whenfemalewaspsimplanttheireggsintohostcaterpillarlarvae,thevirusesarereleasedintothebodycavityofalepidopterahost,suppressingtheimmunesystem.Thisallowsthesurvivalofthewaspeggsandlarvaetodevelopintonewadults.Inthisway,polydnavirusinwaspsplaysaroleasanursecellbysurroundingtheeggsandlarvaeandblockingthecaterpillarhost'santi-parasitedefenseresponse(Villareal,2001).Theseexamplesinhumansandwaspsshowthatnotallviralinfectionsarepathogenic.Manyvirusescaninfecttheirhostpersistentlythroughoutthehost'slifetimewithoutdisease.Suchvirusescanbringtheviralseedsofgeneticcreationintotheirhost(Villareal,2001,2003).NucleotidesequencingofDNApolyadenvirushasrevealedacomplexorganization,resemblingaeukaryotegenomicregionmorethanaviralgenome.Althoughendocellularsymbiontgenomeshaveundergoneadramaticlossofgenes,evolutionofsymbioticvirusesappearstobecharacterizedbyextensiveduplicationofvirulencegenescodingfortruncatedversionsofcellularproteins(Espagneetal,2004).Theimportanceofheterochromatin,epigenesist,non-codingDNA,andnon-transcriptionalgenesIntheframeworkoftheVIIIInternationalCongressofGenetic,in1949,RichardGoldschmidtfinishedhisoralpresentationabout"heterochromaticheredity"withthenextquestion:"Shouldhetrochromaticmutationbeconsideredamajorfactorinmacroevolution?".However,inthesynthetictheoryofevolutionframework,theseideaswerenotaccepted.Evolutionistsatthattimefocusedtheirattentiononeuchromaticregionswhereproteincodinggenesarelocated.Yearslater,withtheadventofthecentraldogmaofmolecularbiology,structuralgenesbecameevenmoreimportantinevolutionarygenetics.Inthisconceptualspace,thegenewasstrictlyconsideredasasequenceofnucleotidesthatresultedfromaprotein.Therestofthegenomewasconsidered"uselessgeneticmaterial"or"geneticjunk".Heterochromatin,whereDNAsatelliterepeatsarelocated,mediatesmanydiversefunctionswithinthecellnucleus,includingcentromerefunctions,genesilencing,andnuclearorganization.RecentstudiesidentifiedmethylationofthehistoneH3tailasapost-translationalmarkerthataffectsacetylationandphosphorylationofhistonetailresidues,andalsoactsasarecognitionsignalforbindingofheterochromatinprotein1(HP1)(DillonandFestnstein,2002).Thesepersistentnon-geneticalterationsinchromatinhavebeennamedepigeneticchanges(Dangetal.2009).Thepost-translationalmodificationofhistonetailsgeneratea"histonecode"thatdefineslocalandglobalchromatinstates;theresultantregulationofgenefunctionisthoughttogoverncellfate,proliferationanddifferentiation(StralandAllis,2000).Otherepigeneticmethylationmarkersinthehistone3(H3)ineukaryoteXchromosomeshavebeencorrelatedtoactivegeneexpressionandalsotogenesilencing(Lachneretal.,2001,Nakayamaetal.,2001).RegulationofXinactivationinmammalsisanotherclassicexampleofepigenetics.TheoriginalchoiceofwhichXchromosomewillbeinactivatedoccursearlyduringembryogenesis.Inactivationisrandominthosecellsthatformtheproperembryo,whereasthepaternalXchromosomeisalwayschosenforinactivationinthosecellsthatwillformextraembryonictissues(ParkandKuroda,2001).Thislastepigeneticmechanismisanexampleofagenomicimprinting,similartothosedescribedinsexdeterminationofCoccids(Insecta)(Brown,1964,1966).Inrecentyears,DNAsequencinghasrevealedthatthehumangenomecomprises3billionbasepairs,butonlyapproximately2%correspondtoproteincodinggenesorstructuralgenes.Thereareotherfunctionalgenesinthisarea,suchasribosomalRNAandtransferRNA.Theremaining98%arenon-codingDNAlocatedinheterochromaticareasandrepeatedDNA.Studiesofmoleculargeneticshaveshownthatthesenon-codingDNAareusefulfortheorganismandhavebeencalled,inaholisticconcept,"non-transcriptionalgenes"(Frías,2004).Thus,inabroadconceptofgenes,theycorrespondtocodingornon-codingsequencesofDNAthathavearoleinthebody.Therefore,telomericgenes,centromericgenesandoriginofreplicationgenesarelocatedintheserepeatedDNAareas(Frías,2007a).Recently,non-codingRNAessentialingeneticregulationhasbeendiscoveredandinPearson'sopinion(2006)theycouldbecalled"genes".Atpresentweknowthatmanynon-codingRNA(smallRNAandinterferenceRNA)areimportantingeneticexpression.Manyofthesedouble-helixRNAhaveaviralorigin(LauandBartel.2003).Prokaryotesandvirushaveonlystructuralgenesthatarealsopresentinalleukaryotes.Therefore,thesegenescanbeconsideredas"precursorgenes"or"lowergenes"(plesiomophies)ofevolutionaryprocesses.Non-transcriptionalgenes,presentonlyineukaryotes,aremoreadvancedorhighergenes(apomorphies)(Frías,2007a).Inrecentyears,studiesofspeciationhaveprincipallyfocusedtheirattentiontoDNAsequencinginordertofindmoleculardiagnosticcharactersatthespecieslevel.Molecularphylogeniesdonotalwayscoincidewithmorphologicalphylogenies(Bitschetal.,2004,RubinoffandHolland,2005).Speciesdescriptionisstillbasedonmorphology,butmoleculartoolsappliedtophylogeneticanalysiscanbeagoodcomplementaryapproachtoinferevolutionaryrelationships.ThehomeoticmutationandthelimitationofgradualevolutionClassically,mutationswithsmalleffectshavebeenveryimportanttoexplaingradualisminorganicevolutionandbiodiversity.Homeoticmutationsthatregulatethedevelopmentofeukaryoteswerenotconsideredinitiallyinthesynthetictheoryofevolution.HomeosisisatermcoinedbyWilliamBatesonin1894inhisbookMaterialsfortheStudyofVariation.Homeoticmutationexplainsthereplacementofasegmentalstructurebyanotherduringdevelopment,forexample:eye-stalksandantennae(Goldschmidt1945a).In1915,CalvinBridgefoundthemutationBithoraxinDrosophila.Yearslater,GoldschmidtdescribedseveralhomeoticmutationsinD.melanogaster,particularlythoseinpodoptera,antenna-pediamutation,tetralteramutation(transformationofwingsintohalteres),andtretaptera(transformationofhalteresinwings)(Goldschmidt1945b,1945c).Inhisbook,ThematerialbasisofevolutionGoldschmidtproposedanewtheoryoforganicevolutionbasedonthesehomeoticmutationsandintroducingtheconceptsofmacroevolutionandmicroevolution(Goldschmidt1943).Goldschimidtthoughtthatthesemacromutationsexplainspeciation(macroevolution)bychangesinthedevelopmentoforganisms.Butthisviewwasnotconsideredbycontemporaryevolutionists(Dobzhansky,1940).Thecornerstonesofthesynthetictheoryofevolutionaremicroevolutionandgradualism,basedonmutationswithsmalleffects(poligenes).Themicroevolutionarymechanismsarethesameasthosethatoperateatdifferentlevelsofspeciesandexplaintheexistenceofhighertaxonomiccategories(macroevolution)suchasgenera,families,orders,class,phylumetc.But,forGoldschmidt,microevolutionarymechanismsdonotexplaintheformationofspecies,theyonlygeneratepolymorphisminpopulationsthatarefrequentlyreversible.Homeoticandsystemicmutationarefundamentalfactorsontheoriginofnewspeciesandonotherhighertaxonomiccategories.Manyhomeoticmutationsarenotadaptivewhileotherscouldbe.Forinstance,themutationofophthalmopteradescribedbyMorganinD.melanogaster,whichappearsaslargeinflatedexpansions,usuallyoriginatingintheeyes,isnotanadaptivemutationinDrosophila.Nevertheless,inseveralspeciesofthegenusPhytalmia(Haplostomata,Phytalmiidae)themaleisadornedwithexpandedoutgrowthsfromitseyes,bearingaremarkableresemblancetothemoreextremetypesofophthalmopterafoundinDrosophila.Thus,thesehomeoticmutations,whicharemonstrositiesinDrosophila,appearasanormaltaxonomicfeatureoftheotherfly(GoldschmidtandLederman-Klein,1959).Manyotherexaggeratedstructureshavebeendescribedininsects,generallyseeninmales,thatareusefulforsexualselection(Whittington,2006;EmlenandNijhout,2000).CurrentlytheworksofGarcia-Bellido(1977)andLewis(1978)onDrosophilahomeoticmutationshavebecomefundamentaltoexplainthegeneticbasisofdevelopmentandevolutionineukaryoteorganisms(Carroll,1995).Homeoticgenesarehighlyconservativeandhaveanimportantroleintheregulationandexpressionofthegeneduringthedevelopmentofeukaryotes.Thesegenesarefoundinthemostprimitiveinvertebrates,vertebratesandplants(Buschetal.,1999Shenketat.,1993)andalsointhehumangenome.MajorgenesareHoxandPaxgenesthatproducedisturbancesinearlydevelopment.ThehumanHoxgenesshowhomologywithhomeoticboxgenesofDrosophila.Paxgenescontainanucleotidesequencecalledpairedbox,originallydescribedinasegmentationgeneinDrosophila(Solari,1999).Inmosttaxa,genotypicchangesaremorphologicallymanifestedtocauseevidentphenotypicdiscontinuitiesindifferentpopulations.Basedonthesediscontinuitiesandfossilevidence,thepaleontologistsEldredgeandGould(1972)postulatedthetheoryofpunctuatedequilibria;analternativetophyleticgradualism.However,sometimes,morphologicalchangesareminimal,resultingincrypticspeciescomplexes.Inthesecases,thegreatestdifferencesarefoundinthebehaviorofindividuals.Theevolutionaryleapisnotmorphological,butratherbehavioralandecologicalandthenewmechanismofreproductiveisolationispre-mating.Anotheraspectthathasnotreceivedsufficientattentioninneo-Darwinismischangesinmorphologyduetoheterochronyandepigénesisduringdevelopment.ConradH.WaddingtonandRichardGoldschmidtwarnedaboutthisexclusioninatimelymanner,buttheirclaimswerenotconsideredbyothercontemporaryscientists(Reig,1991).Afewyearslater,Gould(1977)proposedamodelprimarilybasedondevelopmentacceleration(hypermorphy)orretardation(neoteny).Bothprocessescausemorphologicaldiscontinuitiesandcouldgiverisetonewspecies(Frías2009).ExcessiveimportancetoextrinsicbarriersinanimalspeciationThemodeofspeciationinnaturalpopulationsisacentralprobleminthesynthetictheoryofevolution.InTheOriginofSpeciesDarwinconsideredspeciationassynonymoustoevolutionandthatonespeciesproceedspre-existingspecies.Romanes(1897)calledspeciationthetransformationofaspeciesovertimeanditsmultiplicationinthespace(Mayr,1949).Thereisconsensusthatnewspeciesarisewhennewreproductivemechanisms,post-copulatoryorpre-copulatory,appearandsuspendthegeneflowamongpopulations.However,thereisnoconsensusifthesenewisolatingmechanismsariseinsympatry,allopatryorparapatry.Thus,aprobleminspeciationisunderstandingtheoriginofintrinsicisolatingbarriersthatpreventthegeneflowinsympatry.Anothertaskisunderstandingwhichevolutionaryforcesproducedthesebarriers(CoyneandOrr,2004).Theallopatricmodelisthemostwidelyacceptedmodelofspeciationintheframeworkofthesynthetictheoryofevolution.ErnestMayrwasthearchitectthismodel,inwhichinteresthasfocusedongeographicspeciation(Mayr,1949,Mayr,1968).Thismodelisdesignedasaprocessofchangeinabiologicalsystemduetoexternalforces.Theexistenceofanextrinsicbarrierisaprerequisitetotheemergenceofnewreproductiveisolationmechanismsandnewspecies(Mayr,1949).Therefore,thisisamechanisticmodelinwhichanimalbehaviordoesnothavearolewithoutapriorinterruptionofgeneflowamongpopulationsbyanextrinsicbarrier(Reig,1991).Consideringthatseveralmillionspecieshavebeendescribedandmanyothershavenotyetbeendescribed,therearenotenoughgeographicalbarrierstoexplaintheoriginofnewintrinsicisolationmechanismsandspeciationinallopatricconditions.Apparentlytheallopatricmodelisnotthemostparsimoniousmodeltoexplainspeciation.Intrinsicmechanismsofspecies,suchashomeosis,chromosomalrearrangements,developmentgenetics,epigénesis,andbehavioralimprintingcouldbethemostcommontoexplaintheoriginofnewisolationmechanismsandspeciationinsympatryorinsemi-geographicconditions.Asanalternativetoallopatricspeciation,BenjaminWalsh(1864)offeredatheoryinwhichahostraceofphytophagousinsectsevolvesinsympatry.InTheOriginofSpecies,DarwinemphasizedWalsh'sideaoftheoriginofnewvarietiesandspeciesofphytopagousinsectsinsympatry.MaynardSmith(1966)proposedatheoreticalmodelforsympatricspeciationthroughdisruptiveselectioninatwonichesituations.GuyBush,studyinghost-raceformationinRhagoletispomonella(Walsh),hasbeenthemaindefenderofsympatricspeciation.Ithasbeenshownthatthechoiceofanewhostplantcanseparatepopulationsjustasamountain,anoceanorarivercan(Gibbons,1996;Wu,1996;Via,2001,Frías,2005,Frías,2007b).Precopulatoryreproductiveisolationinsympatryhasbeenextensivelydemonstratedinphytophagousinsects,especiallyinthefamilyTephritidaeofDíptera(Bush,1969,1994,Federetal,1994,Frías1989,2001,2005).Malesandfemalesshowhostfidelityandtheirentirelifecycletakeplaceonhostplants.Hostfidelityismainlyduetotwoclassesofodorant:a)characteristicodorreleasedbyplants(ChristensonandFoote,1960)and,b)pheromonesreleasedbymalesandfemalesontheirhostplants(Katsoyannos,1975;Prokopy,1976).Theolfactorysystemofinsectsconsistsofthreeclassesofproteins:1)odorantbindingprotein(OBPs);2)olfactoryreceptors(ORs);and3)odorantdegradingenzymes(ODEs).OBPsconstitutemulti-genefamiliesandconsistoftwogroups:1)bindingproteinsofgeneralodorant;and2)pheromonebindingproteins(Sanchez-Gracia,2005).Changesinchemicalsofplantsandinproteinsofodorantreceptorsinfliesmayexplainhostchangesundersympatry.Mostparadigmsofsympatricspeciationinvolvecolonizationbyaphytophagousinsectofanintroducedcultivatedhostplant(Bushl969,Frías2007b).Recentlyhowever,amodelofsympatricspeciationhasbeenpostulatedthroughtheco-evolutionbetweenspeciesofthegenusTrupanea(Tephritidae)andtheirhostplantsofthegenusHaplopappus(Asteraceae),basedonthehybridizationofhostplants(Frías,2005).Comparedtoothermodelsofsympatricspeciation,thisisthemostparsimoniousmodelofspeciationbecausethehybridplantisonlydistributedtoplaceswherebothparentalplantscoexist,correspondingtoaprimarystateoftheevolutionofpolyploidcomplexesinplants,ashasbeenpostulatedbyStebbins.ThenewspeciesTrupaneasimpatricaisassociatedwithhybridplantsandderivedsympatricallyfromaT.foliosispopulation,whichisassociatedwithoneoftheparentalplants(Frías,2005).Sincefrequentnaturalhybridizationtakesplacesimpatricallyamongangiospermspecies(Grant,1981),themodelofsympatricspeciationinphytophagousinsects,involvingcolonizationofnewlyestablishedhybridplantspecies,couldbeverycommonininsectsassociatedwithAsteraceae(Frías,2005).RecentstudiesofmolecularbiologyinthenervoussystemofDrosophilaprovideabasisforunderstandinghowlearnedbehaviorofthelarvaecouldbeinheritedbytheadult.IthasbeenfoundthatsomenervecellsofthecephalicganglionofDrosophilalarvaecontributetoformingthenervoussystemofadults.(GerberandStocker,2007).StudiesoftheparasitoidwaspAphidiumervihavedemonstratedthatodorlearningduringimmaturestagesistransferredtoadults,suggestingthattheacquisitionofanolfactorymemoryduringthelarvalstagepersiststhroughmetamorphosis(Gutierrez-Ibañezetal.2007).Thesefindingsindicatethathostfidelitycouldalsobedeterminedbybehavioralimprintingintheframeworkofaneo-Lamarckianmodel.Althoughsympatricspeciationbyhybridizationandallopolyploidyinplantsiswidelyaccepted,Gallardoetal.(1999)discoveredpolyploidyinamammal.Thisfindinggaveawindowtosympatricspeciationinanimalsintheabsenceofgeographicbarriers.Anothermodelofspeciationwithoutgeographicbarriers,insemi-geographicconditionsorparapatricspeciation,occursthroughintrinsicbarrierscausedbychromosomalrearrangementsandnegativeheterosisofhybrids(White,1974;White,1978;FríasandAtria1998;Gravilets,2000).Torefertothesekaryotypeschanges,Goldschmidtintroducedtheconceptof"systemicmutation"basedonthetransformationofintra-chromosomalpattern.Anewspatiallydifferentrearrangementofintrachromosomalconstitutionoriginatesfrominversion,translocations,orheterochromaticmodifications.Andthusanew,stablesystememergesthatleadstospeciation(Goldschmidt1943;Bush,1982).Stegnii(1996)extendstheconceptofsystemicmutationincorporatingthosechangesthatleadtonewrearrangementsofthechromocentricapparatus,aswellaschangesrelatedtothechromosome-membraneconnectionsystem.Goldchmidt'sideascontributedsignificantlytounderstandingtheroleofchromosomalrearrangementsinthespeciationofcertaingroupsoforganisms,especiallyinDrosophilaspecies(Dobzhansky,1973;Brncic,1957).However,therolesofheterochromaticchangesandchromocentricapparatushavenotbeenextensivelystudied.Ithasbeenarguedthatmacroevolutionhasarelationshiptocentromericandtelomericheterochromatinchangesandalsotochangesinthechromocentricapparatusforspeciesbelongingtotwodifferentphyleticgroups,Díptera(Tephritidae)andMepraia(Reduviidae).Allthesechomosomicrearrangements,especiallythoseinMepraiaspp,explainhowpostcopulatoryreproductiveisolationmechanisms,withoutanextrinsicbarrier,originated(FríasandAtria,1998;Frías,2009).CONCLUSIONItisclearthatthegeneticcodeisfoundinstructuralgenes,lowergenesorancestralgenes,whicharesharedwithvirusesandprokaryotes.Apparentlyhowever,muchofthegeneticprogramthatmakesdifferentiationanddevelopmentofamulticellularorganismspossibleisinnon-codingDNA,wherenon-transcriptionalgenes,transposableelementsandendogenousvirusesarelocated.Thesegenesarelinkedtotheadventofnewandvitalrolesineukaryotes,suchaschromosomeorigin,mitosis,meiosis,celldifferentiationanddevelopment.However,thegeneticprogramisnotonlylocatedintheDNA,butalsoinhigherlevelsofgenomicorganization.IthasbeenarguedthatDNAmethylationisastableepigeneticmodificationandgeneimprintingthatevolvedindependentlyinangiospermplantsandmammals.(Hsiehetal.,2009;Gehringetal.,2009).Duetogenomicimprinting,epigeneticchangesareinheritedinadifferentmannerfromMendel'sprinciples.Thegeneticcodeisuniversal,herewefindthebasicelementsofthegeneticprogramresponsiblefordevelopinganeworganismandnewlifeforms.Thisprogramisexpressedorterminatedduetogeneticandepigeneticinformationandexternalenvironmentalconditions.Speciationalwaysinvolvesgenotypic,epigenotypicandphenotypicleaps.Smallleapsoriginatespecies,largeleapsoriginategenera,otherlargerleapsoriginatefamilies,andthusprogressivelylargerleapscouldevenexplaintheemergenceofhighersystematiccategories.ThegreatextinctionoftheJurassicandthegreatspeciesexplosionintheCambrianandtheCretaceousdemonstratetheexistenceofleapsinthehistoryoforganicevolution.Thesefactsindicatethatspeciationisnotgradual.Naturalselectiondoesnothaveacreativeeffectonspecies,butratherbarriersthattheorganismmustavoid.Intrinsicepigeneticandgeneticfactorsareresponsibleforinducingtheformationofnewspeciesinnewecologicalenvironments.Neitherhasatmosphericpressureledtothecreationofbirdsorbutterflies,andasMonodandJacobsaid,"Itisjustbychanceandnecessity."Newgenomicandepigenomiccombinationsrandomlyemerged,andifenvironmentsaresuitableforthesenewgenotypes,thespeciesareadaptedtotheenvironments.Metaphoricallyspeaking,atmosphericpressuredidnotcreatetheairplane;itisthemechanicwhoadjuststhevehicletomakeitfly.Moreover,theroleofvirusesintheevolutionandadaptationofprokaryotesandeukaryoteshasnotbeenevaluatedintheframeworkofthesynthetictheory.Thereisnobridgebetweenvirologyandevolutionarytheory.Thisisprobablybecauseviruseshavelongbeenconsideredtohaveoriginatedfromthegenomeofeukaryotes.TheywouldhavebeenfragmentsofRNAorDNAcellsthatescapedalongtimeagofromeukaryoticchromosomes,evolvingafterwardsbycapturingadditionalgenesfromthegenomesoftheirhosts.Nevertheless,thisviewhasnowbeenchallengedbythediscoveryofribozymesandbythesurprisinghomologybetweenviruseswithverydistantlyrelatedhosts,andbyphylogeneticanalysessuggestingthatgenesmighthaveflowedfromvirusestoeukaryoticchromosomes(Fileéetal.,2003).IfRNAviruseswerethefirstlivingmanifestation,thentheycouldbemolecularfossilsofthisprimitiveRNAworld(Chela-Flores,1994).Inthispool,RNAviruseswouldhaveevolvedfirst,followedbyretro-elementsandDNAviruses.Thevirusworldconceptandthesemodelsofmajortransitionsintheevolutionofcellsprovidecomplementarypiecesofanemergingcoherentpictureofthehistoryoflife(Kooninetal,2006).ThelargeamountofretrovirusesDNAinthehumangenomeandothereukaryotes,apparentlycontradictsthedebuggingroleofnaturalselection.However,theincreaseinrepeatedDNAwiththecomplexityofhigherorganismsshowsanadaptivevalue(LauandBartel,2003).Thus,theparadoxofC-valuewouldnotbeaparadox(Frías,2007a).Alargeamountofredundantgeneticmaterialineukaryoteshasaviralorigin,inparticularsmallRNA,RNAinterference,intronsandmobilegeneticelements.Allthesegeneticselementswerehorizontallyacquired,butonceincorporatedintothehostgenomeandpassingtheWeissmanbarrier,theywereverticallytransmittedaccordingaMendelianmodelofheredity.Thus,Steele'sassumptionisprobablycorrectandhismodelcouldbeexpandedtoexplaintheheredityofthelargeamountofDNAretrovirusineukaryotes.IthasbeenhavebeenfoundthatDNAvirus(polydnvirus)inparasiticwaspscouldbeembeddedinthegenomeofthehost.BothDNAvirusesandretroviruseshaveasymbioticrelationshipwiththehost.Findingsinthehumangenome,suchasgenesfrombacteria,virusesacquiredbyhorizontaltransmissionandhomologousregionsofhumangeneswithotherorganisms,suchasDrosophila(KatohandKatoh,2003),indicatethattheeukaryoticgenomeisunstableoveralongtime-scale.However,itmaybeamosaicflowofinformationfromdifferentsourcesinasymbioticco-evolutionaryprocess.Thestudyofthehumangenomeevolutionhasconcentratedonhumansandtheirhominidancestors,withoutmuchattentiontootherorganismsandvirusesthatalsoevolvedfromthesameenvironments(VanBlerkom,2003).Withrespecttogenesofendogenousvirusesembeddedinthehostgenome,thereisdoubtwhetherthesegenesshouldbeconsideredforeignorfromthehost,asoccurswithmitochondrialandchloroplastgenes.Itisnecessarytoestablishbridgesbetweenvirusesandeukaryoticgenomeorganizationtobetterunderstandingtheroleoflateralgenetictransferencesinmacro-evolutionaryprocesses.Inparticular,itisnecessarytocarryoutfunctionalgenomicsstudies.ThroughthecontributionsofLynnMargulis(1988),itiscurrentlyacceptedthatmitochondriaandchloroplastareendosymbiontsofbacterialorigin.ManybiologistsalsoaccepttheecologicalGaiahypothesisofLovelockandMargulis(1974),wherelivingorganismareintegratedwithotherphysicalcomponentsinourplanetinordertomaintainadynamicbalanceorhomeostasisinthesystemthatcounteractsthesecondlawofthermodynamics.Itislikelythatviruseshaveparticipatedformillionsofyearsas"workers",remodelingtheeukaryoticgenomeandproducingevolutionarynoveltiestogetherwithotherclassicalmechanisms,suchashomeoticandsystemicmutationsandchromosomicrearrangements,joinedtootherfactorslikeepigénesisandheterochronyduringdevelopment.Allthesenewmolecularaspectsuncoveredbythesynthetictheoryofevolutionsuggesttheneedtomakeanewevolutionarysynthesis.ACKNOWLEDGEMENTSThisisaposthumoustributetoDr.GustavoHoeckerSalasThanktoananonymousreviewerforhissuggestionsthathelpedmeimprovethemanuscript.ThisresearchhasbeensupportedbyProjectFIBAS06/08DIUMCE.REFERENCESAHUJAMR(1988)SomaticCellGeneticsofWoodyPlants.LuwerAcademicPublishers.USA.231pp.        [ Links ]BARDAROVS,BARDAROVJRMS,PAVELKAV,SAMBANDAMURTHYM,LARSENJ,TUFARIELLOJ,CHANGHATFULL,JACOBSWR(2002)Specializedtransduction:anefficientmethodforgeneratingmarkedandunmarkedtargetedgenedisruptionsinMycobacteriumtuberculosis,M.bovisBCGandMsmegmatis.Microbiology148:3007-3017.        [ Links ]BITSCHJ,BITSCHC,BOURGOINTH,HAENSECD(2004)Thephylogeneticpositionofearlyhexapodlineages:morphologicaldatacontradictmoleculardata.SystEntomol29:433-440.        [ Links ]BRNCICD(1957)HeterosisandtheintegrationofthegenotypeingeographicpopulationsofDrosophilapseudoobscura.Genetics39:77-88.        [ Links ]BROWNSW(1964)HeterochromaticchromosomesintheCoccids.Science145(3628):130-136.        [ Links ]BROWNSW(1966)Heterochromatin.Science28(151):417-425.        [ Links ]BUSCHMA,BOMBLIESK,WEIGELD(1999)ActivationofafloralhomeoticgeneinArabidopsis.Science285(5427):585-587.        [ Links ]BUSHGL(1969).Matingbehaviour,hostspecificity,andecologicalsignificanceofsiblingspeciesinfrugivorousfliesofthegenusRhagoletís(Díptera:Tephritidae).AmNat103(934):669-672).        [ Links ]BUSHGL(1982).Goldschmidt'sFolies.Paleobiology,8(4):463-469.        [ Links ]BUSHGL(1994).Sympatricspeciation:newwineinoldbottles.TrendsEcologyEvol9:285-288.        [ Links ]CARROLLSB(1995)HomeoticgenesandtheevolutionofArthropodsandChordates.Nature376:479-485.        [ Links ]CECHTR(1986)RNAasanenzyme.ScientificAmerican253:51-59.        [ Links ]CHELA-FLORESJ(1994)AreviroidsmolecularfossilsoftheRNAworld?.JThBiol166:163-166.        [ Links ]COYNEJA,ORRHA(2004)Species:RealityandConcepts:9-54.InCoyneJA,ORRHAed,Speciation,SinauerAssociates,Inc.Publisher,SunderlandMassachusetsUSA:545pp.        [ Links ]CHRISTENSONLD,FOOTERH(I960)Biologyoffruitflies.AnnRevEntomol5:171-192.        [ Links ]DANGWK,STEFFENK,PERRYR,DORSEYJA,JOHNSONFB,SHILATIFARDA,KAEBERLEINM,KENNEDYBK,BERGERSL(2009)HistoneH4lysine16acetylationregulatecellularlifespan.Nature459(7248):802-807.        [ Links ]DARLINGTONCD(1937)TheearlyhibridisersandtheoriginsofGenetics.Herbetia:63-69.        [ Links ]DARWINCH(1983)ElOrigendelasEspecies.Sarpe,Madrid.638pag.        [ Links ]DILLONN,FESTENSTEINR(2002)Unravellingh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