Microevolutionary, macroevolutionary, ecological and taxonomical implications of punctuational theories of adaptive evolution.

0.47 MB·English

by  Flegr, Jaroslav

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REVIEW Open Access
Microevolutionary, macroevolutionary, ecological
and taxonomical implications of punctuational
theories of adaptive evolution
Jaroslav Flegr
Abstract: Punctuationaltheoriesof evolution suggestthat adaptive evolution proceeds mostly, or even entirely,in
thedistinct periods ofexistence of a particular species. The mechanisms ofthis punctuated nature of evolution
suggested by thevarious theories differ. Thereforethe predictions of particular theories concerning various
evolutionary phenomena also differ.
Punctuational theories can be subdivided intofive classes, which differ intheir mechanism and their evolutionary
and ecological implications. For example,the transilience model of Templeton (class III),genetic revolution model
ofMayr(class IV) or the frozen plasticity theory of Flegr (class V),suggests thatadaptive evolution insexual species
is operative shortly after the emergence ofa speciesby peripatric speciation –whileit is evolutionary plastic. To a
major degree, i.e. throughout 98-99% oftheir existence, sexual speciesare evolutionarily frozen (class III) or elastic
(class IV and V) ona microevolutionary time scale and evolutionarily frozen on a macroevolutionarytime scale and
can onlywait for extinction, or thehighlyimprobable return ofa population segment to theplastic state due to
peripatric speciation.
The punctuationaltheorieshave many evolutionary and ecological implications. Most of these predictions could be
testedempirically, and should be analyzedin greater depth theoretically.The punctuational theories offermany
new predictions that need to be tested, but alsoprovideexplanations for a much broaderspectrum of known
biological phenomena thanclassical gradualistic evolutionary theories.
Reviewers: This article was reviewed byClaus Wilke, Pierre Pantarotti and David Penny (nominatedby Anthony
Poole).
Keywords: Speciation, Frozen plasticity, Frozen evolution, Peripatric speciation, Invasive species, Domestication,
Asexual species, Genetic draft,Genetic hitchhiking, Advantage of sex,Evolutionary trends, Dead clade walking,
Cambrian explosion,Origin ofgenera, Taxonomy
Open peer review during speciation. The mechanisms of this type of evo-
Reviewed by Claus Wilke, Pierre Pantarotti and David lutionary behavior of sexual species suggested by the
Penny (nominated by Anthony Poole). For the full various theories differ, for areview see[1]. Forexample,
reviews,pleasegotothe Reviewers'commentssection. the genetic revolution model [2] implicitly and the fro-
zen plasticity theory explicitly [3] suggest that a species
is evolutionary plastic when its members are genetically
Background
uniform, i.e. only after a portion of the original species
Most punctuational theories of evolution, including the
has split off, skirted extinction for several generations,
evolutionary conceptions of Wright, Mayr, Carson,
and then undergone rapid multiplication (Figure 1).
Templeton and Flegr (for comparison seeTable 1), sug-
Following a short period of time, estimated by
gest that sexually reproducing species respond evolu-
paleontological data to correspond to 1-2% of the ex-
tionarily to selection (are evolutionarily plastic) only
istence of the species, polymorphism accumulates in
the gene pool; and thus, in each generation, new muta-
Correspondence:[email protected]
JaroslavFlegr,FacultyofScience,CharlesUniversityinPrague,Viničná7, tionsoccurinthepresenceofdifferentalleles.Thetheory
CZ-12844,Praha2,CzechRepublic
©2013Flegr;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsoftheCreative
CommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,and
reproductioninanymedium,providedtheoriginalworkisproperlycited.
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Table1Differencesbetweenvariouspunctuationaltheoriesandmodels
Theoryanditsauthor Theaim Suggestedmechanism
Shiftingbalancetheory toexplaintheabilityofspecieswithlargesubdivided 1.fragmentationofpopulationtosmallsubpopulations
WrightS.19321 populationscrossvalleysinadaptivelandscape whereanefficiencyofselectionislow2.spreadingand
fixationofanewallele(thatisdetrimentalwhenrare)ina
subpopulationbydrift3.“Infection”ofothersubpopulations
withindividualswithnewgenotypeoriginatedfroma
successfulpopulationandtheoriginationofnew
populationsbytheseindividuals
Geneticrevolution toexplaintheroleoffoundereventsinspeciation 1.changeofbalancedfrequencyofallelesinasplit-off
MayrE.19542 subpopulationduetosamplingeffect2.selectionforalleles
withbesteffectonfitnessinsteadofbest-cooperatoralleles
Founder-flushmodel toexplaintheroleoffoundereventsinspeciation 1.samplingeffectduetorapidone-stepreductionofa
CarsonH.L.19683 populationsize,2.expansionofthepopulationinanopen
uninhibitedecologicalniche,whichrelaxesallformsof
selectionallowingforsurvivingrecombinantsandmutants
withsuboptimalphenotypes(crossingvalleysintheadaptive
landscape)3.reaching(orovershooting)thecarrying
capacityofalocalityandtherestorationofselection
Genetictransilience toexplaintheroleoffoundereventsinspeciation 1.samplingeffectduetorapidone-stepreductionofa
model populationortohybridization,2.anincreaseoftheamount
TempletonA.R.19804 ofselectablegeneticvariabilityduetotransformationof
nonadditive(andthereforenonselectable)geneticvariability
toadditivegeneticvariabilityandbyhighersurvival
probabilityforcarriersofnewmutationsintheexpanding
population,whichincreasesresponsivenessofthe
populationtoselection3.restorationofthepopulationsize
limitationandselection
Punctuatedequilibrium toexplainthediscontinuousnatureofevolutionand variousmechanismssuggestedbyEldredgeandGold,
EldredgeN.19715 coincidenceofanageneticandcladogeneticevents includingperipatricspeciationandstrongselectionin
unusualconditionsontheperipheryofthespecies’range,
peripatricspeciationaccompaniedbygeneticrevolution,
sorting(accordingtoFutuyma7,withoutspeciation,any
evolutionarynoveltyisreversibleduetogeneflow),etc.
Frozenplasticitytheory toexplainwhyoldspeciesaremicroevolutionarilyelastic 1.mostpolymorphismexistinginanoldspeciesissustained
FlegrJ.19986 andmacroevolutionarilyfrozen,howfrozenspeciescanturn init’sgenepoolbyfrequencydependentselectioncreating
plastic,andthecontinuouslydecreasingrateof interconnectednetworkresistanttochangesofallele
macroevolution frequencies,2.mostnew(potentiallyuseful)allelesare
capturedinthiselasticnetworkofallelesduetopleiotropy
anditseffecton(stabilized)frequenciesofoldalleles,3.in
smallsplit-offpopulationsbalancingontheedgeof
extinctionforseveralgenerations,adecreaseinstrengthof
selection,includingfrequencydependentselection,will
occur,andmostgeneticpolymorphismwilldisappeardueto
drift4.afterexpansionofpopulationsize,nowlarge
geneticallyuniformpopulationturnsevolutionaryplastic–
newadvantageousmutationscanspreadinthenetwork-free
populationbyselection5.traitsresistanttothawing
accumulateinthegenepoolbysortingonthebasisof
stability6.accumulationofpermanentlyfrozentraitsbythe
mechanismofsortingonthebasisofstabilityinparticular
cladesduringmacroevolution
TheGeneticRevolutionmodelimplicitlyandtheFrozenPlasticitymodelexplicitlysuggestthatfrequency-dependentselectionplaysanimportantrolein
stabilizationofthegenepoolofaspecies.Therefore,accordingtothesetwotheories,macroevolutionaryfrozenspeciesaremicroevolutionarilyelastic.According
totheShiftingBalancetheory,theFounderFlushandtheGeneticTransiliencemodels,theyaremicroevolutionaryfrozen,i.e.theyhavesignificantlyreduced
plasticityincomparisonwiththeirplasticstate.AccordingtoFutuyma’ssortingmodel,macroevolutionarilyfrozenspeciescanbemicroevolutionarilyplastic.1
(Wright1932),2(Mayr1954),3(Carson1968),4(Templeton1980),5(Eldredge1971),6(Flegr1998),7in(Gould2002),p.77.Infact,thePunctuatedequilibrium
theoryinitscurrentformwaspublishedin1972byEldredgeandGould(EldredgeandGould1972)andtheFrozenplasticitytheoryin2008(Flegr2008)and2010
(Flegr2010)byFlegr.
of evolutionarily stable strategies indicates that, under greater this deflection, the more the gene pool resists the
these conditions, selection cannot lead to long-term selection; after it ceases, the allele frequencies spontan-
changesinthephenotypesoforganisms(ananalogyofthe eously return to their original values. Therefore, the spe-
fixationofthe“best”strategyinapopulation),butonlyto ciesceasestobeevolutionarilyplasticandbecomeselastic
a deflection of the frequency of the individual alleles onamicroevolutionarytimescaleandfrozenonamacro-
(strategies) from evolutionarily stable equilibrium. The evolutionary time scale. It then exists in this state until
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Figure1Adaptiveevolutioninsexualspeciesaccordingtofrozenplasticitytheory.Itmustbeemphasizedthatextinctionisafarmore
probablefateforasmallpopulationthanexpansion.However,unsuccessfulspeciationeventsarenotinterestingfromtheperspectiveof
evolution.
(unfavorable) environmental changes accumulate so that 21 hours, are known to better synchronize their circa-
themacroevolutionarilyfrozenspeciesbecomesextinct. dian rhythms with shorter light–dark cycles than the
Here I show that punctuational models of evolution current 24-hour cycle [4].
have considerable evolutionary and ecological implica-
tions (see Table 2) that could be tested empirically, and LowerViabilityandFertilityofSelectedOrganisms
shouldbeanalyzedtheoreticallyingreater depth. Representativesofold,eithermicroevolutionaryfrozenand
therefore “obsolete” species (class II and III theories) or
Results and discussion elastic species, kept out of their original state by selection
Microevolutionaryelasticityandadaptationtopast (class IVand V theories), have lowered viability or fertility
condition in comparison with representatives of young species living
According to the classical gradualistic theories, all spe- under conditions similar to those existing at the time of
cies respond to selection as if they were plasticine while, their origination [3]. Therefore, the population density is
according to punctuational theories, most species are re- probably negatively correlated with species age; a study of
sistant to selection as if they were lead (class II and class the correlation of the molecular age of a species with its
III theories) or respond to selection as though they were averageabundancecouldeasilytestthisprediction.
rubber – at first, they respond readily to selection pres- The correlation could also explain the existence of the
sure; however, as the average phenotype of the organism most universal ecological law – that every community
deviates from its original state, selection is less and less shows a hollow curve on a histogram with many rare,
effective and, at a certain point, the response ceases andonlyafewcommonspecies[5].Thisisaquitestable
(class IV or class V theories) (Table 2). According to situation; species retain their basic status as common or
class IV and class V punctuational theories, the average rare for millions of years [6]. Class II-V punctuational
phenotype returns to the original state when the selec- theories of evolution predict that common species are
tion stops[3]. young species, still evolutionarily plastic or having re-
There are several critical implications: in the world of cently lost their plasticity, that still live under conditions
species that do not respond to selection, organisms are similar to those existing at the time of their origination.
not optimally adapted to the conditions of their current Thisagrees withtheobservedcorrelationbetweenglobal
environment but to those present during the evolution- and local abundance in young species, but not in old.
ary plasticity of the particular species. This should be Old species are probably less competitive in a similarly
true especially for evolutionarily old species, as their en- broad spectrum of biotopes as young species [7]. Class
vironmental conditions probably differ most from those II-V punctuational theories of evolution also predict that
existing during their origination. For example, algae (the the paleontological record will more often show a grad-
typical representatives of ultrabradytelic species), which ual change from common to rare species rather than the
originated in the Paleozoic when days lasted about opposite changefrom raretocommon species.
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Table2Differencesbetweenpredictionsofthegradualisticandpunctuationaltheoriesofevolution
Gradualistic GroupI GroupII GroupIII GroupIV GroupV
theories punctuational punctuational punctuational punctuational punctuational
theories theories theories theories theories
typicalrepresentative Fisher’s Futuyma’s Wright’smodel Templeton’s Mayr’smodel Flegr’smodel
model model model
anagenesisandcladogenesisarecoupled no yes yes yes yes yes
**1,2
divergenceofspeciescorrelateswith no yes yes yes yes yes
taxonrichness1
geneticpolymorphismdecelerates no no no no yes yes
evolution**3
mostspeciesunderusualconditions asplasiticine asplasiticine ratheraslead ratheraslead asrubber asruber
respondtoselection*4 thanplasticine thanplasticine
twospeciesinthesamenichefrequently no no yes yes yes yes
caneasilycoexist*
speciesareadaptedtooriginal no no yes yes yes yes
environment*5
localandglobalabundancedonot no no yes yes yes yes
correlateforoldspecies**6
abundanceofspeciesdecreaseswith no no yes yes yes yes
speciesage
abilityofspeciestorespondto no no no no yes yes
environmentalchangesdecreaseswith
speciesage**7
abilityofspeciestochangetaxon- no no no no no yes
characteristictraitsdecreaseswithclade
age*
speciesonislandsarederivedmorethan no yes yes yes yes yes
thoseoncontinents*1
asexualspeciesaremoreadaptedtotheir no no no yes yes yes
environment*8
cross-pollinatingspeciesmorestablethan no yes no yes yes yes
self-pollinatingspecies*9
invasivespeciesexpresshighercapacity no no no yes yes yes
torespondselection**10
domesticatedspeciesexpresshigher no no no yes yes yes
capacitytorespondselection
domesticatedspeciesareevolutionarily no no no no yes yes
younger
successfulselectiondecreasesfitness*11 no no no no yes yes
evolutionofaltruisticbehaviorbygroup no no no yes yes yes
selectioniseasy*12
phylogenetictreesusuallyresemble*13 tree shrub shrub shrub shrub shrub
intraspeciesvariabilityinacladeusually no no no no no yes
decreasesintime*
interspeciesvariability(disparity)ina no no no no no yes
cladeusuallydecreases*
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Table2Differencesbetweenpredictionsofthegradualisticandpunctuationaltheoriesofevolution(Continued)
deadcladewalkingshouldfrequently no no no no no yes
occur*
slowlong-termtrendsarequitepossible* no yes yes yes yes yes
generaandhighertaxaareobjective no yes yes yes yes yes
existingentities*
Gradualistictheoriesincludenotonlyclassicalneodarwinistic(Fisherian)modelsbutalsoselfishgenemodelofDawkins(Dawkins1976).TheFutuyma’smodel
(stabilizationofgradualisticallydevelopedtraitsbyaspeciation)wasdescribedin(Gould2002),p.77,othermodelsaredescribedinTab.1.ThegroupIIencloses
theWright’sShiftingbalancemodel(Wright1932)andthegroupIIIenclosesthemodelsofCarsonandTempleton(Carson1968;Templeton1980)astheelasticity
ofspeciesorthefrequencydependentselectionisprobablynotexplicitlymentionedinthesemodels.TheFlegr’sfrozenplasticitymodel(classV)differsfromthe
Mayer’sGeneticrevolution-basedmodel(classIV)byincludingtheoryofevolutionarystablestrategiesfordescriptionofbehaviorofallelesingenetically
polymorphicpopulationandbyincludingtheconceptionofaccumulationofpermanentlyfrozentraitsbysortingforstability.Twoasterisksdenotethe
predictionsthathavealreadybeentestedwithpositiveresult.Oneasteriskdenotesthepredictionsthathavenotbeenintentionallytestedbutaresupportedby
publisheddata.1(Ricklefs2004),2(Pageletal.2006),3(Bryantetal.1986;Mezhzherin1997),4(DobzhanskyandSpassky1969),5(Costasetal.1996),6(Prinzingetal.
2004),7(Mikulas2008),8(HaagandEbert2004;Pecketal.1998),9(Flegr2002),10(Novak2007;Prentisetal.2008;Yonekuraetal.2007),11(BradshawandHolzapfel
2006;Nusseyetal.2005),12(KulichandFlegr2010),13(Gould2002;Heard1992).
LimitedGeographicalRangeofSpecies wild phenotype as a consequence of the action of natural
On the basis of class IVand classV theories, it can also selection which, during a few subsequent generations,
be expected that populations near the center of the spe- removes from the population the individuals with reduced
cies’ range express higher mean viability or fertility than viabilityandfertility,i.e.withthephenotypeofthehuman-
those on its periphery, which have had to adapt to con- bredrace.
ditions differentfrom those atthe time ofitsorigination.
E.g. tits are able to adapt to a different climate, with its CoexistenceofSpeciesthatUsetheSameResource
corresponding shift in peak abundance of caterpillars, by The absence of evolutionary plasticity predicted by class
a shift of their own breeding season. However, the fertil- II, III, IV and V punctuational theories could also ex-
ityoftheseadaptedpopulations decreasesincomparison plain long-term coexistence of species that use the same
with birdsadaptedtotheoriginal climate[8,9]. resource. Theoretical analysis shows this coexistence is
Negative correlation between deviation from the equi- possible, but highly unstable in evolutionarily plastic
libriumfrequency of alleles(andfrom theoriginalpheno- species [10]. Sooner or later, one of them increases in
type of the species) and the fitness predicted by any class exploitation intensity or efficiency, thereby causing the
IV and class V punctuational theory of evolution could extinction of the competing species. The absence of evo-
provide an alternative explanation for the existence of lutionary plasticity in sexual species could be an impor-
distinct geographic ranges of species. Elastic species can tant positive factor in the conservation of global and
adapttogeographicallychangingconditionsonlytoacer- localbiodiversity.
taindegree.Atsomepoint,thedecreaseinfitnessaccom-
panying the departure of the phenotype from the original EfficiencyofGroupSelectioninNon-plasticSpecies
stateissogreat thatitis incompatible withthe long-term The low and vanishing inheritance of phenotypic traits
survivalofthepopulation. in polymorphic sexual species predicted by class III, IV
and V punctuational theories could also explain the per-
LowerViabilityandFertilityofDecorativeBreeds sistence of altruistic behavior and general efficiency of
The same negative correlation between departure of a group selection. The most serious objection of evolu-
phenotype from the original state and the mean fitness tionary biologists against the role of group selection in
could explain the lower viability and fertility of most evolutionary processes consists in the fact that a trait
decorative breeds of practically any domesticated species. that provides an advantage to a group and simultan-
When the populations of pure-bred animals are left to eously places the individual that is its carrier at a disad-
theirfate,membersofthepopulationreturntothepheno- vantage has a low chance of spreading and enduring in
type of their wild predecessors within a few generations. nature. Groups in which the altruistic trait spreads
Thisphenomenondiffersfromthereturnofthephenotype would prosper better than groups in which this trait is
toanoriginalwildforminthecaseofcrossesbetweentwo lacking and the average fitness of the members of this
different races. In crosses, the almost immediate return to group would be greater; however, selfish individuals who
the original phenotype is caused by a breakdown of the do not exhibit this trait and do not behave altruistically,
unique combination of alleles (responsible for the appea- but only enjoy the advantages provided by the presence
rance of the members of the individual races) as a conse- of altruists, would have the greatest fitness within these
quence of recombination and segregation of alleles. In groups. In sexual (elastic) species, any behavioral trait
membersofthesamerace,thereisagradualreturntothe (for example, altruistic behavior) is usually determined
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by the greater number of genes and many of these genes Data on the evolutionary plasticity (evolvability) of inva-
have (due to epistasis) a context-dependent influence on sive species are rather scarce [17-19]; however, e.g., the
the particular trait. Consequently the heritability of most invasive grass Phalaris arundinacea demonstrates greater
traits is low. Under these conditions, altruists emerge heritability and higher evolutionary plasticity (greater
from the population as if by chance in families that are responseofthephenotypetothelocalconditions)inNorth
completely unrelated and have different phenotypes, i.e. America than in its original area in Europe [20]. In accor-
individuals with quite different behavior, with a probabi- dance with the predictions of punctuational theories,
lity that is determined only by the proportion of particu- parthenogenetic species (which always have much greater
lar alleles in the entire population. Thus populations can heritabilityoffitnessthansexualspecies)[21]andpolyploid
compete for the greatest average fitness of their mem- species (which have often slipped through a genetic
bers; those that have the greatest proportion of the rele- bottleneck as species of peripatric origin) [19] are
vant alleles, resulting in the greatest number of altruists over-represented among invasive species.
being formed (emerging by chance), will win in this
competition. The models show that group and inter- LowEfficiencyofDomesticationofPlantandAnimal
speciesselectioncanoccurinnatureinfavorofaltruistic Species
traits (because the percentage proportion of alleles in The existence of only a low proportion of evolutionarily
the population is inherited from one generation to the plastic species can also explain the fact that humans
next) and its results cannot be cancelled out by individ- have succeeded in domesticating only a negligible num-
ual selection because the trait itself, altruistic behavior, is ber of plant and animal species [22]. Only plastic species
not inherited [11]. can adapt to the drastically changed conditions of life in
captivity without a substantial reduction in viability and
ExistenceandSuccessofInvasiveSpecies fertility. Class III, IV and V punctuational theories of
The existence of two species types, very common non- evolution explicitly or implicitly suggest that domestica-
plastic (microevolutionary frozen, according to class II tion should be successful mostly in young, unfrozen
and III theories or elastic, according to class IV and V species. It is worth recalling that most selection experi-
theories) and very rare plastic, offers a new explanation ments were performed either on domestic animals,
for the existence of invasive species. The transfer of a probably with lower genetic variance from the very
species to a new territory is a necessary, but not suffi- beginning, [22] or on small populations that had passed
cient, condition for invasion. In the vast majority of through a narrow bottleneck just before, or at the begin-
cases, the species succumbs to competition with local ning of, the experiment. Therefore, the ability of a spe-
species and dies out. Only a small fraction of introduc- cies to respond to selection is probably overestimated
tions “succeed”. For example, red deer were introduced and the natural elasticity is underestimated by the
into New Zealand a total of 32 times and only the last results of these experiments or of long-term selection
attempt was successful; however, these deer now occupy programsperformedondomesticates [23].
the entire area of the southern island [12]. Similarly, the Class III, IV and V punctuational theories predict that
now excessively successful starling settled in America most varieties of domesticated plants would have been
only after at least nine attempts [13]. Invasive success is derived from species with a capacity for vegetative
usually preceded by a relatively long lag phase, in which reproduction, e.g. by means of tubers, rhizomes or grafts,
thefutureinvasive speciespeacefullycoexistswithnative or from self-pollinating species [22]. The plasticity of
species inthe limitedareaoftheiroriginal introduction. asexual species is higher than that of sexual species, and
According to classical gradualistic evolutionary theor- that plasticity is greater in self-pollinating species than in
ies, native species,whichare adapted to local conditions, cross-pollinating species [24]. Therefore, these species can
should outcompete newly introduced species [14,15]. bemorereadilychangedbyartificialselection.Ontheother
According to the discussed class II-V punctuational the- hand, sexually reproducing and cross-pollinating varieties
ories, the ecological success of some newcomers is not shouldbemorestableandlosepropertiesacquiredbyarti-
very surprising. During the introduction and lag phase, ficialselectionmoreslowly.Duetonaturalselection,aplas-
the genetic polymorphism of an introduced population tic variety has a tendency to increase its fertility at the
decreases, which could result in the conversion of a expenseofpropertiesusefulforman.Incontrast,asexually
non-plastic species to the plastic state [16]. Non-plastic reproducing (elastic) variety can only respond to selection
species are best adapted to the conditions existing at the to a certain degree, and therefore cannot lose its useful
time of their origin (past conditions), while plastic properties due to natural selection. It was reported in the
species can adapt to current conditions.Moreover, plastic older literature that the varieties of cross-pollinating rye
species can outcompete non-plastic species in the usually remained in seed company catalogues much
coevolutionary arms-race. longerthandidthoseofself-pollinatingwheat[24].
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SuccessofAsexualSpeciesinHabitatswithExtreme whilepunctuationalmodelsofanyclassassumethatmajor
Conditions irreversible phenotypic changes are always associated with
The plasticity of asexual species should be greater in speciation.Theoppositedoesnothold,asmostspeciation
habitats that are poor in resources or where survival is events, such as vicariant allopatric speciation, parapatric
limited by unfavorable abiotic factors. Here, the main speciationandmanyformsofsympatricspeciation,arenot
criterion of evolutionary success is how well (not how coupled with a dramatic reduction in genetic polymorph-
quickly) the species can change its phenotype in re- ism and return to plasticity. These forms of speciation
sponse to environmental requirements. It is noteworthy could be responsible for the origin of most species, while
that asexual species or asexual lineages of otherwise sex- new generaor higher taxa (i.e. monophyletic lineages with
ual species are found primarily in habitats with extreme characteristic prominent evolutionary novelties) mostly
conditions – in habitats that are extremely dry, cold or result from peripatric speciation. Therefore, punctuational
poisonous. The proportion of asexual species increases, theoriesofevolutionpredictthatthenumberofevolution-
for example, with increasing altitude and latitude, or arychangesinphenotypeinaphylogeneticlineagereflects
wherethesoilcontainshighconcentrationsofpoisonous thenumberofspeciationsinthislineratherthanitsage.A
heavy metals [25,26]. On the other hand, elastic sexual study of passerine birds has found the number of speci-
species should be better off in an environment rich in ationwithinaphylogeneticlinetohaveaverystrongeffect
resources and with many competing species where the on the rate of anagenesis. The number of species alone
rate of evolutionary responses in the coevolutionary explained 33.3% of the total variation in morphology [28].
arm-race plays the crucial role. The fact that they retain Moreover,thereportedrateofanagenesisonislandsseems
most of their genetic polymorphism enables them to to be higher than on the mainland [28]. The higher fre-
rapidlyrespond to any selection pressures byshifting the quencyofperipatricspeciationonislandscanbeacluefor
frequencies of their alleles without needing to wait for explanationoftheobservedphenomenon.
rareadvantageous mutations. Anothercorollaryoftheanagenesis-cladogenesisassoci-
ationpredictedbythepunctualisticmodelsofevolutionis
Evolutionarypassivityofelasticspeciesandthe thattheextantrepresentativesofancientphylogenetictree
advantageofsex branchesthathavesustainedalowernumberofspeciation
Elasticity of sexual species predicted by class IV and V events should bear more plesiomorphic characters than
theories or evolutionary passivity of sexual species pre- representativesofapicalbranchesofthephylogenetictree.
dictedbyclassIIItheoriescouldalsobeadvantageousina According to classical gradualistic theories of evolution,
long-termperspective.Underthefluctuatingconditionsof no such correlation between species age and its antiquity
a stochastic environment, plastic asexual species could shouldbeexpected.
adapttotransientenvironmentalchangewhilenon-plastic
species resist such a change of their phenotypes. When CorrelationbetweentheRateofMolecularEvolutionand
the environmental conditions return to normal, a plastic theSpeciationRate
species could fail to return to its optimal phenotype Thecorrelationbetweentheratesofanagenesisandspeci-
rapidly enough to avoid the risk of extinction, while the ation can be detected even on a molecular level. A mo-
population of an elastic species (class IVand V theories) lecularstudy [29] hasshown thata relatively large part of
returns to its original phenotype within a few generations the variability in the substitution rate can be explained by
and a population of microevolutionary frozen species differences in the speciation rate between evolutionary
(class III theories) stays near the original optimum all the lineages. Of course, a large part of the monitored nucleo-
time.AssuggestedbyG.C.Williams[27],themainadvan- tidesubstitutionsareneutralmutationsknowntobefixed
tage provided by sexual reproduction could consist in a by means of genetic drift and genetic draft and not by
substantialreductionintheevolutionarycapabilityofsex- selection. Drift probably operates at the same rate in fro-
ual species. As a consequence of their elasticity and/or zen, elastic and plastic species, however, the genetic draft
frozenness, sexual species are evolutionarily passive operatesmoreeffectivelyduringplasticphaseofevolution
throughout much of their existence and cannot oppor- when many neutral and nearly neutral mutations are
tunistically respond to temporary short-term changes in beingfixedwithpositivemutationsbygenetichitchhiking.
the external conditions. Approximately 35% of the substitutions (20-70%, depend-
ingonthestudiedtaxon)wasshowntooccurinbriefpe-
CoincidenceofChangesofthePhenotypeofOrganisms riodsofspeciation.Itisworthmentioningthatwearenot
withSpeciation awareofhowmanyspeciationeventsactuallyoccurinthe
According to gradualistic models, there should be no cor- studied, seemingly unbranched lineages. Therefore, the
relation between cladogenesis and anagenesis (between published estimates of speciation-associated substitution
speciation and changes in the phenotype of organisms) ratesrepresentonlythelowermarginoftherealfigures.
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Molecularstudiesalsoconfirmincreasedratesofevolu- similar in shape to the figure drawn by Darwin [37] and
tioninislandspecies.Thesespecieshavenotonlyahigher unlike modern trees (which are usually automatically
substitutionratebutalsoahigherfrequencyofnonsynon- interpreted as phylogenetic trees but are in fact inspired
ymoussubstitutionamongtheobservedmutations,which by the shape of the cladogram, a graphic representation
suggests that positive selection rather than drift plays a ofthedistributionofsynapomorphies within ataxon).
moreimportantroleonislands(whereahigherfrequency
of peripatric speciation is expected) [30]. Of course, an- HigherVariabilityofEarly-BranchedSpeciesand
other explanation for observed higher nonsynonymous DecreasingSpeciationRateofClades
substitutionrateinislandspecies,namelythehigherprob- Thedecreasedvariabilityofspecieswithageofthephylo-
ability of fixation of slightly negative mutations during genetic line and the maximum biodiversity achieved early
peripatricspeciation,alsoexists. after the origin of the phylogenetic line [38,39] are other
phenomena that are not supported in gradualistic evolu-
PunctuationalEvolutionandtheOriginofEvolutionary tionary theories but are explicable within classV punctu-
Trends ational theories.Webster[40] reportedthat the frequency
TheclassII-Vpunctuationalmodelsofevolutionalsooffer and extent of morphological variations in 982 trilobite
a new explanation for the existence of evolutionary trends, speciesaregreatestearlyintheevolutionofthegroup.He
the slow directional phenotypic changes in organisms of has shown that “the proportion of species with at least
particular phylogenetic lineages that endure much longer one polymorphism drops sharply between the Middle
than the individual species involved. The trends are too Cambrian (75%) and Late Cambrian (8%), then rises to
slowtobegearedbyselection–thechangeinthevalueof 40% in the Early Ordovician (coincident with the first
the trait per generation is so small that it is completely samplingofthediversephacopidandproetidorders),after
invisibleforselection[31],p.835.Accordingtogradualistic which there is a progressive decline through the Middle
evolutionarytheories,theselectionpressurehastobesuffi- Devonian (1%), interrupted only by a particularly low
cientlystrongtoovercomegeneticdrift.However,thistype value (0%) in the Late Silurian. No polymorphism was
of selection should result in far more rapid changes than recorded in character-state coding among the 23 post-
those that emerge as trends in the paleontological record. Devonianspecies[41]”.
Punctuational theories suggest a new solution to the para- Change in the diversity of a clade (but not necessarily
doxofveryslowevolutionarytrends.Accordingtopunctu- the abundance of a species) is usually asymmetrical in
ational theories, the trend could, in fact, be a product of a time; a clade quickly achieves maximum diversity and
relatively strong and long-term selective pressure to which slowlygoesextinct[39,42].Inaddition,thespeciationrate
species can respond, however, only in the brief and rare usually declines with increasing age of a clade [43,44].
periodsoftheirevolutionaryplasticity. Bothphenomenacouldhaveacommoncause,continuous
irreversible freezing of more and more traits during the
Shrub-ShapedratherthanTree-ShapedPhylogenetic evolution ofa clade[3]. Traits differinresistancetotran-
Trees sition from frozen to plastic in response to reduction of
Long-term, the number of species on Earth is relatively genetic polymorphism. For some traits, this is likely to
stable or even increases [32-35]. Thus, if some species happen readily, coupled with a relatively small reduction
become extinct without speciation, then other species in genetic polymorphism. For others, transition from fro-
must necessarily undergo speciation a great many times. zen to plastic is difficult or even impossible, as it requires
It is therefore highly probable that a species in a transi- anunrealisticallylongperiodofpersistenceofanunrealis-
ently plastic state splits off not one but several different tically small population. On a macroevolutionary time-
species. Ithas alreadybeen pointed out that the shape of scale, more and more traits that are characteristic for the
phylogenetic trees differs significantly from that pre- clade (or rather the corresponding taxon) pass into the
dicted by the neutral model of random speciation and permanently frozen state due to a universal process of
extinction [31,36]. Phylogenetic trees are usually shrub- sorting for stability. Stable traits (systems etc.) persist
shaped rather than tree-shaped. Most disparate species while unstable traits (systems, etc.) pass away. A stable
originate simultaneously from a common ancestor as a trait is a trait coded by many genes that are interchange-
result of adaptive radiation. Particular species that have able in their effect.Themutation of anallele in onelocus
originated in a common radiation event and from a sin- doesnotresultinachangeinsuchatrait,whilemutation
gleevolutionarilyplasticancestorcoexistforalong time, inallthelociishighlyimprobableespeciallyif,duetoplei-
without splitting off new species. Most branches end otropy, the genes in particular loci also influence other
without producing a successor; however, some of them traits. Another source of the evolutionary stability of a
could split off a new plastic species that could undergo trait is frequency-dependent selection, particularly the
a new burst of radiation. Interestingly, such a tree is steep dependence of fitness on the frequency of an allele.
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When the fitness of an individual decreases sharply with environment and would probably become extinct in the
the increased frequency of an allele (of a particular trait), nextchronostratigraphicstage.
even a drastic reduction inpopulation size cannot lead to
total loss of the polymorphism in a particular locus. Due CambrianExplosion
to dominance, and especially to epistatic interactions of Another phenomenon that cannot be explained within
more than two genes, the slope of fitness can be very the traditional gradualistic evolutionary theories is the
steep. In the dominance case, the fitness of homozygotes Cambrian explosion [46,47]. All the basic animal archi-
with genotype aa could decrease at a rate proportional to tectures were apparently established by the close of the
the second power of the trait frequency. In the case of Cambrian explosion; subsequent evolutionary changes,
epistatic interactions between more than two genes, the even those that allowed animals to move out of the sea
rate could be proportionally higher. This kind of trait onto the land, involved only modifications of those basic
probably survives peripatric speciation in a polymorphic body plans. Mostprobably,not only thegeneraldiversity
state, or polymorphism in such a trait is restored very of metazoan body plans, but also the diversity within
quicklyinthenewlyemergingspeciesduetomutations. particular phyla reached its maximum within 10–20 mil-
In a new taxon, i.e., a clade that was named by taxono- lion years during the Cambrian , and remained stable or
mists because of the presence of certain combination of even decreased throughout the following 500 million
(‘important’) traits, a relatively high proportion of species years [46,48]. The number of species increased irregu-
contain many apomorphic traits that could become un- larly and discontinuously during the Phanerozoic; how-
frozen during standard peripatric speciation or that are ever, the number of body plans, i.e. disparity, probably
relativelyplasticevenatthelevelofaspecies(orevenofa decreased.
local population). In time, more and more traits in more Considerable efforts have been exerted to suggest that
andmorespeciesturntoasemi-permanentlyorevenper- the Cambrian explosion, a phenomenon that had no
manently frozen state. The representatives of a particular support in contemporaneous gradualistic evolutionary
taxon are not only less and less variable (more and more theories [49,50], is not in any way mysterious or that it
elastic – resistant to selection pressure) but also exhibit never even occurred [51-54]. Molecular clock data based
elasticity that is less and less affected by future peripatric on concatenated amino acid sequences of 129 proteins
speciations. Originally, many representatives of a taxon from 36 eukaryotes suggest that representatives of meta-
had the capacitytoevolvenew body plans after peripatric zoan phyla probably diverged 100–210 million years be-
speciation. In the end, only some species retained this fore the Cambrium [55]. (Previous molecular studies
capacity and, even in these species, some traits had a suggested an even earlier divergence time; however, the
highly limited capacity to respond to selection after peri- results of current multigene studies are more reliable.)
patricspeciation. Nevertheless, this molecular data is useful for tracking
events of cladogenesis, but not events of anagenesis [56].
DeadCladeWalking The metazoan phyla could diverge long before the
This last mechanism can explain another well-known Cambrian; most probably, however, their representatives
phenomenon, namely: dead clade walking. It is widely had very uniform body plans until the beginning of the
knownthatunexpectedlymanydiversifiedanddiversifying Cambrian when some extrinsic (ecological) or intrinsic
clades that survive a period of mass extinction turn mar- (genetic) event probably triggered the morphological
ginalordeclineintheaftermathstage.Jablonski[45]wrote diversification oftheMetazoa.
that “For four of the Big Five mass extinctions of the The Cambrian explosion is in accordance with predic-
Phanerozoic, the marine genera that survived the extinc- tions of classV punctuational theories. At the beginning
tion suffered about 10–20% attrition in the immediately of the evolution of the metazoanclade, many traits, even
following geologic stage, significantly greater than the those that determine body architecture, had the capacity
losses sustained in pre-extinction stages. The stages to turn plastic during peripatric speciations in many
immediately following the three Palaeozoic mass extinc- metazoan lineages. Therefore, both radical remodeling
tions also account for 17% of all order-level losses in of body architecture as well as novel origination therein
marine invertebrates over that interval, which is, again, were possible in the early stages of metazoan evolution.
significantly greater than for other stratigraphic stages Through time, more and more traits became perman-
(no orders are lost immediately after the end-Triassic or ently frozen. Most probably, different traits would lose
end-Cretaceous mass extinctions).” Such a pattern could the capacity to turn plastic in differing successions in
be expected when all the representatives of a clade that particular phyla. Therefore, anagenetic potential faded
survived the mass extinction were irreversibly frozen [3]. and adaptation came to be based on modification of
Acladedepletedofallthespeciesthatcanbeturnedplas- existent plans rather than creation of new ones. Were
tic by peripatric speciation cannot adapt to the changing something, e.g. a virus or humankind, to kill all the
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metazoan species on Earth with the exception ofa single broader spectrum of known biological phenomena than
cockroach species, classical evolutionary theories argue classicgradualisticevolutionarytheories.
this species would differentiate into many new phyla
withradicallydifferentbodyplanstoexploitalltheavail- Reviewers' comments
able niches. The frozen plasticity theory explicitly argues Report1
[3] that it would differentiate into many new species of ClausWilke,TheUniversityofTexasatAustin,UnitedStates
cockroaches,leavingmostniches empty. ofAmerica
Overall, this is an interesting and thought-provoking
ObjectiveExistenceofSpeciesandGenusTaxonomic article, and I'll be happy to see it published. I have one
Categories major request, though: The author states repeatedly that
The punctuational theories suggest that the taxonomic it would be possible to test the various theories against
category of species, and sometimes even that of genera each other. I think the paper would improve greatly
and higher taxa, could objectively denote the existing en- from a section that explicitly suggests concrete tests to
tity, rather than merely being a useful epistemological distinguish theories. As I was reading the paper, I was
constructofbiologists.Withinanypunctuationaltheory,a waiting forsuch a section,but itnevercame.
biological species can be defined as a set of individuals
sharing an identical gene pool throughout the period be- Author’s response: I would like to thank the referee for
tween two speciation events. Similarly, within class III-V encouraging comments. I included the hypotheses to be
punctuational theories, a genus can be defined as a set of tested in particular subchapters and also summarized the
individuals sharing a common exclusive ancestor in the predictions that may distinguish between the discussed
periodbetweentwoperiodsofevolutionaryplasticity. modelsofevolutioninTable2.Ibelievethatcorresponding
specialists (paleontologists, ecologists, molecular biologists
Conclusions etc.) are more competent to suggest proper experimental
The picture of macroevolution postulated by most of designs for concrete tests of particular hypotheses. More-
present punctuational theories of evolution corresponds over, many of these testshave already been performed; see
well with palaentological data and the punctuated equi- Table2andthelistedreferences.
librium model of evolution [57,58] is now a generally
accepted model of the evolution of multicellular life on Report2
Earth[59]. PierrePontarotti,Universited'AixMarseille,France
However, the punctuational models could have a very The author presents quickly the gradualist versus the
important impact on understanding, not only macroevo- punctualist theories of evolution, including his own
lutionary processes, but also microevolutionary and eco- theory (published in 1998) . The readers of this article
logical processes (see Table 2). The picture of ecological would really need to use the two tables (included in this
processes presented by punctuational models differs in article) and to read the articles noted in references to
manyrespectsfromthatprovidedbythecurrenttextbook really understand the differences between the different
theory of evolution and ecology. All of these predictions theories, which is a lot of work. Beside the field specia-
of punctuational models could be tested empirically and/ listsIamafraid thatvery few people willreadthearticle.
or analyzed in greater depth theoretically. Although the I would like to add that the original article describing
previous section mentioned a number of facts demon- the author theory got very few citations, showing that
strating the correctness of the punctuational models of few scientists are aware of the author theory. My advice
evolution, it must be emphasized that none of them can is that the author should rewrite his article and specially
be considered to prove it when taken alone. Alternative theintroduction onamore synthetic way.
explanations for any of the above-mentioned facts that
do not encompass the concept of punctuated evolution Author’sresponse:Iagreewiththerefereethatitisdif-
already exist. However, these alternative explanations are ficult to understand the differences between the discussed
post hoc explanations, sometimes not very probable and theories without careful study of the Table 1. According
sometimes rather awkward and, in addition, frequently to my opinion, a similar study of Table 2 (which sum-
mutually incompatible or incompatible with the currently marizes differences in the implications of particular the-
accepted explanations of other phenomena. In contrast, ories) is not necessary. Actually, the present paper was
the punctuational models of biological evolution were originally part of the paper “Elastic, not plastic species:
establishedpriortoaccumulationofmostofthedatathat Frozen plasticity theory and the origin of adaptive evolu-
now confirm their validity. In my opinion the punctu- tion in sexually reproducing organisms” Biol. Direct
ational theories of evolution offer new predictions that 2010, 5:2. It is therefore useful (but not necessary) for
should be tested and provides explanations for a much readers of the present article to also read the previous