Download 6.6 Selection: Winning and Losing

Genotypes,
Phenotypes,
andSelection
Selectionoperates directly on phenotypesbecausephenotypic
variationamongorganismsrnfluencesthe relativeprobability
of survivaland reproduction.
Thosephenotypes,
tn turn, are influencedby
alleles.Althoughthe relationship
betweenallelesand phenotypesis
rarelyknownandoftencomplex,it is stillpossiblefor allelesat genetic
l o c it o e x p e r r e n csee l e c t r o nP.o p u l a t i ogne n e t i c i s tcsa n s a m p l ei n d i vrdualsfor their genotypeat a locusand comparethe fitnessof individualswith one genotype(r.e.,the averagefrtnessof the genotype)
with the fitnessesof individualswith other genotypes.Whengenotypesdifferconsistently
in theirf itness,the geneticlocuscan be said
(s) is usedto describe
to be underselection.
Theselectioncoefficient
how muchthe genotypesdifferin theirfitness.
I n m a n yc a s e st,h e a l l e l i cv a r i a t i o a
n t a p a r t i c u l alro c u sd o e sn o t
'h
I n t l u e n cteh e p n e n o t y p eI n. s u c hc a s e st,h e a l l e r eas r e d d e n "f r o r n
the actionof seleciionbecausetheyareselectrvely
neutral.Evenif an
alleledoes resultin a phenotypicchange,it stillcould be selectively
neutralif the changein phenotypehas no effect on reproductive
SUCCCSS,
Key Concept
Allelesareselectivelyneutralif they haveno effecton the fitnessof
theirbearers.
Thisphenomenon
oftenoccurswhengeneticvariation
at a locusdoesnot affectthe phenotype
of an individual
6.6 Selection:
WinningandLosing
Fitness:Thesuccess
of an organism
at survivingand reproducing,
andthus
contributingoffspringto future
generations.
Relativefitness (of a genotype):
Thesuccess
ofthe genotypeat
(itsfitness)
producingnew individuals
standardized
by the success
of other
genotypes
in the population(for
example,
dividedby the average
fitnessof the population).
166
In Chapter 2, we introduced the concept of selectionas first developedby Charles
Darwin and Alfred RusselWallace.Both naturalistsrecognizedthe profound importance of selectionas a mechanism of evolution. Natural selection arises whenever
(1)individualsvary in the expressionoftheir phenotypes,
and (2) this variationcauses
some individuals to perform better than others.Over many generations,Darwin and
Wallace argued, selection can drive large-scaleevolutionary change,allowing new
adaptationsto arise.In Chapter 10,we will considerthe origin of adaptationsin more
detail. For now, let's focus on the question of how selectionchangesthe frequencies
of allelesin a population.
The reproductivesuccessof an individual with a particular phenotype is known
as fitness, and selectionoccurs when individuals vary in their fitness. While this
may seem straightforward enough,studying the actual fitness of real organismsis a
surprisingly complicatedmatter. The best way to measurefitness would begin with
tallying the lifetime reproductivecontribution of an individual and then noting how
many of the offspring manageto survive to reproductiveagethemselves.In practice,
however,it's hardly ever possibleto make such a detailedmeasurement.
Scientistssettle insteadfor reliable proxies for fitness.They sometimesmeasure
the probability that an individual survivesto the ageof reproduction,for example,or
they measurethe number of offspring that organismsproduce in a specific season.
Whatever the actualmetric, measuringselectionentailscomparing thesefitnessmeasuresfor many different individuals and relating variation in fitnesswith variation in
the expressionof a phenotype.
Another difficulty when it comes to measuring fitness is the complicated relationship betweengenotypeand phenotype.The fitnessof an organism is the product
of its entire phenotype.We'll seein Chapters7 and 8 how scientistscan make measurementsof phenotypic selectionto study how complex morphological and behavioral traits evolve. But first let's consider how population geneticistsstudy fitness.
Instead of studying an entire phenoqpe, they focus on the evolution of allelesat a
geneticlocus.
Population geneticistsoften distill all of the different fitness components,such
as survival, mating success,and fecundity, into a single value, called w. This value
describesthe relative contribution of individuals with one genotype,comparedwith
the averagecontribution of all individuals in the population. If individuals with a
particular genotype,for example,4747, consistentlycontribute more offspring than
individuals with other genotypes(e.g.,A1A2,A2A2),then their relative fitness will be
greaterthan one. Conversely,if the net contributions of individuals with a genotype
are lower than those of other individuals, the relative fitness will be less than one.
c H A p r E Rs r x r H E w A y s o F c H A N G E :D R r F TA N D s E L E c r r o N
Sometimespopulation geneticistscalculaterelative fitness by comparing the fitness
of all individuals to the fitness of the most successfulgenotype in the population,
rather than by the mean fitness of the population. In such cases,the genotypewith
the highest fitness has a relative fitness of w : 1, and all other genotypeshave relative fitnessesthat are between 0 and 1. Regardlessof which way it is measured,selec
tion will always occur if two or more genotypesdiffer consistentlyin their relative
fitness.The strength of selectionwill reflect how different the genotypesare in their
respectivefitnesses.
To understand how selectionleads to changesin the frequenciesof alleles,we
can consider the contributions of an allele, rather than a genotype,to fitness. But
calculatingthe relative fitness of an allele is more complicatedthan calculatingthat
of a genotype,for two reasons.First,allelesin diploid organismsdon't act alone.They
are alwayspaired with another alleleto form a genotype.If there is, say,a dominance
interaction between them, that interaction will influence the phenotype. Second,
selectiondoes not act directly on alleles.It acts on individuals and their phenotypes.
Nevertheless,it is still possibleto calculatethe net contributions of an alleleto fitness.To do so,we must considerthe fitnesscontributions of individuals heterozygous
for the allele as well as that of homozygotes,and weigh how many individuals with
each genotype are actually present in the population and contributing offspring to
the next generation.Box 6.5 showshow the net fitnesscontribution of an allele,called
the averageexcessof fitness, is calculated.
The averageexcessof fitness for an allele can be used to predict how the frequency of the allelewill changefrom one generationto the next:
Lp:px(ao,
Averageexcessof fitness (of an
allele):Thedifference
betweenthe
averagefitnessof individuals
bearing
the alleleandthe average
fitnessof the
oooulation
asa whole.
w)
where Ap is the change in allele frequency due to selection,p is the frequency of
the A1 allele,w is the averagefitness of the population, and a,a,is the averageexcess
of fitness for the A7 allele.This equation can tell us a lot about the nature of natural
selection.
The sign of the averageexcessof fitness(ao) , f or example,determineswhether
selectionincreasesan allele'sfrequency or decreasesit. Whenever an allele is present in a population, its frequency is greaterthan zero; and as long as the population
exists,its averagefitness,w, is also greaterthan zero (becausew is the sum of all individuals with each genotype times their respectivecontributions of offspring to the
next generation).Sinceboth p and w are by definition positive,the sign of Ap must
be determined by the averageexcessof fitness of the allele. Whenever the fitness
effectsof an allele are positive, selectionshould increasethe frequency of the allele
over time; the converseis true when the fitnesseffectsare negative.
This equation also tells us that the speed of increase(or decrease)in the frequency of an allele will depend on the strength of selectionthat it experiences-the
magnitude of aa,.When the averageexcessof fitness is very large (positive or negative), the resulting changein allele frequency will be greater than when the average
excessof fitness is smaller.
Finally,this equation shows us that the effectivenessof selectionat changing an
allele'sfrequency dependson how common it is in the population.When an allele is
very rare (p : 0), the power of selectionto act will be low even if the fitness effects
of the allele are pronounced.
SmallDifferences,Big Results
Alleles can differ enormously in fitness. A single mutation can disable an essential
protein, leading to a lethal genetic disorder. These alleles experience strong negative
selection because children who die of such a disorder cannot pass on the mutation to
their offspring. As a result, a typical severe genetic disorder affects only a tiny fraction
of the population. But even when alleles are separated by only a small difference in
their average excess of fitness, selection can have big long-term effects. That's because
populations grow like investments earning interest.
A N DL o s r N G
6 . 6 s E L E c r o Nw
: rNNtNG
'167
E
S e l e cti o nC h a n g e A
s l leleFr equencies
ll
Let'sconsiderhow naturalselectionchangesallelefrequenciesby
equilibrium
at a genetic
startingwith a populationin Hardy-Weinberg
locus.Wewillthencalculatehow selectionpullsihe populationout of
of the alleles.
equilibriumand,in so doing,shiftsthe frequencies
We'llusethe samelocusand allelesthat we did in Box6.2,A, and
Ar, and starting frequenciesof p and 4 respectively.We'vealready
equilibrium,the freseenthat for a populationin Hardy-Weinberg
quenciesof eachpossiblegenotypeare
f(A,A') = P'
f(A1A') : 2pq
Genotype: A,A,
f,rtt
(p'zxwrr)fw
\q'xwrr)/w
p,tr = l(p2 x w'r)f il + l(pq x n',) I *)
:(p'xwttlpexw,r)fw
l(q2 x wrr)f wl + l(pq x *rr) /fi)
:(qrxwzzrpexwp)fw
q,*t:
Naturalselectionis a mechanismof evolutionbecauseit can
causeallelefrequenciesto changefrom generationto generation.
fitnesses)to our
Now that we haveappliedselection(as differential
genotypes,let them reproduce,and calculatedthe new allelefrequenciesin the offspringgeneration,
the questionis, how havethe
changed?
allelefrequencies
To calculatethe changein frequencyof the A, allele,Ap,we subp.ay.
p, from the newfrequerte\,
tract the startingfrequency,
LP=Pt+1-P
roqnontirrolrr
r e e y v v L t v v ' J .
(timet + 1),
genotypefrequencies
Tocalculatethe
afterselection
we needto multiplythe frequencyof eachgenotypeby its relative
fitness,In essence,this simulatesa parentalpopulationthat reproduces to generatean ofispringgenerationwith zygotegenotype
in the
frequencies
oI p2,Zpq,and q2(theseare the allelefrequencies
populationimmediately
Theseoffspringthenexpebeforeselection).
matureadults
rienceselectionas they developinto reproductively
themselves,who then mate to produceyet anothergenerationof
progeny.The relativesuccessof individualswith each genotypeat
for mates,
survivingthroughto adulthood,competingsuccessfully
relative
and producingviableoffspringis reflectedin their respective
fitnessvalues-selectionis actingon this geneticlocus,Becauseof
selection,
somegenotypeswill increasein frequencyat the expense
of othersin the nextgeneration.
So,at time (r + l), the relativeabundanceof eachgenotypefrequencywillbe represented
by the following.
Genotype:
A'A,
AtAz
AzAz
Numbers:
p2 \ wt
2pq X wp
q2 x wzz
with each of thesegenotypesin this
But the numberof individuals
new generationwill not be the same as in the previousgeneration.
with
or individuals
Individuals
may haveproducedmultipleoffspring,
particulargenotypesmay havediedbeforebreeding,
for example.To
for eachgenotype,we
convertthesenumbersinto new frequencies
needto siandardizethem by the total numberof individualsin the
Thisnewtotal isjust the sum of the numbersof indinewgeneration.
vidualshavingeachpossiblegenotype:
w = pt X w111- 2pq X wp * q2 X wzz
w is alsocalledthe averagef itnessof the populationsinceit's the sum
of the fitnessesof each genotypemultipliedby (i.e.,weightedby)
the frequencies
at whichthey occur.Usingthe averagefitnessof the
populaiion,
afterselection
we can now turn the relativeabundances
intofrequencies.
168
(zpqxwt)fw
and
Selectionactson a geneticlocuswheneverthe genotypesof that
locus differ in their relativefitness.In this case,we can assignfitrespectively.
Fitnesscan
nessesto eachgenotypeaswn,wn,andw22,
to the age of
act throughmany components,such as survivorship
reproduction,
matingsuccess,and fecundity,but ultimatelytheseall
translateintothe successof eachgenotypeat contributingoffspring
Here,we'll let our fitnessmeasuresencomto the next generation.
passallof these,so that w,,,w,r,andw, denotethe proportional
conwith A,A,,AtA2,andA2A2geno'
tributionsof offspringby individuals
r J P v r '
A,A,
And from theseresults,we can calculateeacha//e/efrequencyin this
plushalf
newgenerationas the frequencyof homozygoteindividuals
the frequencyof heterozygotes:
f(A,A'1 : nz
hrnoc
AtAz
a N Ds E L E c r l o N
c H A p r E sRt xr H Ew A y so F c H A N G ED: R I F T
p = pz + p4. To expressthis overthe
The startingfrequency
it by I rntheformof wf w, sothat
denominator,
w,wemultiply
p = (p' x w + pq x w) / w.Ihereforc.
LP=P,+I_P
: l ( p ' x w t r 4 p Qx w p ) f w ) - [ ( p t x w + p q x w ) / w )
= ( p ' x w t * p 4 x w . r z -p ' x i - p q x i ) l i
= p x (p X w,, I QX wn - p X w - q x w)I w
: b l . ) x ( p x w , 1- p x w + q x w e - S x u )
= (p/O) x [p x (w,, - ,)] + lq x (w,,- w))
The term [p x (r,, - t)] + lq x (r', - t)l is known as the
averageexcessof fitnessfor the A, allele.lt is the mean difference
havingthe A, alleleand the fitness
betweenthe fitnessof individuals
the averageexcessof fitness
of the populationas a whole.In essence,
eventhoughalleleshaveno
is a wayto assignf itnessvaluesto a//e/es,
phenotypesof their own-they havephenotypesonly whenthey are
Box Figure6.5.1 TheaverageexcessoffitnessoftheA, allele(a1,)
and
is calculated
from the frequencyof A1allelesin homozygotes
differences
in
fitness
from
the
eachadjustedby their
heterozygotes,
population.
meanofthe
Proportion
of A' alleles
of A, alleles
Proportion
present
in ArA,
that are
that are presentin A,A,
heterozygousindividuals
homozygousindividuals
-w)l +
Differencein fitness
betweenA,A, individuals
and the meanfitnessof
the population
ex(wp-w)l
Differencein fitness
betweenA,A, individuals
and the meanfitnessof
the population
combinedin pairsto form genotypes.
Thus,althoughit is individuals with genotypeswho experienceselectionand who differin their
relativecontributions
to subsequentgenerations,
we can stillassign
relativefitnessesto a//e/esin the form of their averageexcessof f itness.Thisapproachallowsus to seeclearlythe relationship
between
a l l e l ea
s n df i t n e s s .
We can now expressthe changein allelefrequenciesresulting
from selectionas
A,p:(pfw)xao,
0, whetherAp is positiveor not dependsentirelyon the sign of ar,,
This meansthat whetherthe alleleincreases
in frequencyfrom generationto generation,
or decreases,
dependson whetherits average excessof fitnessis positiveor negative.
Whenthe net effectof
an alleleis an increasein f itness(averageexcessin fitnessis greater
than 0), meaningthat the alleleexperiences
positiveselection,the
alleleis predictedto increasein f requency.
Conversely,
whenthe net
effectof an alleleis a decreasein fitness(averageexcessin fitnessis
lessthan 0), meaningthat the alleleexperiences
negativeselection,
the alleleis predrcted
to decreasein frequency.
Second,the averageexcessof fitnessdependsnot only on the
fitnessesbut a/soon the frequencles
of eachallele.This meansthat
the effectof selectionactingon an allelewilldependon the population contextin which it is found.Forexample,two populationswith
identicalfitnessesfor eachgenotypecouldhavevery differentaverageexcesses
of fitnessif they havedifferentallelef requencies
before
selection.Selectionmay causerapidchangesin allelefrequencyin
one population,but only minor changesin the other.Whenan allele
rsvery rare(as it wouldbe if it had recentlyarisenthroughmutation)
selectionmay be much lesseffectiveat changingits frequencythan
it wouldbe if the alleleweremore common.
Ap: p x ("o,/A)
whereao,is the averageexcessof fitnessof the A, allele.We can also
calcuiatethe averageexcessof f itnessfor the,42alleleas
a n , : l p x ( w n - . ) l + l q x ( w r ,- w ) l
and the predictedchangein frequencyof the 42 alleleas a resultof
selectionas
A q : ( qf w ) x a o ,
Lq:qx("or/r)
Severalimportantconclusions
shouldbe evidentfrom thesecalculations.First,becausep andw are alwaysgreaterthan or equalto
Let's say you invest $100 in a fund that earns 5 percent interest each year. In
the first year,the fund will increaseby $5. In the second,it will increaseby 95.25.In
every subsequentyear,the fund will increaseby a larger and larger amount. In 50
years,you'll have more than 91,146.Becauseof this acceleratinggrowth, even a small
changein the interest rate can have a big effect over time. If the interest rate on your
fund is 7 percent insteadof 5 percent,you'll make only an extra $2 in the first year.
But, in 50 years,the fund will be more than $2,945-close to triple what an interest
rate of 5 percent would yield. Slight differencesin fitness get magnified in a similar
way. over time, an allelewith a slightly higher averageexcessfor fitnesscan come to
dominate a population.
Unlike drift, this compounding power of natural selectionis more effective in
larger populations than smaller ones. That's becausegenetic drift can erode allelic
variation in small populations,even eliminating beneficialmutations. In large populations, by contrast,genetic drift has a weaker effect. Figure6.12shows a computer
simulation that illustratesthis effect,in which an allelewith a selectiveadvantageof
5 percent is added to populations of different sizes.In the big population of 10,000
Figure6.12 Naturalselectionis ineffective
in smallpopulations
and
effectivein largeones.Thesegraphsshowthe resultsof computer
simulations
of a populationin whichan allelethat raisesfitnessby
5 percentis addedto populations
ofdifferentsizes(eachcoloredline
represents
a differentsimulation).
In all cases,
the allelestartsat a
10individuals
o
i3.D
>.8
frequencyof 0.1(10percent),
andsubsequent
changesin its frequency
resultfrom the combinedactionof selectionanddrift. In the smallest
populations,
the alleledisappears
from halfthe simulations,
even
thoughit hasbeneficial
effectson fitness.But in largepopulations,
the
allelebecomesmorecommonin all of them.(Adaptedfrom Bell2OO8.)
1 O Oi n d i v i d u a l s
1 0 0 0i n d i v i d u a l s
1 0 , 0 0 0i n d i v i d u a l s
100o/o
50%
ri
cJ
_o
0o/o
80 120
80 120 0 20 40 60 8 0 120
Generation
80 120
6 . 5 s E L E c T t o Nw
: tNNlNGAND LostNG
159
individuals, it becomesmore common in all the simulations.In a population of 10
individuals,however,it disappearsfrom half of the simulations.High relative fitness,
in other words, is not a guaranteethat an allele will spread-or even persist-in a
population, becausethe effectsof drift can be stronger than those of selectionwhen
populations are very small.
Patternsof Selectionin TimeandSpace
Pleiotropy:Theconditionwhen a
mutationin a singlegeneaffectsthe
expression
of manydiferent phenotypic traits.Pleiotropyis consideredto
be antagonistic
if a mutationwith beneficialeffectsfor one trait alsocauses
detrimentaleffectson other traits.
Selectioncan produce patterns of surprising complexity. In the next few sections,
we'll consider how those patterns are generated,starting with one important fact
about mutations: they often have more than one effect on an organism.These multiple effects are the result of the interconnectednessof biology. A single regulatory
gene,for example,can influence the expressionof many other genes.This phenomenon is known as pleiotropy.
The evolution of resistancein mosquitoeson the coast of Francedemonstrates
how pleiotropy can affect the nature of selection.When the Esterl allele emerged
in the early 1970s,it provided mosquitoeswith resistanceto insecticides.But it had
other effectson the mosquitoesas well. Researchersat the University of Montpellier
have found that the Esferr mosquitoes have a higher probability of being caught by
spiders and other predatorsthan insecticide-susceptible
mosquitoesdo, for example
(Berticatet al. 2004).A mutation that has improved fitness in one context-by providing resistanceto insecticides-has also alteredthe physiologyof thesemosquitoes
in a deleteriousway that might well lower their fitness in other contexts.This form
of pleiotropy, in which the effectsof a mutation have opposite effectson fitness,is
known as antagonisticpleiotropy.
The net effect of an allele on fitness is the sum of its pleotropic effects on the
organism in question.Even if an allelehas some beneficialeffects,it may,on balance,
lower reproductive successoverall. How the balance tips depends on the environment in which an organism lives. For mosquitoeson the Frenchcoast,any protection
againstinsecticidescan dramaticallyraisefitnessbecausesusceptiblemosquitoesare
dying in droves.Even if the extra esterasesmake the mosquitoesmore vulnerable to
predators,they still, on balance,make the insectsmore fit.
Such is not the casefurther inland. There, the Esterlalleleprovides no benefit
from resistancebecausethere's no insecticideto resist.Instead,the allele lowers fitnessby making the insectseasierprey. The curves in Figure5.2 are the result of this
shift in balance.Selectionraised the frequency of Estertalong the coastwhile keeping it low inland. This differencewas maintained even as mosquitoeswere migrating from one site to another and their geneswere flowing acrosssouthern France.
As soon as copies of Estey'left the insecticidezone, they were often eliminated by
selection.
As Figure6.13 shows, the Esterlallelebecame common along the coast in the
1970s,but it later becamerare.That's becausea new allele,known as Ester4,emerged
around 1985.It alsoled to the overproductionof esterases.
Intriguingly, Esferabecame
more common as Esterlwasdisappearing-even though it provides slightly /essprotection againstinsecticidesthan the older allele.A clue to its successcomesfrom the
slope of its curve. Esferadoes not drop off steeply as you go inland. It's likely that
Esferadoesnot impose the high cost of Esferr.Selectionfavors the allele on the coast,
but mosquitoes don't pay a price for carrying it if they migrate inland (Raymond et
a l .1 9 9 8 ) .
Fifty ThousandGenerationsof Selection:
ExperimentalEvolution
Some of the most important insights into how selectionaffects alleles have come
from experimentsthat scientistsset up in their laboratories.They can carefully control the conditions in which organisms grow and reproduce, and they can analyze the
entire population under study.
17O
c H A p r E Rs t x r H E w A y s o F c H A N G E : D R r F TA N D s E L E c r t o N
o
_OJ
o
U
c
(U
100%
100o/o
80%
80o/o
60o/o
60"/o
40%
40%
20o/o
20o/o
Figure 6.13 Thisseriesof graphs
extendsthe historyof resistancealleles
in mosquitoes
that we encountered
in
Figure6.2.After spreadingwidely in
gradually
the 1970s,
the Ester'allele
becamerarerin the 1980sand 199Os
while anotherallele,knownas Estera,
becamewidespread.
The shift may
reflecta physiological
costimposed
on the insectsby Esterl.Esteraalleles
may conferresistanceon mosquitoes
without this cost,makingits relative
f
OJ
L
0
0
111213141
Kilometers
fromthecoast
111213141
Kilometers
fromthe coast
100o/o
10Qo/o
80%
80Yo
aio/wv/u
60o/o
fi
40o/o
40o/o
9.
20o/"
20o/o
t
o
ts
o
fitnesshigheranddrivingit to higher
(Adaptedfrom Raymond
frequencies.
et al.1998.)
f
u
0
0
111213141
Kilometers
fromthe coast
Negativeselection:Selectionthat decreases
the frequency
of alleleswithin
a population.
Negativeselectionoccurs
111213141
Kilometers
fromthe coast
One of the longestrunning of theseexperimentsis taking placeat Michigan State
University (Barrick et al. 2009).Richard Lenski started it in 1988with a single,E coli
bacterium. He allowed the microbe to produce a small group of geneticallyidentical
descendants.From these clones,he started 12 genetically identical populations of
bacteria(Figure6.14).Eachpopulation lives in a flask containing 10 milliliters (ml) of
a solution. The bacteriagrow on glucose,but Lenski supplied only a limited concentration. Each day-including weekends and holidays-someone in Lenski's group
withdraws 0.1ml from a culture and transfersthat into 9.9 ml of fresh medium. They
do this for eachofthe 12 populations,keeping eachpopulation separatefrom the others.The bacteriagrow until the glucoseis depletedand then sit there until the same
processis repeatedthe next day.In a singleday,the bacteriadivide about seventimes.
AII of the bacteria descendedfrom a single ancestralgenotype.As they reproduced, they occasionallyacquired new mutations. Alleles that lowered their reproductive successexperiencednegative selection.Any allelesthat spedup their growth
or boosted their survival rate experiencedpositive selection. The random sample
Lenski took eachday from eachflask reflectedthese shifting frequenciesof alleles.
Every 500 generations,Lenski stored some of the bacteria from each of the 12
lines in a freezer.Freezingdid not kill them, so the samplesbecamea frozen fossil
record that could be resurrected at a later time. Thawing them out later, Lenski could
directly observehow quickly the ancestraland descendantbacteria grew under the
sameconditions.He could thus directly measuretheir changein averagefitness.
The experiment has now progressedfor 50,000 generations.(It would have
taken about a million years if Lenski were using humans as experimentalorganisms
instead of bacteria.)Figure6.15shows the evolution of Lenski'sE. coli over the first
20,000generations.The bacteriabecamemore fit in the new environment than their
ancestorshad been in all 12 lines.The averagecompetitive fitness of the populations
increasedby approximately 75 percent relative to the ancestor.In other words, all 12
of the bacterial populations evolved in responseto natural selection:they had accumulated mutations that made them more efficient at growing under the conditions
that Lenski set up (Barricket al. 2009).
Preservinga frozen fossil record doesn't just allow Lenski to compete ancestors
against descendants.It also allows him and his colleaguesto compare their DNA.
Becausethe experiment began with a single microbe, and becausethe microbe's
descendantsreproducedasexuallywithout horizontal gene transfer,the researchers
wheneverthe averageexcessfor fitnessof an alleleis lessthan zero.
Positiveselection: Selectionthat increases
the frequencyof alleleswithin
a population.
Positiveselectionoccurs
wheneverthe averageexcessfor fitnessof an alleleis greaterthan zero.
Figure6.14 RichardLenskiand his
colleagueshavebred bacteriafor over
20 yearsusingthis method.
#
OneEscherichia
coli
$
RNRRRRRRRRRR
se$€'eM$ssaereD€.€9
12genetically
identical
lines(flasks)
!
I
f
Morning:
eachflaskgetsnew
supplyof glucose. <-.1
r!
+t
glucose
Afternoon:
runsout. I
&l
'T
Nextday:smallsamPle
of re#
surviviors
fromall 12lines
transferred
to new flasks.
.&
Sampleof eachline
frozen for later study
every500 generations.
6 . 6 s E L E c l o N :w r N N r N G
A N DL o s r N G
171
2.0
o
-c
1.8
qJo
.=P
PO
1.6
(Jn
1A
l
CJG
o(J
' 1 0 , 0 0 0 15 , 0 0 0
5000
Time(generations)
Figure6.15 Thebacteriain Lenski's
natural
experimenthaveexperienced
New mutationshavecaused
selection.
faster
to reproduce
the descendants
u n d e rt h e c o n d i t i o nosf t h e e x p e r i m e n t
did.(Adaptedfrom
thantheir ancestors
Cooperand Lenski2000.)
Epistasis:
Occurswhenthe effectsof
a n a l l e l ea t o n eg e n e t i cl o c u sa r em o d i fied by allelesat oneor moreotherloci
172
20,000
can be confident that allelespresent in descendantsbut not in the original ancestor
must have arisen through mutation during the experiment itself.
have been investigatingthesenew mutations,observ
Lenskiand his colleagues
ing how they affect the fitness of the bacteria. In one experiment, they selecteda
singlemicrobefrom generation10,000to analyze(Stanek,Cooper,and Lenski2009).
They transferred1296 different segmentsof its DNA into ancestralbacteriafrom
the same line. Then they mixed eachkind of engineeredbacteriawith unmanipu
lated ancestralones and allowed them to grow side by side. These trials revealed
one evolvedsegmentin particularthat increasedthe fitnessof the bacteria.Further
to pinpoint the mutation within the seg
analysisallowedLenski and his colleagues
A singlenucleotidewas mutatedin a protein-bindingsite,
ment that was responsible.
calledBoxGl,which regulatesa pair of nearby genes.Thesegenesencodeproteins
calledGlmS and GlmU,which help synthesizethe bacterialcell wall. To confirm that
the mutationwas indeedresponsiblefor increasingbacterialfitness,they insertedthe
singlenucleotideinto BoxGl in the ancestralbacteria.That tiny insertion raisedthe
relativefitnessof the bacteriaby 5 percent.
Having identified this mutation and measuredits fitness,Lenski and his col
leaguesthen setout to traceits origin.At somepoint during the evolutionof that par
the mutation must have emergedand therl
ticular line of E. coli,they hypothesized,
increasedin frequency.They turned to the line'sfrozenfossilrecord,selectedbacteria
sample,and examinedthem for the presenceof the BoxGl
from each5O0-generation
mutation. None of the bacteriathey examinedfrom generation500 had the BoxGl
mutation.So the mutation must havearisenafter that point. The bacteriain genera
tion 1000told a differentstory:45 percentof them carriedthe mutation.And in gen'
found that 97 percentof the bacteriahad it. This rapirl
eration 1500,the researchers
s p r e a di s t h e k i n d o [ p a t t e r ny o u ' de x p e c tf r o m a m u t a t i o nt h a t i n c r e a s efsi t n e s s .
It's not immediatelyobvioushow the mutation benefitsthe bacteria,but Lenski
have some clues.In bacteriawith the BoxGl mutation,lessGlmS
and his colleagues
It's possiblethat the bacteriadivert resourcesfrom buildinc
and GlmU is expressed.
thick cell walls to other functions,speedingup their reproduction.
The BoxGl mutation is just one of a growing collectionof beneficialmutatiorl'
that Lenski and his colleagueshave identified in their long-term evolution experi
ment. These mutations arose sequentially in the bacterial lines, building on tht'
comparisonsof these mtrt,r
increasedfitness of previous mutations. Large-scale
tions are revealing lessons about how beneficial mutations interact. Some mrtt.r
tions, for example, are beneficial only when they follow certain other mutatiorl'
That's becausetheir effectson the bacteria interact in a processknown as epistasi.
Only one line of E. coli evolved the BoxGl mutation. But other mtrtations aro''
independently in several different lines, and the scientistsfound three genes th.''
mutatedin all 12 lines.While evolutionmoved in the sameoveralldirectionin tht'::
experiment-a rapid increasein fitness followed by a tapering off-the mutatiorl'
that drove this changewere not the same.We'll revisit the contingency and con\t.:
genceof adaptationsin Chapter10.
c H A p r E Rs l x r H E w A Y s o F c H A N G E :D R I F TA N D s E L E c r l o N
Dominance:AlleleversusAllele
Bacteriaare useful for running evolution experimentsbecausetheir haploid genetics
are relatively simple. Selectioncan be more complex in diploid organisms,however,
due to the interactions between the two copies of each genetic locus.As we saw in
Chapter 5, an allele can act independentlyof its partner,or it can be either dominant
or recessive.Eachof thesestatescan have different effectson the courseof selection.
Let's first consider allelesthat act independently.In Chapter 5, we introduced
the work of |oel Hirschhorn and his colleagueson the geneticsof height. One of the
genesthey discovered,HMGA2, has a strong influence on stature.Peoplewho carry
one copy of a variant of the genewill grow about half a centimetertaller,on average,
than people who lack it. Peoplewho are homozygous for the allele get double the
effect and grow about a centimetertaller. Such interactionsbetween allelesare called
additive becausethe effectsof the allelescan be predicted simply by summing the
copiesthat are present.
Additive alleles are especiallyvulnerable to the action of selection.Whenever
an additive allele is present,it will affect the phenotype,and selectioncan act on it.
Favorableallelescan be carried all the way to fixation becauseheterozygousindividuals will have higher fitness than individuals lacking the allele,and homozygousindividuals will fare even better. Eventually,the population will contain only individuals
homozygousfor the allele (Figure6.16).Conversely,deleteriousallelescan be swept
all the way out of a population. Every time the allele is present,it is exposedto selection, and its bearerssuffer lower fitnessthan other individuals lacking the allele.Here
too, the result will be absolute:selectionwill remove the allele completely from the
population.
Additiveallele:An allelethat yields
twice the phenotypiceffectwhen two
copiesarepresentat a givenlocusthan
whenonlya singlecopyis present.
Additiveallelesare not influenced
by
the presence
of otheralleles(e.g.,there
is no dominance).
Figure6.16 Effects
recessive,
anddominant
alleles.
Eachline
of positive
selection
onadditive,
predicted
givena selection
shows
changes
in allelefrequency
coefficient
of 0.05.Alleles
with
phenotypes
to
they
will
increase
from
additiveeffectson
arealways
exposed selection,
so
steadily
Recessive
alleles
are
themoment
theyarisedueto mutation
untiltheyarefixedin thepopulation.
likely
genotypes.
notexposed
initially,
because
they
are
to
occur
only
in
heterozygous
to selection
Theymaylingerforthousands
of generations
untildrifteitherremoves
themor increases
their
homozygous
recessive
individufrequency.
Eventually,
if driftincreases
theirfrequency
sufficiently,
willbeginto increase
alswillbeginto appear
inthepopulation.
Assoonasthishappens,
selection
Dominant
alleles
areexposed
to selection
thefrequency
of thealleleandswiftlycarryit to fixation.
However,
increasimmediately
infrequency
rapidly.
asdominant
alleles
become
andwillincrease
(by
recessive)
increasingly
rare.
As
we've
inglycommon,
thealternative
alleles definition,
become
justseen,rarerecessive
ofselection
they
are
carried
in a
alleles
areinvisible
to theaction
because
(Adapted
fix
a
completely
allele.
from
heterozygous
state.Thusselection
alonecannot
dominant
Conner
andHartl2004.)
100%
80o/o
=l
OU-/o
(u
E 40yo
L
20o/o
0o/o
1 0 0 2 0 0 3 0 0 400
500 600 700 800
Numberof generations
900 1000 1100
6.6 selecrtolt: wtNNtNG AND LostNG
173
Dominant and recessivealleles.on the other hand. are not additive. A dominant
allelewill overshadowthe other allele at the same locus.It will have the same effect
on an individual's phenotype whether one copy is present in a heterozygoteor two
copiesare in a homozygote.A recessiveallele,on the other hand, can affect the phenotype only when it is paired with another recessiveallele-that is, when it occursin
a homozygousrecessiveindividual.
This interaction blunts the power of selectionto spread allelesto fixation or to
eliminate them from a population. When a mutation gives rise to a new recessive
allele,the individual carrying it is, by necessity,a heterozygote.As a result, the new
recessiveallelewill have no effecton its phenotype.The heterozygousindividual may
or may not passdown the new recessivealleleto its offspring; if it does,its offspring
will be heterozygotesaswell becauseno other individuals in the population carry the
allele (they are all homozygousfor the ancestralallele).Even if, by chance,some other
member of the population also acquiresthe same recessivemutation, the odds will
be tiny that the two alleleswill end up combined in a homozygote.As a result, rare
allelesare almost alwayshousedin heterozygousindividuals.
Since recessiveallelesdon't affect the phenotype of heterozygotes,they remain
largely hidden from the action of selection,Drift alone determineswhether they persist in the population.Eventually,drift may increasea recessiveallele'snumbers,such
that heterozygotesbecomefairly common. At that stage,the odds becomemore likely
that two heterozygoteswill encounter each other and mate. Only then do homozygous recessiveoffspring begin to appear in the population. And only then can selec
tion begin to act on the recessiveallele.
If the effects of the allele are positive, selection can quickly increase the fre
quency of the allele.As the allele spreads,more and more individuals are born with
homozygousrecessivegenotypes.Becausethe dominant alternative allele performs
lesswell (its averageexcessfor fitness is negative),it declinesin frequency.Because
these negativeeffectsare present in both heterozygousand homozygousgenotypes,
this deleteriousallelehas nowhere to hide. Selectioncan purge it completelyfrom the
population. Thus, after a long period during which the recessiveallele experiences
only drift, it can rapidly spreadto fixation (seeFigure 6.16).
Selectionhas a different effect on deleteriousrecessivealleles.If drift createsa
high frequency of heterozygotes,they will start to produce homozygotesthat start to
suffer lowered fitness.As a result, the allelewill becomeless common. But selection
cannot remove the allele completely,despite its low fitness.As soon as the recessivt,
allele'sfrequencydrops low again,it occursonly in a heterozygousstatewhere it i.
hidden once more from selection.
Selection has a very different impact on a dominant allele that appears in .r
population. Right from the start, the new dominant allele is exposedto selection.ll
its effects are favorable (its averageexcessof fitness is positive),it spreadsrapidlr
through the population. At first, while it is still rare, it is present almost entirely in
heterozygousindividuals. That's becauseall of the rest of the population carries tl'rt'
ancestralallele at that locus. As the dominant allele becomesmore common, ho\\
ever,heterozygousindividuals begin to pair with other heterozygousindividuals antr
produce homozygous individuals that carry two copies of the new dominant alleltThey experiencethe same fitness advantageas heterozygotes,and the frequency r':
the allele continuesto climb.
As the frequency of the new dominant allele approachesfixation, the populatio:
is increasingly composed of dominant homozygotes.Fewer and fewer individua.are heterozygous.Even fewer offspring that are homozygousfor the ancestralallel,
are produced. Eventually,the ancestral(now recessive)allele becomesso rare th.,'
heterozygotesalmost never meet and mate. At this point, the recessiveallele is prtent only in heterozygotes.Sincethe recessiveallelehas no effecton the phenotype, :
heterozygotes,there is no longer any differencein fitness among individuals caus(':
by this genetic locus.There is no more selectionacting on the allele.Its fate is nr'.,,
governedby drift. Thus,while selectioncan drive a dominant alleleto high frequen, .
174
c H A p r E Rs r x r H E w A y s o F c H A N G E :D R I F TA N D s E L E c r r o N
very rapidly, it cannot drive the allele all the way to fixation, becauseit cannot elimi
nate the ancestralrecessiveallele.
Thesedynamics help explain why populationsharbor so much geneticvariation,
and why so much of this variation is comprisedof rare recessivealleleswith deleterious effects.Whenever mutations generatealleleswith dominance interactions,the
potential arisesfor deleteriousrecessiveallelesto hide from selectionin a heterozygous state.And as long as they are rare, the deleteriousallelescan persist in populations for thousands of generations,until they are eventually lost to drift. We'll see
later in this chapter how this variation can rear its ugly head when recessivealleles
are flushed out of hidine.
Mutation-Selection
Balance
Another factor that promotes genetic diversity in populations is the origin of new
mutations. At first, this might seem like a weak force, since the rate of new mutations at any particular genetic locus is typically very low. According to one recent
study (Roachet al. 2010),the mutation rate in humans is 1.1 X l0-o per position per
haploid genome.In other words, a gene would have to be copied on averagefor 100
million generationsbefore a particular position mutated.
But we actually don't have to wait nearly so long for mutations to arise.For one
thing, each human genome is huge, containing 3.5 billion base pairs. With such a
big target,even a low mutation rate will be guaranteedto produce some mutations.
About 70 new mutations arise in each baby, according to Roach et al. (2010).And
sinceabout 140 million babiesare born eachyear,we can estimatethat about 9.8 billion new mutations are arising in humans eachyear. While the odds of a mutation
striking any particular locus as it is being copied are extremely low, the rate at which
mutations arise in the entire human population is not.
While many of thesemutations turn out to be neutral,a significant number have
important phenotypic effects.Cystic fibrosis, for example, is a genetic disorder in
which the lungs build up with fluid, leading to pneumonia. The median life expectancy for Americans with cystic fibrosis is 35. The diseaseis causedby mutations to
the CFI"Rgene,which encodesa chloride channel in epithelial cells. More than 300
different disease-causing
allelesof the CFIR gene have alreadybeen identified (Tsui
1992).Cysticfibrosis is considereda simple geneticdisorder,becauseonly a single
gene is involved. As we saw in Chapter 5, other traits are typically far more complex,
influencedby hundreds or thousandsof genes.A mutation to any of those genescan
potentially have an effect on a complex trait.
Mutations are thus an important mechanism of evolution, injecting new alleles
into gene pools and thus changing the allele frequencies.Once a new mutation
arrives,drift and selectionmay begin to act on them. If the alleleis deleterious,selection will act to reduceits frequency.Meanwhile,however,new mutations at that locus
will keep emerging, lifting up the allele'sfrequency.The production of new mutations and negativeselectionwill act like opposingteamsin a tug-of-war.Together,this
mutation-selectionbalancewill result in an equilibrium frequency of the allele (we
show how to calculatethis equilibrium in Box 6.6).Mutation-selectionbalancehelps
explain why rare deleteriousalleleswith recessiveeffectspersist in populations,adding to geneticvariation (Crow 1986,Templeton2006).
SelectingDiversity
We ve seen how selection can reduce genetic diversity by driving some alleles to
fixation and eliminating othersfrom populations.But under certain conditions,selection actually fosters variation. In some situations,for example,the relative fitness
of a genotype is high when it is rare, but low when it is common. Selectionin these
casesis known as negative frequency-dependent selection. Before we explain how
Negativefrequency-dependent
selection: Raregenotypeshavehigher
fitnessthancommongenotypes.
This
process
canmaintaingeneticvariation
within oooulations.
6 . 6 s E L E c r t o N :w t N N t N G A N D L o s t N G
175
i,llt
Key Concepts
Whenthe componentsof variationact independently,
their effectsareadditive,so that variation
attributableto genesandvariationattributableto the environmentsumto yieldthe total phenotypicvariance
of the sample.
Thisallowsbiologists
to estimatethe relativecontributions
of different
sourcesofvariationto the phenotypicdistributionobserved.
The heritabilityof a trait is the proportionof phenotypicvariancethat is dueto geneticdifferences
amongindividuals.
Broadsenseheritabilityreflectsall of the geneticcontributionsto a trait'sphenotypicvariance
including
additive,
dominant,andepistaticgeneefects.lt alsoincludes
influences
of the parent
phenotypeon the environmentof offspringthat cancausesiblingsto resembleeachother (maternal
and paternaleffects),suchas nestqualityor qualityof food provided.
7.2 TheEvolutionary
Response
to Selection
Oncewe understandthe sourcesof variancein a quantitative trait, we can study how
that trait evolves.Let's say we want to study the evolution of body size in the fish
living in a lake.We examine the reproductivesuccessof fish. If there's a nonrandom
differencewith respectto body size,selectionexistsfor that trait. Figure7.6 illustrates
someof the forms this selectioncan take.If selectionfavors phenotypesat one end of
a distribution of valuesfor a trait, the population may evolve in that direction. In our
lake,we might find that small fishes are more likely to survive droughts than larger
ones,for example.This type of selectionis called directional selection.
In other cases,selectionmay favor valuesat the middle of the distribution, while
the reproductivefitness of organismswith traits at the ends of the distribution may
c
o
f
Figure7.6 Selection
canact in different wayson a population.
Directional
selection(left)favorsindividuals
at
AJ
u
one endof a trait distribution,
suchas
animalswith smallbodysize.As illus-
>-$b
(e.9.,size)
Phenotype
trated,largeindividuals
havelowerfit(negative
nessthan smallerindividuals
DIRECTIONAL
SELECTION
selectionagainstlargesizesis indicated
by the red shading).After selection,
and providedthe trait is heritable,
-
the distributionof phenotypes
should
shiftto the left,towarda smallermean
bodysize.Stabilizing
selection(middle)
favorsindividuals
with a trait nearthe
populationmean.In this case,fishwith
the largestandsmallestbodysizeshave
the lowestfitness(greenshading),
and
in the generation
afterselection,
the
variance
ofthe population(but not the
&
STABILIZING
SELECTION
t
ry
favoringindividuals
at eitherend of
After
the distribution.
Here,if selectionis
selection
strongenough,populations
maybegin
to divergein phenotype(i.e.,they may
becomedimorphic).
198
DISRUPTIVE
SELECTION
ili{r
Before
selection
mean)shouldbe smallerthan it was
generation.
in the preceding
Disruptive selection(right)selectsagainst
the populationmean(purpleshading),
,NW
c H A p r E Rs E V E NB E y o N DA L L E L E se: u a N T r r a r r v E G E N E T T casN D T H E E v o L U T I o No F p H E N o r v p E s
\
-
Figure7,7 In 1896,researchers
in
l l l i n o i sb e g a na c e n t u r y - l o negx p e r i -
High oil content
Low oil content
mentin directional
selection.
Out of a
standof severalthousandcornplants,
,I63
they selected earsand measured
their oil content.Theyselected
the 24
earswith the highestoil contentto
createone lineof corn,andthe 24 ears
with the lowestoil contentto create
anotherline.Eachyear,they selected
the highestoil producers
from the high
C
c)
E
o
u "l )_
o
Ol
!tu
CJ
Y
o
L
population
Original
rangein oil contentin thestarting
40
50
60
Generation
I
.*--
strain,andthe lowestfrom the low As
you canseein this graph,the average
o i l c o n t e n itn e a c hl i n eo f c o r nh a s
changedsteadily.
Today,
the oil content
of eachlineis far differentfrom that
in the originalplants.(Adaptedfrom
Moose,Dudley,and Rocheford
2004.)
-
H i g hl i n e
Low line
L-
Scutellar
bristles
--.r*
I..r-
rt--
r-_
ld*II
+
12
10
_
---J
Figure7.8 ThodayandGibson(1961)
produceddisruptiveselectionin a
populationof flies.Theyallowedonly
r-
t-.
15
20
the flieswith highor low numbersof
bristleson their thoraxto reproduce.
In 12generations,
the distributionof
25
Numberof bristles
30
35
bristlenumberschangedfrom a normal
distributionto two isolatedpeaks.
( A d a p t e fdr o m K l u ga n dC u m m i n g s
1997.)
7 . 2 T H EE V o L U T T o N A R vE s p o N s rEo s E L E c l o N
199
I
Selectiondifferential (S):A measure
ofthe strengthof phenotypic
selection.
Theselectiondifferential
describes
the differencebetweenthe meanof
a l l m e m b e ros f a p o p u l a t i oann dt h e
meanof the individuals
that reproduce,
contributing
offspringto the next
generation.
be lower. We might discoverthat the fishesin the lake fare best if they're closeto the
population mean, while big and small fisheshave fewer offspring. This is known as
stabilizing selectionbecauseit tends to keep the population from moving away from
a narrow range of valuesfor the trait. In still other cases,the individuals with a trait
value close to the mean might fare less well than individuals at the ends of the distribution; very big and very small fish do better than medium-sizedfish. In this case,
the fishesexperiencedisruptive selection.(We will examine empirical examplesof all
three forms of selectionin detail in the next chapter.)
It's important to bear in mind that selectionof the sort shown in Figure 7.6 is
not synonymouswith evolution. Evolution is a changein allelefrequenciesin a population. Selectioncan potentially lead to evolution if the difference in reproductive
successis tied to geneticvariation. How quickly the population evolvesin response
to selectiondependson the amount of variation there is in a phenotypic trait in the
population, and how much of the variation in that trait is inherited (ft2).
To calculatethe evolutionary responseto selection,quantitative geneticistsmust
measurethe selectionon a phenotypic trait. We saw in the last chapter how population geneticistsmeasurethe strength of selectionas the selectioncoefficient:the
amount, s, by which the fitness of a genotypeis reducedrelative to the most-fit genotype in the population (Box 6.4). Quantitative geneticistsuse a different method.
They measureselectionfor a trait as the differencein the trait mean of reproducing
individuals and the mean of the general population (the selection differential, S;
Figure7.9). Directional selectionoccurs whenever the mean phenotype of breeding
individuals (Xr) difiers from the mean phenotype of all the individuals in the parents'generation(&). If the differenceis large,selectionis strong. Let'ssay that in the
lake we're studying, fish with big body sizesare much more successfulthan smaller
ones at reproducing when conditions are harsh. But under mild conditions, smaller
fish also survive and reproduce.Figure 7.9 shows a graph of their body sizes.Under
-t4
ro
Onlythe biggest
individuals
reproduce
J
.>
.g
i._-s--1.-N/ean sizeof
reproducing
(Xr)
individuals
cJ
_o
E
f
z
Bodysize
Weakselection
sizeof reproducing
(Xu)
individuals
B i ga n dm e d i u m
individuals
reproduce
F" --5
Figure 7.9 Thegraphon the left showsthe rangeof bodysizesin a
population.
hypothetical
Topright:lfonly the verybiggestindividuals
reproduce,the populationexperiences
strongselectionfor largebody
size.Themeansizeof the reproducing
individuals
is muchbiggerthan
2OO
= strength of selection(difference
betweenmean sizeof entirepopulationand
mean sizeof reproducingindividuals,
Xr-Xr)
the meanof the entirepopulation.
Bottomright:lf big and medium
individuals
reproduce,
selectionis lessstrong,andthe meansizeof
the reproducing
individuals
is muchcloserto the meansizeof the
entirepopulation.
c H A p r E Rs E V E NB E y o N D a L L E L E s :e u a N T r r a r r v E G E N E T T c a
sND THEEvoLUTroN oF pHENorypEs
Offspring
h 2= 0
_o .Y
c>
z.\
np
! ;
z.l
I
:i
1;
c
ii
a
-- "'.'."'" -a
*
{* Wi:;"
0<h2>1
'5
r
:(o
:11
c.Y
c>
n
z.l
{
s
! =
ii
r!
,ii
'I
ll
l:
ff=n'X)
il
it;
3
i:i
ri1i. nr.r.r*-$L
L =
_o.=
c>
L =
z.\
i-R = s*i
Figure7.lO A population's
response
to selection(R)dependsin part
on the heritabilityofthe trait beingselected.
Left:Largeindividuals
in a hypothetical
population
areselected.
Topright:In this populaiion, bodysizeis not heritable.
In otherwords,the sizeof parentsis
not correlated
with the sizeof theiroffspring.
Despiteexperiencing
strongselectionfor bodysize,the population's
meansizedoesnot
changein the nextgeneration.
Theresponse
is zero.Middleright:At
intermediate
levelsof heritability,
the ofspringwill be intermediate
in
sizebetweenthe meansizeof the parentalpopulationasa wholeand
the meansizeofthe selectedindividuals.
Theresponse
to selection
is equalto the strengthof selectiontimesthe heritabilityof the trait
(R : h2 X ,l). Lowerright:lf bodysizeis completelyheritable,
the
response
is equalto selection.
lrarshconditions,selectionfor large bodiesis strong (Xu >> Xp). In milder condit i o n s ,s e l e c t i o ni s w e a k e r( X s > X c l .
Selectionis present in both of these examplesbecausea nonrandom subsetof
fishesis producing more offspring than average.But will that selectionlead to evolution? That dependson how much of the phenotypic variation in body size is attribLrtableto additive genetic differencesamong the individuals-that is, on the narrow
. e n s eh e r i t a b i l i t yo l t h e t r a i t ( f t 2 ) .
If differencesin the body size of fish depend solely on the environment-the
temperatureof the water,for example,or how much food a fish larva finds-then ft2
,.villbe zero.The offspring body sizesin this population will not resemblethe sizes
,rf their parents.The next generationof fish will grow into adults that have the same
rlistribution of body sizesthat the population had before. The population will not
..r'olvedespitethe presenceof selection.
At the other extreme,when /r2 : 1, all of the phenotypicvariation is due to allelic
lifferencesamong the individuals. In this caseoffspring sizesexactly track the sizes
R E S P O N ST
EO S E L E C T I O N
7.2 THE EVOLUTIONARY
201
I
i,l|@Yhv|:.19',."n*ofanoffspring-ParentRegression
E q u at lo t h e N a r r o wS e n s H
e e r i t a b i l i thy',7
Narrowsenseheritability(1.r'z)
is the proportionof phenotypicvariance that is transmittedfrom parentsio offspring(Box 7.2).For
this reason,it's the variancethat causesa populationto evolvein
reqnonqe+n sele.tinn One wav lo measlre r2 rs with a so-called
(Falconerand Mackay1996).Scientists
otfspring-parent
regression
measurethe phenotypicresemblance
of a trait betweenparentsand
theiroffspringin a numberof differentfamilies.
Theythen regressthe
meantrait valueof offspringagainstthe meantrait valueof the parents.(The parentmean is oftencalledthe midparentvaluebecause
thereareonlytwo parents.)
When these valuesare plottedfor many differentfamilies,the
relationshipis an indicationof the extent to which offspringtrait
valuesresemblethoseof their parents.lf there is a significantposi(i.e.,the slopeis greaterthan 0), then parentswith
tive relationship
unusuallylargetrait valuestend to produceoffspringwho alsohave
unusuallylargetrait values(and viceversafor parentswith smaller
trait values),The top two graphsrn Box FrgureZ3.i show two such
relationships.
Let'ssaythat we'reexaminingthe body sizeof two speciesof fish.
In each of the graphs,the parent values are plotted along the
x-axis,and offspringtrait valuesare plotted on the y-axis.(Both
plots are drawn so that the x- and y-axesintersectat the mean
phenotyplcvalueof each population-theorigin of the plot is the
mean of both offspringand parentaltrait values.)As you can see,
both graphs have a positiveslope.but the left-handgraph displays a steeperslope than the right-handgraph (a: 0.8 and 0.2,
respectively).
ln other words,the olfspringin the left-handgraph
havea strongerresemblance
to their parentsthan the otfspringin
the right-handgraph(at leastwhenit comesto bodysize),
Let'snow considerhow the phenotypictrait changesfrom one
generation
to the next.In the absenceof selectionor anothermechanism of evolution,a populationshouldnot evolve.Offspringphenotypes shouldbe similarto parentalphenotypes,even if the trait in
questionis heritable.(This is the phenotypicmanifestationof the
Hardy-Weinberg
theoremwe sawin Chapter6).
Box Figure7.3.1 Thetop two graphsshowparent-offspring
regressionsfor two populations.
Purplecirclesindicateindividuals
that
reproduced.
Thedifference
betweenthe average
valueofthe trait
in the entirepopulationandamongthe reproducing
individuals
is
the strengthof selection(5).Theresponse
to selection(R)depends
on the narrowsenseheritability
hereby
ofthe trait,represented
the slopeof parent-offspring
regression.
The lowerfiguresshowthe
distributionofthe trait in the originalpopulationand in the offspring
ofthe selectedparents.In the left-handexample,
the evolutionary
response
is largebecause
narrowsenseheritabilityis high.
X selected
X selected
[--s-i
Offspring
2O2
c H A p r E Rs E V E NB E y o N Da L L E L E s e: u a N T r r a r l v E G E N E T I c A
s N D T H E E v o L U T r o No F p H E N o r y p E s
Parents
Offspring
But considerwhat happensif we apply selectionto this population.We'vealreadyseenhow selectioncan be a powerfulmechanism
from one genof evolutionbecauseit can changeallelefrequencies
erationto the next(Box6.5).Becauseadditiveeffectsof allelescause
relativesto resembleeachother in their phenotypes(i.e.,becauseof
/,2),selectionalsocan be a powerfulmechanismof phenotypicevolution. lt can causethe distributionof phenotypesto changefrom one
generation
to the next.
Let'ssay that selectionfavorsbig body size in both speciesof
f ishesin the two graphsshownhere.We'llrepresentthis selectionby
usingpurplecirclesto representindividuals
that wereableto reproduce.Theseparentsalonecontributeoffspringto the next generation
of the population.
This situatronresultsin positivedirectionalselection on the phenotypictrait becausethe meantrait valuein selected
parentsis greaterthan the startingmeanof the parentalpopulation.
(s).
Thedifferencebetweenthesemeansis the selectiondifferential
To predict how much the offspringgenerationwill evolve in
responseto this selection,we use the offspring-parent
regression.
To do this, followthe mean valueof selectedparentson the x-axis
up until it intersectswith the regressionline (verticaldashedline in
eachplot).Fromthis point,readacrossto the corresponding
valueon
the offspring(y) axis(horizontaldashedlines).This is the new mean
traitvalueexpectedfor the offspring.lf this newvaluediffersfrom the
meanof the populationbeforeselection-inthiscase,if the newmean
lresabovethe origin-then the offspringdistributionwill haveshifted
towardlargertrait sizes.The populationwill haveevolvedin response
to selection.(The differencebetweenthe new mean of offspringand
the startingmean is a measureof the populationresponseto selection,R.)
When the slope of the offspring-parent
regressionis steep,the
offspringphenotypedistributionwillexperience
a big shift.Whenthe
slopeof the regression
is shallow,the offspringphenotypeswill shift
less.The slopeof the regression,
then,determineshow much a given
population
willevolvein responseto selection.
As we knowalready,
the
componentof variancethat causesa populationto evolvein response
(ft'z).
to selectionis,by definition,
the narrowsenseheritability
So the
slopeof the offspring-parentregressionmust equalft2.
We can reachthis same conclusionby lookingat the regression
equationitself.A linearregressionwill take the form y : a \ x -r b,
wherethe slopeof the relationship,
a, is equalto the changein trait
valuealongthe y-axis,Ay, dividedby the changein trait valuealong
the x-axis,AX:
a:
L Y fL x
In an offspring-parentregression,AI/ : R, and AX = S, so:
a : L Y /A X = R / S
and we know from the breeder'sequation(see Sectron7.2) IhaI
R = h2 x,5, and thereforeIhat h2 : R I S. So the slopeof the regression,a, equalsthe ftz.
of their parents.In such a case,spatialheterogeneityin water temperatureor the supply of food for fry does not matter. Selectionon body size translatesinto an increase
in the averagesize of fish in the next generation.In this case,the new mean body
size of the next generationof fish will be the same as the mean size of the selected
parents.The evolutionary responseto selectionwould equal the strength of selection
imposed.
We can now see that the evolutionary responseof a population to selection
dependsboth on the strength of selectionon a trait and the heritability of that trait.
In fact, we can calculatethe evolutionary response(R) with a remarkably simple
equation,known as the breeder'sequation:
R:lz2xS
The two terms on the right side of the equation reflect the ingredients Darwin
first recognizedas necessaryfor evolution in responseto selection(Chapter2): phenotypic variation that influencesfitness (S),and the ability to transmit those phenotypic characteristicsto offspring (h2).fi selectionis strong, a population can respond
even if a trait is only weakly heritable. And even weak selection can lead to significant
evolutionary change,if a trait's heritability is high. But the most rapid evolutionary
responsesoccur when both selectionand heritability are large.
KeyConcepts
Selection
andevolution
arenofthesamething.Populations
canexperience
selection
evenifthey
cannotevolvein resoonse
to it.
Thespeedof evolutionis a productof the strengthof selection(S)andthe extentto whichoffspring
resembletheir parentsfor that trait (the heritabilityofthe trait, i2).
Eo s E L E c l o l
2 . 2 T H EE V o L U T T o N A R vE s p o N s T
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