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Home , Fitness (biology), Selection coefficient

,, and Selection

Selectionoperates directly on phenotypesbecause phenotypic In manycases, the allelicvariation at a particularlocus does not 'h variationamong organisms rnf luences the relativeprobability of sur- Intluencethe pnenotype. In such cases, the alleres are dden"frorn vivaland reproduction.Those phenotypes, tn turn, are influenced by the actionof seleciionbecause they are selectrvely neutral. Even if an .Although the relationshipbetween alleles and phenotypesis alleledoes result in a phenotypicchange, it stillcould be selectively rarelyknown and often complex, it isstill possible for allelesat genetic neutralif the changein phenotypehas no effecton reproductive locito experrenceselectron. Population geneticists can sample indi- SUCCCSS, vrdualsfor theirgenotype at a locusand comparethe fitnessof indi- vidualswith onegenotype (r.e., the averagefrtness of the ) Key Concept with the fitnessesof individualswith othergenotypes. When geno- Allelesare selectively neutral if they haveno effecton the fitnessof typesdiffer consistently in theirf itness,the genetic locus can be said theirbearers. This phenomenon often occurs when to beunder selection. The (s) isused to describe at a locusdoes not affect the phenotypeof an individual howmuch the genotypesdiffer in theirfitness.

6.6 Selection:Winning and Losing In Chapter 2, we introduced the concept of selectionas first developedby and Alfred RusselWallace. Both naturalistsrecognized the profound impor- tance of selectionas a mechanism of . ariseswhenever (1)individuals vary 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 Chapter10, we will considerthe origin of adaptationsin more detail. For now, let's focus on the question of how selectionchanges the frequencies of allelesin a population. The reproductivesuccess of an individual with a particular is known :The success of anorganism as fitness, and selectionoccurs when individuals vary in their fitness. While this at survivingand reproducing, and thus may seemstraightforward enough,studying the actual fitness of real organismsis a contributingoffspring to future surprisingly complicatedmatter. The best way to measurefitness would begin with generations. tallying the lifetime reproductivecontribution of an individual and then noting how many of the offspring manageto survive to reproductiveage themselves. In practice, however,it's hardly ever possibleto make such a detailedmeasurement. Scientistssettle instead for reliableproxies 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 specificseason. Whatever the actualmetric, measuringselection entails comparing thesefitness mea- suresfor 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 rela- tionship betweengenotype and phenotype.The fitnessof an organism is the product of its entire phenotype.We'll seein Chapters7 and 8 how scientistscan make mea- surementsof phenotypic selectionto study how complex morphological and behav- ioral 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. Populationgeneticists often distill all of the different fitness components,such Relativefitness (of a genotype): as survival, mating success,and fecundity, into a single value, called w. This value Thesuccess ofthe genotypeat describesthe relative contribution of individuals with one genotype,compared with producingnew individuals (its fitness) the averagecontribution of all individuals in the population. If individuals with a standardizedby the successof other particular genotype,for example,4747, consistentlycontribute more offspring than genotypesin the population(for individuals with other genotypes(e.g., A1A2, A2A2), then their relative fitness will be example,divided by the average greaterthan one. Conversely,if the net contributions of individuals with a genotype fitnessof the population). are lower than those of other individuals, the relative fitness will be less than one.

166 cHAprERsrx rHE wAys oF cHANGE:DRrFT AND sELEcrroN Sometimespopulation geneticistscalculate relative 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 rela- tive fitnessesthat are between0 and 1.Regardless of 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 , rather than a genotype,to fitness. But calculatingthe relative fitness of an allele is more complicatedthan calculatingthat of a genotype,for two reasons.First, alleles in 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 actson individuals and their phenotypes. Nevertheless,it is still possibleto calculatethe net contributions of an alleleto fit- ness.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 Averageexcess of fitness (of an the next generation.Box 6.5 showshow the net fitnesscontribution of an allele,called allele):The difference between the the averageexcess of fitness, is calculated. averagefitness of individualsbearing The averageexcess of fitness for an allele can be used to predict how the fre- the alleleand the averagefitness of the quency of the allelewill changefrom one generationto the next: oooulationas a whole.

Lp:px(ao, w)

where Ap is the change in 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 averageexcess of fitness(a o ) , for example,determines whether selectionincreases an allele'sfrequency or decreasesit. Whenever an allele is pres- ent in a population, its frequency is greaterthan zero; and as long as the population exists,its averagefitness, w, is alsogreater than zero (becausew is the sum of all indi- viduals with each genotype times their respectivecontributions of offspring to the next generation).Since both p and w are by definition positive,the sign of Ap must be determined by the averageexcess of fitness of the allele. Whenever the fitness effectsof an allele are positive,selection should increasethe frequency of the allele over time; the converseis true when the fitnesseffects are negative. This equation also tells us that the speedof increase(or decrease)in the fre- quency of an allelewill depend on the strength of selectionthat it experiences-the magnitude of aa,.When the averageexcess of fitness is very large (positiveor nega- tive), the resulting changein allele frequencywill be greaterthan 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 alleleis 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 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.

'167 6.6 sELEcroN:wrNNtNG AND LosrNG E SelectionChanges Allele Frequencies ll Let'sconsider how naturalselection changes allele frequencies by Genotype: A,A, AtAz A,A, startingwith a populationin Hardy-Weinbergequilibrium at a genetic (p'zxwrr)fw (zpqxwt)fw \q'xwrr)/w locus.We willthen calculate how selection pulls ihe populationout of f,rtt equilibriumand, in so doing,shifts the frequenciesof the alleles. Andfrom theseresults, we cancalculate each a//e/e frequency in this We'lluse the samelocus and alleles that we did in Box6.2, A, and newgeneration as the frequencyof homozygoteindividuals plus half Ar, and starting frequenciesof p and 4 respectively.We've already the frequencyof heterozygotes: seenthat for a populationin Hardy-Weinbergequilibrium, the fre- p,tr = x w'r) il + x n',) *) quenciesof eachpossible genotype are l(p2 f l(pq I :(p'xwttlpexw,r)fw f(A,A') = P' and : 2pq f(A1A') q,*t: l(q2x wrr)f wl + l(pq x *rr) /fi) f(A,A'1 : nz :(qrxwzzrpexwp)fw genetic genotypes Selectionacts on a locuswhenever the of that Naturalselection is a mechanismof evolutionbecause it can we can assignfit- locusdiffer in their relativefitness. In this case, causeallele frequencies to changefrom generationto generation. genotype nessesto each aswn,wn,andw22,respectively. Fitness can Nowthat we haveapplied selection (as differentialfitnesses) to our act throughmany components,such as survivorshipto the age of genotypes,let them reproduce,and calculatedthe new allelefre- reproduction,mating success, and fecundity, but ultimatelythese all quenciesin the offspringgeneration, the questionis, how havethe genotype translateinto the successof each at contributingoffspring allelefrequencies changed? generation. measuresencom- to the next Here,we'll let our fitness Tocalculate the changein frequencyof theA, allele,Ap, we sub- pass proportional allof these,so that w,,, w,r, and w, denotethe con- tractthe startingfrequency, p, fromthe newfrequerte\, p.ay. tributionsof offspringby individualswith A,A,, AtA2, and A2A2 geno' LP=Pt+1-P hrnoc roqnontirrolrr rJPvr' reeyvvLtvv'J. Tocalculatethe genotype frequencies afterselection (timet + 1), The startingfrequency p = pz+ p4.To expressthis overthe we needto multiplythe frequencyof eachgenotype by its relative denominator,w,we multiply it byI rnthe form of w f w,sothat fitness,In essence,this simulatesa parentalpopulation that repro- p = (p' x w + pq x w)/ w.Ihereforc. duces to generatean ofispringgeneration with zygotegenotype frequenciesoI p2,Zpq,and q2 (these are the allelefrequencies in the LP=P,+I_P populationimmediately before selection). These offspring then expe- : l(p' x wtr 4 pQx wp)f w)- [(pt x w + pq x w) / w) rienceselection as they developinto reproductivelymature adults - = (p'x wt * p4 x w.rz-p'xi pq xi) li themselves,who then mate to produceyet anothergeneration of = p x (p X w,, I X wn - p X w - q x w) w progeny.The relativesuccess of individualswith eachgenotype at Q I : - survivingthrough to adulthood,competing successfully for mates, b l.) x (p x w,1 p x w + q x we- S xu) - - andproducing viable offspring is reflectedin theirrespective relative = (p/O) x [p x (w,, ,)] + lq x (w,, w)) fitnessvalues-selection is actingon this geneticlocus, Because of The term x (r,, - t)] + x (r', - t)l is known as the selection,some genotypes will increase in frequencyat the expense [p lq averageexcess of fitnessfor the A, allele.lt is the mean difference of othersin the nextgeneration. betweenthe fitnessof individualshaving the A, alleleand the fitness So,at time (r + l), the relativeabundance of eachgenotype fre- of the populationas a whole.In essence, the average excess of fitness quencywill be representedby the following. isa wayto assignfitness values to a//e/es,even though alleles have no Genotype: A'A, AtAz AzAz phenotypesof theirown-they havephenotypes only when they are

Numbers: p2 \ wt 2pq X wp q2 x wzz Box Figure6.5.1 Theaverage excess offitness oftheA, allele(a1,) iscalculated from the frequency of A1alleles in homozygotesand But the numberof individualswith eachof thesegenotypes in this newgeneration will not be the sameas in the previousgeneration. heterozygotes,each adjusted by their differencesin fitnessfrom the Individualsmay haveproduced multiple offspring, or individualswith meanofthe population. particulargenotypes for example.To may havedied before breeding, Proportionof A, alleles Proportionof A' alleles convertthese numbers into newfrequencies for eachgenotype, we that arepresent in A,A, that arepresent in ArA, needto siandardizethem by the total numberof individualsin the homozygousindividuals heterozygousindividuals newgeneration. This new total is just the sum of the numbersof indi- vidualshaving each possible genotype: -w)l w = pt X w111- 2pq X wp * q2 X wzz + ex(wp-w)l

w is alsocalled the averagef itnessof the populationsince it's the sum of the fitnessesof eachgenotype multiplied by (i.e.,weighted by) Differencein fitness Differencein fitness the frequenciesat whichthey occur. Using the averagefitness of the betweenA,A, individuals betweenA,A, individuals populaiion,we nowturn the relativeabundances after selection can and the meanfitness of andthe meanfitness of intofrequencies. the population the population

168 cHAprERstx rHE wAys oF cHANGE:DRIFT aND sELEcrloN combinedin pairsto form genotypes.Thus, although it is individu- 0, whetherAp is positiveor not dependsentirely on the signof ar,, alswith genotypes who experienceselection and who differin their Thismeans that whetherthe alleleincreases in frequencyfrom gen- relativecontributions to subsequentgenerations, we can stillassign erationto generation,or decreases,depends on whetherits aver- relativefitnesses to a//e/esin the form of theiraverage excess of fit- ageexcess of fitnessis positiveor negative.When the net effectof ness.This approach allows us to seeclearly the relationshipbetween an alleleis an increasein f itness(average excess in fitnessis greater allelesand f itness. than 0), meaningthat the alleleexperiences positive selection, the We can now expressthe changein allelefrequencies resulting alleleis predictedto increasein f requency.Conversely, when the net from selectionas effectof an alleleis a decreasein fitness(average excess in fitnessis A,p:(pfw)xao, lessthan 0), meaningthat the alleleexperiences negative selection, Ap: p x ("o,/A) the alleleis predrctedto decreasein frequency. Second,the averageexcess of fitnessdepends not only on the whereao, is the averageexcess of fitnessof theA, allele.We canalso fitnessesbut a/soon the frequenclesof eachallele. This means that calcuiatethe averageexcess of fitness for the,42 alleleas the effectof selectionacting on an allelewill depend on the popula- tion contextin whichit is found. an,: lp x (wn - .)l + lq x (wr,- w)l Forexample, two populationswith identicalfitnesses for eachgenotype could have very different aver- predicted and the changein frequencyof the 42 alleleas a resultof ageexcesses of fitnessif theyhave different allele frequencies before selectionas selection.Selection may causerapid changes in allelefrequency in (q Aq: f w) x ao, one population,but onlyminor changes in the other.When an allele Lq:qx("or/r) rsvery rare (as it wouldbe if it hadrecently arisen through mutation) selectionmay be much lesseffective at changingits frequency than Severalimportant conclusions should be evidentfrom these cal- it wouldbe if the allelewere more common. culations.First, because p andw arealways greater than 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.Because of this acceleratinggrowth, even a small changein the interest rate can have a big effectover 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 averageexcess for 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 popu- lations, by contrast, has a weaker effect. Figure6.12 shows a computer simulation that illustratesthis effect,in which an allelewith a selectiveadvantage of 5 percent is added to populations of different sizes.In the big population of 10,000

Figure6.12 Naturalselection is ineffectivein smallpopulations and frequencyof 0.1(10 percent), and subsequent changes in itsfrequency effectivein largeones. These graphs show the resultsof computer resultfrom the combinedaction of selectionand drift. In the smallest simulationsof a populationin whichan allele that raisesfitness by populations,the alleledisappears from halfthe simulations,even 5 percentis added to populationsofdifferent sizes (each colored line thoughit hasbeneficial effects on fitness.But in largepopulations, the representsa different simulation). In allcases, the allelestarts at a allelebecomes more common in allof them.(Adapted from Bell2OO8.)

10individuals 1OOindividuals 1000individuals 10,000individuals 100o/o o i3.D >.8 50%

ri cJ _o 0o/o 80 120 80 120 0 20 40 60 80 120 80 120 Generation

6.5 sELEcTtoN:wtNNlNG AND 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 strongerthan those of selectionwhen populations are very small.

Patternsof Selectionin Timeand Space 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 : they often have more than one effect on an organism.These mul- tiple effectsare the result of the interconnectednessof biology. A single regulatory ,for example,can influence the expressionof many other .This phenom- :The condition when a enon is known as pleiotropy. mutationin a singlegene affects the The evolution of resistancein mosquitoeson the coastof Francedemonstrates expressionof manydiferent pheno- how pleiotropy can affect the nature of selection.When the Esterl allele emerged typic traits.Pleiotropy is consideredto in the early 1970s,it provided mosquitoeswith resistanceto insecticides.But it had beantagonistic if a mutationwith ben- other effectson the mosquitoesas well. Researchersat the University of Montpellier eficialeffects for one trait alsocauses have found that the Esferr mosquitoes have a higher probability of being caught by detrimentaleffects on other traits. spidersand other predatorsthan insecticide-susceptiblemosquitoes do, for example (Berticatet al. 2004).A mutation that has improved fitness in one context-by pro- viding resistanceto insecticides-has alsoaltered the 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 effectson the organismin question.Even if an allelehas somebeneficial effects, it may,on balance, lower reproductive successoverall. How the balance tips depends on the environ- ment in which an organismlives. For mosquitoeson the Frenchcoast, any protection againstinsecticides can dramaticallyraise fitness because susceptible mosquitoes are 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 resistancebecause there's no insecticideto resist.Instead, the allele lowers fit- nessby making the insectseasier prey. The curvesin Figure5.2 are the result of this shift in balance.Selection raised the frequency of Estertalong the coastwhile keep- ing it low inland. This differencewas maintained even as mosquitoeswere migrat- ing 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 /esspro- tection againstinsecticides than the older allele.A clue to its successcomes from the slope of its curve. Esferadoes not drop off steeply as you go inland. It's likely that Esferadoes not impose the high cost of Esferr.Selection favors the alleleon the coast, but mosquitoes don't pay a price for carrying it if they migrate inland (Raymond et al.1998).

Fifty ThousandGenerations of Selection: ExperimentalEvolution Some of the most important insights into how selectionaffects alleles have come from experimentsthat scientistsset up in their laboratories.They can carefully con- trol the conditions in which organisms grow and reproduce, and they can analyze the entire population under study.

17O cHAprERstx rHE wAys oF cHANGE:DRrFT AND sELEcrtoN 100% 100o/o Figure 6.13 Thisseries of graphs extendsthe historyof resistancealleles o 80% 80o/o _OJ in mosquitoesthat we encounteredin o 60o/o 60"/o Figure6.2. After spreadingwidely in U the 1970s,the Ester'allelegradually c (U 40% 40% f becamerarer in the 1980sand 199Os OJ 20o/o 20o/o while anotherallele, known as Estera, L becamewidespread. The shift may 0 0 reflecta physiologicalcost imposed 111213141 111213141 on the insectsby Esterl.Estera alleles Kilometersfrom the coast Kilometersfrom the coast mayconfer resistance on mosquitoes without this cost,making its relative 10Qo/o 100o/o fitnesshigher and driving it to higher t 80% 80Yo frequencies.(Adapted from Raymond o et al.1998.) ts aio/- o wv/u 60o/o fi 40o/o 40o/o f 9. 20o/" 20o/o u

0 0 Negativeselection: Selection that de- 111213141 111213141 creasesthe frequencyof alleleswithin Kilometersfrom the coast Kilometersfrom the coast a population.Negative selection occurs wheneverthe averageexcess for fit- One of the longestrunning of theseexperiments is taking placeat Michigan State nessof an alleleis lessthan zero. University (Barrick et al. 2009).Richard Lenski startedit in 1988with a single,E coli Positiveselection: Selectionthat in- bacterium. He allowed the microbe to produce a small group of geneticallyidentical creasesthe frequency of alleleswithin descendants.From these clones,he started 12 genetically identical populations of a population.Positive selection occurs bacteria(Figure 6.14). Each population lives in a flask containing 10 milliliters (ml) of wheneverthe averageexcess for fit- a solution. The bacteriagrow on glucose,but Lenski supplied only a limited concen- nessof anallele is greater than zero. tration. 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 12populations, keeping each population separatefrom the oth- Figure6.14 RichardLenski and his ers.The bacteriagrow until the glucoseis depletedand then sit there until the same colleagueshave bred bacteria for over processis repeatedthe next day.In a singleday, the bacteriadivide about seventimes. 20 yearsusing this method. AII of the bacteria descendedfrom a single ancestralgenotype. As they repro- duced, they occasionallyacquired new mutations. Alleles that lowered their repro- ductive successexperienced negative selection.Any allelesthat spedup their growth # rate positive selection. The random or boosted their survival experienced sample OneEscherichia coli Lenski took eachday from eachflask reflectedthese shifting frequenciesof alleles. Every 500 generations,Lenski stored some of the bacteria from each of the 12 $ RNRRRRRRRRRR lines in a freezer.Freezing did not kill them, so the samplesbecame a frozen fossil se$€'eM$ssaereD€.€9 record that could be resurrected at a later time. Thawing them out later, Lenski could 12genetically identical lines (flasks) directly observehow quickly the ancestraland descendantbacteria grew under the ! I sameconditions. He could thus directly measuretheir changein averagefitness. f The experiment has now progressedfor 50,000 generations.(It would have Morning:each flask gets new taken about a million yearsif Lenski were using humans as experimentalorganisms supplyof glucose. <-.1 instead of bacteria.)Figure 6.15 shows the evolution of Lenski'sE. coli over the first +tr! 20,000generations. The bacteriabecame more fit in the new environment than their Afternoon:glucose runs out. ancestorshad been in all 12 lines.The averagecompetitive fitnessof the populations I increasedby approximately75 percent relativeto the ancestor.In other words, all 12 &l'T of the bacterial populations evolved in responseto natural selection:they had accu- Nextday: small samPle of re# mulated mutations that made them more efficient at growing under the conditions surviviorsfrom all 12lines that Lenski set up (Barricket al. 2009). transferredto newflasks. Preservinga frozen fossil record doesn't just allow Lenski to compete ancestors .& against descendants.It also allows him and his colleaguesto compare their DNA. Sampleof eachline Becausethe experiment began with a single microbe, and becausethe microbe's frozen for later study descendantsreproduced asexually without horizontal gene transfer,the researchers every500 generations.

6.6 sELEcloN:wrNNrNG AND LosrNG 171 2.0 o -c 1.8 qJo .=P PO 1.6

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'10,000 5000 15,000 20,000 Time(generations)

Figure6.15 Thebacteria in Lenski's present in descendantsbut not in the original ancestor experimenthave experienced natural can be confident that alleles mutation during the experiment itself. selection.New mutations have caused must have arisenthrough havebeen investigating these new mutations,observ the descendantsto reproducefaster Lenskiand his colleagues fitness of the bacteria. In one experiment, they selecteda underthe conditions of theexperiment ing how they affect the 10,000to analyze(Stanek, Cooper, and Lenski2009). thantheir ancestors did. (Adapted from singlemicrobe from generation segmentsof its DNA into ancestralbacteria from Cooperand Lenski 2000.) They transferred1296 different the sameline. Then they mixed eachkind of engineeredbacteria with unmanipu lated ancestralones and allowed them to grow side by side. These trials revealed one evolvedsegment in particularthat increasedthe fitnessof the bacteria.Further analysisallowed Lenski and his colleaguesto pinpoint the mutation within the seg ment that was responsible.A singlenucleotide was mutatedin a protein-bindingsite, calledBoxGl, which regulatesa pair of nearbygenes. These genes encode proteins calledGlmS and GlmU,which help synthesizethe bacterialcell wall. To confirm that the mutationwas indeedresponsible for increasingbacterial fitness, they insertedthe singlenucleotide into BoxGlin the ancestralbacteria. That tiny insertionraised the relativefitness of the bacteriaby 5 percent. Having identifiedthis mutation and measuredits fitness,Lenski and his col leaguesthen setout to traceits origin.At somepoint during the evolutionof that par ticular line of E. coli,they hypothesized,the mutation must haveemerged and therl increasedin frequency.They turnedto the line'sfrozen fossil record, selected bacteria from each5O0-generation sample, and examinedthem for the presenceof the BoxGl mutation.None of the bacteriathey examinedfrom generation500 had the BoxGl mutation.So the mutation must havearisen after that point.The bacteriain genera tion 1000told a differentstory: 45 percentof them carriedthe mutation.And in gen' eration1500, the researchersfound that 97 percentof the bacteriahad it. This rapirl spreadis thekind o[patternyou'd expect from a mutationthat increases fitness. It's not immediatelyobvious how the mutation benefitsthe bacteria,but Lenski and his colleagueshave someclues. In bacteriawith the BoxGlmutation, less GlmS and GlmU is expressed.It's possiblethat the bacteriadivert resourcesfrom buildinc thick cellwalls to other functions,speeding up their reproduction. The BoxGlmutation 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' increasedfitness of previous mutations. Large-scalecomparisons of these mtrt,r tions are revealing lessons about how beneficial mutations interact. Some mrtt.r tions, for example, are beneficial only when they follow certain other mutatiorl' :Occurs when the effectsof That's becausetheir effectson the bacteriainteract in a processknown as epistasi. anallele at onegenetic locus are modi- Only one line of E. coli evolvedthe BoxGl mutation. But other mtrtations aro'' fiedby allelesat oneor moreother loci independently in several different lines, and the scientistsfound three genes th.'' mutatedin all 12 lines.While evolutionmoved in the sameoverall direction in 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.

172 cHAprERslx rHE wAYsoF cHANGE:DRIFT AND sELEcrloN Dominance:Allele versus Allele Bacteriaare useful for running evolution experimentsbecause their haploid are relatively simple. Selectioncan be more complex in diploid organisms,however, due to the interactionsbetween the two copies of each genetic locus.As we saw in Chapter5, an allelecan act independentlyof its partner,or it can be either dominant or recessive.Each of thesestates can 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.People who 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. Suchinteractions between alleles are called additive becausethe effectsof the allelescan be predicted simply by summing the Additiveallele: An allelethat yields copiesthat are present. twice the phenotypiceffect when two Additive allelesare especiallyvulnerable to the action of selection.Whenever copiesare present at a givenlocus than an additive allele is present,it will affect the phenotype,and selectioncan act on it. whenonly a singlecopy is present. Favorablealleles can be carriedall the way to fixation becauseheterozygous individu- Additivealleles are not influencedby als will have higher fitnessthan individuals lacking the allele,and homozygousindi- the presenceof otheralleles (e.g., there viduals will fare even better.Eventually, the population will contain only individuals is no dominance). homozygousfor the allele (Figure6.16). Conversely, deleterious alleles can be swept all the way out of a population. Every time the allele is present,it is exposedto selec- tion, and its bearerssuffer lower fitnessthan other individuals lacking the allele.Here too, the result will be absolute:selection will remove the allele completely from the population.

Figure6.16 Effectsof positiveselection on additive, recessive, and dominant alleles. Each line showspredicted changes inallele frequency given a selectioncoefficient of 0.05. Alleles with additiveeffects on phenotypesare always exposed to selection,so they will increase steadily from themoment they arise due to mutationuntil they are fixed in the population. Recessive alleles are notexposed to selectioninitially, because they are likely to occuronly in heterozygousgenotypes. Theymay linger for thousands ofgenerations until drift either removes them or increasestheir frequency.Eventually, if drift increases their frequency sufficiently, homozygous recessive individu- alswill begin to appearin the population. As soon as this happens, selection will begin to increase thefrequency ofthe allele and swiftly carry it to fixation.Dominant alleles are exposed to selection immediatelyand will increase infrequency rapidly. However, asdominant alleles become increas- inglycommon, the alternative alleles (by definition, recessive) become increasingly rare. As we've justseen, rare recessive alleles are invisible to theaction ofselection because they are carried in a heterozygousstate. Thus selection alone cannot fix a completelydominant allele. (Adapted from Connerand Hartl 2004.)

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=l OU-/o (u E 40yo L

20o/o

0o/o 100 200 300 400 500 600 700 800 900 1000 1100 Numberof generations

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 phenotypewhether one copy is present in a heterozygoteor two copiesare in a homozygote.A recessiveallele, on the other hand, can affect the phe- notype only when it is paired with another recessiveallele-that is, when it occursin a homozygousrecessive individual. This interaction blunts the power of selectionto spreadalleles to 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 recessiveallele will haveno effecton its phenotype.The heterozygousindividual may or may not passdown the new recessiveallele to its offspring; if it does,its offspring will be heterozygotesas well 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 alwayshoused in heterozygousindividuals. Since recessivealleles don't affect the phenotype of heterozygotes,they remain largely hidden from the action of selection,Drift alone determineswhether they per- sist in the population.Eventually, drift may increasea recessiveallele's numbers, such that heterozygotesbecome fairly common. At that stage,the oddsbecome more likely that two heterozygoteswill encounter each other and mate. Only then do homozy- gous recessiveoffspring begin to appearin 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 increasethe fre quency of the allele.As the allele spreads,more and more individuals are born with homozygousrecessive genotypes. Because the dominant alternative allele performs lesswell (its averageexcess for fitness is negative),it declinesin frequency.Because thesenegative effects are present in both heterozygousand homozygousgenotypes, this deleteriousallele has 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 deleteriousrecessive alleles. If drift createsa high frequencyof heterozygotes,they will start to produce homozygotesthat start to suffer lowered fitness.As a result,the allelewill becomeless common. But selection cannot remove the allelecompletely, despite its low fitness.As soon as the recessivt, allele'sfrequency drops low again,it occursonly in a heterozygousstate where it i. hidden once more from selection. Selectionhas 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 effectsare favorable (its averageexcess of 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 carriestl'rt' ancestralallele at that locus. As the dominant allele becomesmore common, ho\\ ever,heterozygous individuals begin to pair with other heterozygousindividuals antr produce homozygousindividuals that carry two copiesof the new dominant allelt- They experiencethe same fitness advantageas heterozygotes,and the frequency r': the allelecontinues to climb. As the frequencyof the new dominant alleleapproaches fixation, 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 prt- ent only in heterozygotes.Since the recessiveallele has 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 cHAprERsrx rHE wAys oF cHANGE:DRIFT AND sELEcrroN very rapidly, it cannot drive the allele all the way to fixation, becauseit cannot elimi nate the ancestralrecessive allele. Thesedynamics help explain why populationsharbor so much geneticvariation, and why so much of this variation is comprisedof rare recessivealleles with deleteri- ous effects.Whenever mutations generatealleles with dominance interactions,the potential arisesfor deleteriousrecessive alleles to hide from selectionin a heterozy- gous state.And as long as they are rare,the deleteriousalleles can persist in popula- tions 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-SelectionBalance Another factor that promotes in populations is the origin of new mutations. At first, this might seem like a weak force, since the rate of new muta- tions 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 genewould 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 bil- lion 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 expec- tancy for Americanswith cystic fibrosis is 35. The diseaseis causedby mutations to the CFI"Rgene, which encodesa chloride channel in epithelial cells.More than 300 different disease-causingalleles of the CFIR gene have alreadybeen identified (Tsui 1992).Cystic fibrosis is considereda simple geneticdisorder, because only a single geneis involved. As we saw in Chapter5, other traits are typically far more complex, influencedby hundreds or thousandsof genes.A mutation to any of thosegenes can potentially have an effect on a complex trait. Mutations are thus an important mechanismof 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,selec- tion will act to reduceits frequency.Meanwhile, however, new mutations at that locus will keep emerging, lifting up the allele'sfrequency. The production of new muta- tions and negativeselection will act like opposingteams in a tug-of-war.Together, this mutation-selectionbalance will result in an equilibrium frequency of the allele (we show how to calculatethis equilibrium in Box 6.6).Mutation-selection balance helps explain why rare deleteriousalleles with recessiveeffects persist in populations,add- ing to geneticvariation (Crow 1986,Templeton 2006).

SelectingDiversity

We ve seen how selection can reduce genetic diversity by driving some alleles to Negativefrequency-dependent fixation and eliminating othersfrom populations.But under certain conditions,selec- selection: Raregenotypes have higher tion actually fosters variation. In some situations,for example,the relative fitness fitnessthan common genotypes. This of a genotypeis high when it is rare, but low when it is common. Selectionin these processcan maintain genetic variation casesis known as negative frequency-dependent selection. Before we explain how withinoooulations.

6.6 sELEcrtoN:wtNNtNG AND LostNG 175 Key Concepts Whenthe componentsof variationact independently,their effectsare additive, so that variation i,llt attributableto genesand variation attributable to the environmentsum to yieldthe total pheno- typicvariance of the sample.This allows biologists to estimatethe relativecontributions of different sourcesofvariation to the phenotypicdistribution observed.

Theheritability of a trait is the proportionof phenotypicvariance that is dueto geneticdifferences amongindividuals.

Broadsense heritability reflects all of the geneticcontributions to a trait'sphenotypic variance includingadditive, dominant, and epistatic gene efects. lt alsoincludes influences of the parent phenotypeon the environmentof offspringthat cancause siblings to resembleeach other (maternal and paternaleffects), such as nest quality or 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 examinethe reproductivesuccess of fish. If there'sa nonrandom differencewith respectto body size,selection exists for that trait. Figure7.6 illustrates someof the forms this selectioncan take.If selectionfavors phenotypes at one end of a distribution of valuesfor a trait, the population may evolvein 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,selection may favor valuesat the middle of the distribution, while the reproductivefitness of organismswith traits at the ends of the distribution may

c o Figure7.6 Selectioncan act in differ- f ent wayson a population.Directional AJ u selection(left) favors individuals at oneend of a trait distribution,such as >-$b ,NW animalswith smallbody size. As illus- Phenotype(e.9., size) trated,large individuals have lower fit- nessthan smaller individuals (negative DIRECTIONAL STABILIZING DISRUPTIVE selectionagainst large sizes is indicated SELECTION SELECTION SELECTION by the red shading).After selection, & ili{r andprovided the trait is heritable, - the distributionof phenotypesshould t \ shiftto the left,toward a smallermean bodysize. Stabilizing selection (middle) favorsindividuals with a trait nearthe populationmean. In thiscase, fish with Before selection the largestand smallest body sizes have the lowestfitness (green shading), and in the generationafter selection, the varianceofthe population(but not the mean)should be smaller than it was in the precedinggeneration. Disrup- ry tive selection(right) selects against the populationmean (purple shading), favoringindividuals at eitherend of After the distribution.Here, if selectionis selection strongenough, populations may begin to divergein phenotype(i.e., they may becomedimorphic).

198 cHAprERsEVEN BEyoND ALLELEs: euaNTrrarrvE GENETTcsaND THEEvoLUTIoN oF pHENorvpEs Figure7,7 In 1896,researchers in - Highoil content lllinoisbegan a century-longexperi- - Low oil content mentin directionalselection. Out of a C standof severalthousand corn plants, c) ,I63 E theyselected earsand measured o "_ u l) theiroil content.They selected the 24

o earswith the highestoil contentto Ol !tu createone line of corn,and the 24 ears CJ with the lowestoil contentto create Y o L anotherline. Each year, they selected Originalrange in oilcontent in thestarting population the highestoil producersfrom the high strain,and the lowestfrom the low As youcan see in thisgraph, the average 40 50 60 oilcontent in eachline of cornhas Generation changedsteadily. Today, the oil content of eachline is far differentfrom that in the originalplants. (Adapted from Moose,Dudley, and Rocheford 2004.)

I Highline .*-- - Lowline

L- Scutellarbristles

--.r*

I..r-

rt-- r-_ ld*-

II + _

Figure7.8 Thodayand Gibson (1961) produceddisruptive selection in a populationof flies.They allowed only - ---J - the flieswith highor low numbersof bristleson theirthorax to reproduce. In 12generations, the distributionof 12 t-. r- bristlenumbers changed from a normal distributionto two isolatedpeaks. 10 15 20 25 30 35 (Adaptedfrom Klug and Cummings Numberof bristles 1997.)

7.2 THEEVoLUTToNARv REspoNsE ro sELEcloN 199 be lower.We might discoverthat the fishesin the lake fare best if they're closeto the I population mean,while big and small fisheshave fewer offspring. This is known as stabilizing selectionbecause it tends to keepthe population from moving away from a narrow range of valuesfor the trait. In still other cases,the individuals with a trait value closeto the mean might fare lesswell than individuals at the ends of the dis- tribution; very big and very small fish do better than medium-sizedfish. In this case, the fishesexperience .(We will examineempirical 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 allelefrequencies in a popu- lation. Selectioncan potentially lead to evolution if the difference in reproductive successis tied to geneticvariation. How quickly the population evolvesin response to selectiondepends on 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 evolutionaryresponse to selection,quantitative geneticistsmust measurethe selectionon a phenotypic trait. We saw in the last chapter how popu- lation geneticistsmeasure the strength of selectionas the selectioncoefficient: the Selectiondifferential (S):A measure amount, s, by which the fitness of a genotypeis reducedrelative to the most-fit gen- ofthe strengthof phenotypicselection. otype in the population (Box 6.4). Quantitative geneticistsuse a different method. Theselection differential describes They measureselection for a trait as the differencein the trait mean of reproducing the differencebetween the meanof individuals and the mean of the general population (the selection differential, S; allmembers of a populationand the Figure7.9). Directional selectionoccurs whenever the mean phenotype of breeding meanof the individualsthat reproduce, individuals (Xr) difiers from the mean phenotype of all the individuals in the par- contributingoffspring to the next ents'generation(&). If the differenceis large,selection is strong.Let's say that in the generation. 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 7.9shows a graph of their body sizes.Under

-t4 ro Onlythe biggest J individualsreproduce .> .g i._-s--1.-N/ean sizeof cJ _o reproducing E individuals(Xr) f z Bodysize Weakselection sizeof reproducing individuals(Xu )

Bigand medium individualsreproduce

F--5 " = strength of selection(difference betweenmean size of entirepopulation and meansize of reproducingindividuals, Xr-Xr)

Figure 7.9 Thegraph on the left showsthe rangeof bodysizes in a the meanof the entirepopulation. Bottom right: lf bigand medium hypotheticalpopulation. Top right: lfonly the verybiggest individuals individualsreproduce, selection is lessstrong, and the meansize of reproduce,the populationexperiences strong selection for largebody the reproducingindividuals is muchcloser to the meansize of the size.The mean size of the reproducingindividuals is muchbigger than entirepopulation.

2OO cHAprERsEVEN BEyoND aLLELEs: euaNTrrarrvE GENETTcsaND THE EvoLUTroN oF pHENorypEs Offspring

h2=0

_o .Y c> z.\

np I !; :i z.l 1; c ii a -- "'.'."'"* -a {* Wi:;" 0

1

'5 r :(o :11 c.Y { c> s != n z.l ii r! ,ii 'I ll l: il ff=n'X) it; 3 i:i ri1i. nr.r.r*-$L

L= _o.= c> L= z.\

i-R = s*i Figure7.lO A population'sresponse to selection(R) depends in part intermediatelevels of heritability,the ofspringwill be intermediatein on the heritabilityofthe trait beingselected. Left: Large individuals sizebetween the meansize of the parentalpopulation as a wholeand in a hypotheticalpopulation are selected. Top right: In this popula- the meansize ofthe selectedindividuals. The response to selection iion,body size is not heritable.In otherwords, the sizeof parentsis isequal to the strengthof selectiontimes the heritabilityof the trait notcorrelated with the sizeof theiroffspring. Despite experiencing (R : h2 X ,l).Lower right: lf bodysize is completely heritable, the strongselection for bodysize, the population'smean size does not responseis equal to selection. changein the nextgeneration. The response is zero. Middle right: At

lrarshconditions, selection for largebodies is strong (Xu >> Xp). In milder condi- tions, selection is weaker(Xs > Xcl. Selectionis present in both of these examplesbecause a nonrandom subsetof fishesis producing more offspring than average.But will that selectionlead to evolu- tion? That dependson how much of the phenotypic variation in body size is attrib- Lrtableto additive genetic differencesamong the individuals-that is, on the narrow .enseheritability ol the trait(ft2). 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'olvedespite the 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

7.2 THE EVOLUTIONARYRESPONSE TO SELECTION 201 I i,l|@Yhv|:.19',."n*ofanoffspring-ParentRegression Equalto theNarrow Sense Heritability, h'7

Narrowsense heritability (1.r'z) is the proportionof phenotypicvari- Let'ssay that we'reexamining the body sizeof two speciesof fish. ance that is transmittedfrom parentsio offspring(Box 7.2).For In each of the graphs,the parent valuesare plotted along the this reason,it's the variancethat causesa populationto evolvein x-axis,and offspringtrait valuesare plottedon the y-axis.(Both reqnonqe+n sele.tinn One wav lo measlre r2 rs with a so-called plots are drawn so that the x- and y-axesintersect at the mean otfspring-parentregression (Falconer and Mackay1996). Scientists phenotyplcvalue of each population-theorigin of the plot is the measurethe phenotypicresemblance of a traitbetween parents and mean of both offspringand parentaltrait values.)As you can see, theiroffspring in a numberof differentfamilies. They then regress the both graphs have a positiveslope. but the left-handgraph dis- meantrait value of offspringagainst the meantrait valueof the par- playsa steeperslope than the right-handgraph (a: 0.8 and 0.2, ents.(The parent mean is oftencalled the midparentvalue because respectively).ln other words,the olfspringin the left-handgraph thereare only two parents.) havea strongerresemblance to their parentsthan the otfspringin Whenthese valuesare plottedfor many differentfamilies, the the right-handgraph (at leastwhen it comesto bodysize), relationshipis an indicationof the extentto which offspringtrait Let'snow considerhow the phenotypictrait changesfrom one valuesresemble those of their parents.lf thereis a significant posi- generationto the next.In the absence of selectionor anothermecha- tive relationship(i.e., the slopeis greaterthan 0), then parentswith nismof evolution,a populationshould not evolve.Offspring pheno- unusuallylarge trait values tend to produceoffspring who alsohave types shouldbe similarto parentalphenotypes, even if the trait in unusuallylarge trait values(and viceversa for parentswith smaller questionis heritable.(This is the phenotypicmanifestation of the trait values),The top two graphsrn Box FrgureZ3.i showtwo such Hardy-Weinbergtheorem we sawin Chapter6). relationships.

Box Figure7.3.1 Thetop two graphsshow parent-offspring regres- on the narrowsense heritability ofthe trait,represented here by sionsfor two populations.Purple circles indicate individuals that the slopeof parent-offspringregression. The lowerfigures show the reproduced.The difference between the averagevalue ofthe trait distributionofthe trait in the originalpopulation and in the offspring in the entirepopulation and among the reproducingindividuals is ofthe selectedparents. In the left-handexample, the evolutionary the strengthof selection(5). The response to selection(R) depends responseis largebecause narrow sense heritability is high.

X selected X selected

[--s-i Parents

Offspring Offspring

2O2 cHAprERsEVEN BEyoND aLLELEs: euaNTrrarlvE GENETIcsAND THEEvoLUTroN oF pHENorypEs But considerwhat happensif we applyselection to this popula- towardlarger trait sizes. The population will have evolved in response tion.We've already seen how selection can be a powerfulmechanism to selection.(The differencebetween the new mean of offspringand of evolutionbecause it can changeallele frequencies from one gen- the startingmean is a measureof the populationresponse to selec- erationto the next(Box 6.5). Because additive effects of allelescause tion,R.) relativesto resembleeach other in their phenotypes(i.e., because of Whenthe slopeof the offspring-parentregression is steep,the /,2),selection also can be a powerfulmechanism of phenotypicevolu- offspringphenotype distribution will experience a bigshift. When the tion.lt can causethe distributionof phenotypesto changefrom one slopeof the regressionis shallow,the offspringphenotypes will shift generationto the next. less.The slope of the regression,then, determines how mucha given Let'ssay that selectionfavors big body size in both speciesof populationwillevolve in responseto selection.As we knowalready, the fishes in the two graphsshown here. We'll represent this selectionby componentof variancethat causes a populationto evolvein response usingpurple circles to representindividuals that wereable to repro- to selectionis, by definition,the narrowsense heritability (ft'z). So the duce.These parents alone contribute offspring to the nextgeneration slopeof the offspring-parentregression must equalft2. of the population.This situatronresults in positivedirectional selec- We can reachthis sameconclusion by lookingat the regression tion on the phenotypictrait becausethe meantrait value in selected equationitself. A linearregression will take the form y : a \ x -r b, parentsis greaterthan the startingmean of the parentalpopulation. wherethe slopeof the relationship,a, is equalto the changein trait Thedifference between these means is the selectiondifferential (s). valuealong the y-axis,Ay, dividedby the changein trait valuealong To predict how much the offspringgeneration will evolvein thex-axis, AX: responseto this selection,we use the offspring-parentregression. a: LYfLx To do this,follow the mean valueof selectedparents on the x-axis : = up until it intersectswith the regressionline (vertical dashed line in In an offspring-parentregression, AI/ R,and AX S,so: eachplot). From this point, read across to the correspondingvalue on a: LY/AX = R/S the offspring(y) axis(horizontal dashed lines). This is the newmean traitvalue expected for the offspring.lf thisnew value differs from the and we know from the breeder'sequation (see Sectron7.2) IhaI meanof the populationbefore selection-in this case, if the newmean R = h2x,5, and thereforeIhat h2 : RI S.So the slopeof the regres- lresabove the origin-then the offspringdistribution will have shifted sion,a, equalsthe ftz.

of their parents.In such a case,spatial heterogeneity in water temperatureor the sup- ply of food for fry doesnot 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(Chapter 2): phe- notypic variation that influencesfitness (S),and the ability to transmit those pheno- typic characteristicsto offspring (h2).fi selectionis strong,a population can respond even if a trait is only weakly heritable. And even 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 Selectionand evolution are nof the same thing. Populations can experience selection even ifthey cannotevolve in resoonseto it.

Thespeed of evolutionis a productof the strengthof selection(S) and the extentto whichoffspring resembletheir parentsfor that trait (the heritabilityofthe trait,i2).

2.2 THEEVoLUTToNARv REspoNsE To sELEclol 2O3