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What Does the Comparative Method Reveal About Adaptation?

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What Does the Comparative Method Reveal About Adaptation? What does the Comparative Method Reveal About Adaptation? The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Leroi, A. M., M. R. Rose, and G. V. Lauder. 1994. “What Does the Comparative Method Reveal About Adaptation?” The American Naturalist 143 (3) (March): 381–402. doi:10.1086/285609. Published Version doi:10.1086/285609 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:33948436 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Vol. 143, No. 3 The American Naturalist March 1994 WHAT DOES THE COMPARATIVE METHOD REVEAL ABOUT ADAPTATION? A. M. LEROI, M. R. ROSE, AND G. V. LAUDER* Departmentof Ecology and EvolutionaryBiology, Universityof California,Irvine, California92717 SubmittedJuly 6, 1992; Revised March 4, 1993; Accepted April27, 1993 Abstract.-It has been suggestedrecently that new quantitativemethods for analyzing compara- tive data permitthe identificationof evolutionaryprocesses. Specifically,it has been proposed that new comparative methods can distinguishthe direct effectsof natural selection on the distributionof a traitwithin a clade fromthe effectsof drift,indirect selection, genotype-by- environmentinteraction, and uncontrolledenvironmental variation. Such methodscan suppos- edly unravel t-herelative importanceof these factors by the phylogeneticanalysis of traits, performanceattributes, and habitats. We argue thatthey cannot. We show thatmany different evolutionarymechanisms can, in principle,account for any one interspecificpattern, and we illustrateour case using examples fromthe comparativeliterature. We argue that these con- founded mechanismscan only be unraveled if patternsof selection or genetic variationand covariationare directlymeasured in many species withina clade. Even thoughcomparative methodsare valuable for examiningthe evolutionaryhistory of traits,they will oftenmislead in the studyof adaptive processes. The use ofcomparisons among extant species to identifyadaptations has many contemporarypractitioners, as well as a pedigreestretching back to the Origin of Species,if not to Paley's theisticbiology (Darwin 1859, 1871; Simpson 1953; Bock 1977; Clutton-Brockand Harvey 1979; Gould and Lewontin 1979; Trivers 1985; Coddington 1988; Baum and Larson 1991; Brooks and McLennan 1991; Ridley1992). More recently, the comparative method has also beenused to iden- tifytraits that are apparentlynot adaptive and theconstraints that cause themto be so (Coddington1988; Baum and Larson 1991;Brooks and McLennan1991). Thatis, comparativemethods are now beingused to revealthe mechanismsof evolution.This articleexamines the foundation of thisresearch strategy. First,we mustdefine the scope ofour inquiry. What is meantby "the mecha- nismsof evolution,"and whatkinds of studiesmake claimsabout them?By mechanismsof evolutionwe meanall thoseforces, such as geneticdrift, natu- ral selection,mutation, or migration,that mold the evolutionof populationsor clades. We thinkthat claims about such mechanisms are made moreoften than is readilyapparent, for instance, whenever a traitis identifiedas an adaptation. Thi-sposition may seem peculiarat first.After all, a distinctionis oftendrawn betweenadaptation as a processand adaptationsas traits(Futuyma 1986). But, as manydiscussions of adaptationand adaptationsshow, this distinction tends * To whom correspondenceshould be addressed. E-mail: [email protected]. Am. Nat. 1994. Vol. 143, pp. 381-402. C 1994 by The Universityof Chicago. 0003-0147/94/4303-0002$02.00.All rightsreserved. This content downloaded from 128.103.149.52 on Tue, 03 Mar 2015 16:41:08 UTC All use subject to JSTOR Terms and Conditions 382 THE AMERICAN NATURALIST to dissolve as these termsare more rigorouslydefined. Sober (1984, p. 208), for example, characterizesan adaptationas follows: "A is an adaptationfor task T in populationP ifand only ifA became prevalentin P because therewas selection for A, where the selective advantage of A was due to the fact that A helped performtask T." By Sober's definition,adaptations (as states) are, in part, de- finedby the evolutionaryprocess-direct selectionfor those traits-that gave rise to them. Some definitionsof adaptationdistinguish between the causes of the historical genesis of a traitand its currentmaintenance by selection: "we may designate as an adaptation any featurethat promotes fitness and was builtby selectionfor its currentrole" (Gould and Vrba, 1982, p. 6). This is a more historicalview of adaptation than Sober's. As such, it lends itselfnaturally to a comparativeor phylogeneticcontext, and as the analysis of interspecificpatterns has become more sophisticatedover recent years, it has been widely adopted. Coddington (1988, p. 3), forexample, definesan adaptationas an "apomorphicfunction pro- motedby naturalselection" and states elsewherethat "an evolutionarydefinition of adaptationmust have an historicalcomponent specifying selection as the evolu- tionaryagent responsible for the appearance of the feature" (p. 5). In theirdefini- tionof an adaptation,Baum and Larson (1991) add to thisby explicitlyincorporat- ing the idea of a trait'sperformance; stated in a way comparable to Sober's, it mightread as follows: A' is an adaptation for task T in clade C if and only if (1) A' is currentlymaintained by natural selection in C because of its superior performancea' at task T relativeto the ancestralcondition A and its performance a, and (2) A' originallybecame prevalentin C because of selectionfor its superior performanceax' at task T. Baum and Larson (1991) definemaladaptive and selec- tivelyneutral traits in an analogous fashion:if the performanceof the derivedtrait is lower thanthat of the ancestralcondition (at' < at), thenA' is a "disaptation"; if the derived performanceis equivalent in in-groupand out-grouptaxa (a-' = at), thenA' is a "nonaptation." The importantpoint is that, like Sober's, all these definitionsof adaptations are foundedon statementsabout an evolutionarypro- cess: naturalselection. Given thatadaptations can be definedin principle,how should theybe identi- fiedin practice? Most biologistswould agree that,at a minimum,the functionof a putativeadaptation should be well understood.Many otherswould add thatthe phylogeneticdistribution of a traitshould also be known.Baum and Larson (1991) attemptto apply theirdefinition. They argue thatidentification of thephylogenetic distributionof a derived trait,its performancerelative to the ancestraltrait, and the "selective regime" thatputatively influences its evolutionare necessary and sufficientto distinguishbetween adaptive and nonadaptivetraits. This position, or one similarto it, is held by Greene (1986) and Coddington(1988), as well as Harvey and Pagel (1991, p. 11), who assert, "Stripped to the bone, . the evidence for adaptive evolution revealed by comparative studies is correlated evolution among charactersand environments."It is an attractiveview, for it offersthe hope thatclades can be inventoriedfor adaptations, nonaptations, and disaptationswithout having actually to measure natural selection operatingon traits. This content downloaded from 128.103.149.52 on Tue, 03 Mar 2015 16:41:08 UTC All use subject to JSTOR Terms and Conditions COMPARATIVE METHODS AND ADAPTATION 383 In this article,we take issue withthis position. We will argue thatknowledge ofthe phylogeneticdistribution of traits,their performance, and selectiveregimes are not sufficientto identifyadaptations. This is not a completelynovel perspec- tive; both Mishler(1988) and Brandon (1990) have statedthat a completeadaptive explanationrequires both a demonstrationof the relative fitnessof a putative adaptationand the traitit supplants,as well as genetic information.We agree. But we will go furtherthan these authorsand argue that,in the absence of such broader information,phylogenetic patterns will often suggest that a traitis an adaptationwhen in fact it is not and suggestthat it is not, when in fact it is. We begin our argumentwith a discussion of theoreticaland empiricalfindings frompopulation genetics and show how the effectsof selection, patternsof ge- neticcovariation, genetic background, environment, and the interactionof geno- types withtheir environment influence the observed distributionof traitsamong populations,species, and highertaxa. Given these factors,we reevaluate recent articles-both methodologicaland specificcase studies-that claim to inferadap- tationby the comparativemethod. Finally, we consider the general implications of our critique,particularly with respect to the circumstancesin which the com- parativemethod can legitimatelybe used to analyze adaptationand evolutionary constraint. POPULATION GENETICS OF MULTIPLE FITNESS-RELATED CHARACTERS It is our primaryintent in this section to show how any single comparative patterncan arise by means of very differentevolutionary genetic mechanisms. Formally,our basic argumentscan be developed in terms of a two-character, two-allele,one-locus model, thoughlater we consider otherloci and characters in the developmentof our argument.Say thatwe have two alleles at a locus, BI and B2, that can affecttwo distinctcharacters, Cl and C2, with any patternof dominance: Genotype B1B1 BIB, BIB, H +3, CharacterChaacerC1 Cl HIH2 +4PI+ YI HIH2 H2I + Y2 The Pi and -yispecify the allelic
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