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Transcript
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 2O3