Testing adaptation with phylogeny: how to account for phylogenetic pattern and selective value together

© The Norwegian Academy of Science and Letters • Zoologica Scripta,

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, 5, September 2003, pp483–490

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Grandcolas, P. & D’Haese, C. (2003). Testing adaptation with phylogeny: how to account forphylogenetic pattern and selective value together. —

Zoologica Scripta

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, 483–490.If most agree with the dual pattern/process definition of adaptation, an apomorphy promotedby natural selection, few indeed identify an adaptation using the same methodological proce-dure. Most differences between procedures rest with the way the role of natural selection isanalysed in a phylogenetic perspective. We argue that the selective value of a character cannotbe phylogenetically reconstructed, but must be considered independently from the phylogeneticanalysis in the framework of population biology. The phylogenetic pattern for the characterof interest can only be used to refute or corroborate circumstantially the macro-evolutionarypredictions issuing from population studies.

Philippe Grandcolas, ESA 8043 CNRS, Laboratoire d’Entomologie, Muséum National d’HistoireNaturelle, 45 rue Buffon, 75005 Paris, France. E-mail: [email protected] D’Haese, Division of Invertebrates Zoology, American Museum of Natural History, CentralPark West at 79th Street, New York, NY 10024, USA

Blackwell Publishing, Ltd

Testing adaptation with phylogeny: how to account for phylogenetic pattern and selective value together

P

HILIPPE

G

RANDCOLAS

& C

YRILLE

D’H

AESE

Accepted: 30 September 2002

Introduction

There is now a general agreement concerning the possibilityof analysing adaptation in a phylogenetic perspective (but seeReeve & Sherman 1993). Several seminal studies have estab-lished methodological issues in this respect, either becausethey analysed the general relationships between pattern andprocess (Eldredge & Cracraft 1980), or because they perceivedthe need for a historical definition of adaptation (Gould &Vrba 1982), or because they addressed more specifically fun-damental questions about the utility of phylogenetic patternsto define the concept of adaptation (Greene 1986; Coddington1988; Carpenter 1989; Wanntorp

et al

. 1990; Brooks &McLennan 1991), in the framework of the phylogenetic testsof evolutionary scenarios (Deleporte 1993; Grandcolas

et al

.1994, 1997a, 2001).

Phylogenetics provides a historical perspective concerningthe character supposedly adaptive, and analyses its descentwith possible modification in the clade under study. How-ever, a consensus is not yet attained concerning the specificinformation the phylogenetic pattern can bring concerningadaptation: once reconstructed, the phylogenetic pattern forthe character of interest has been diversely utilized. Greene(1986) proposed to analyse jointly the patterns of a characterand of its performance advantage. Coddington (1988) pro-posed to study only the phylogenetic pattern of the characterand to check the adaptive value in populations. Baum &Larson (1991) replaced the measure of the selective value byconsideration of selective regimes. Others also use these

phylogenetic patterns to refute or corroborate macro-evolutionary predictions of adaptationist models only (modelsderived mostly from population studies — the ‘evolutionaryscenarios’) (Carpenter 1989). Or, phylogenetic patterns areused to implement evolutionary models or to suggest futureresearch directions (Packer 1997).

Indeed, the diversity of procedures aimed at detectingadaptation phylogenetically seems more to indicate a mis-understanding of basic principles of phylogenetic analysis thanto reflect the idiosyncrasies of a diversity of specific goals. Ageneral semantic confusion may also be partly responsible forthis situation. A re-definition of both the methodology andthe terms utilized therefore appears needed. Also, severalauthors have been critical of the use of phylogeny in the studyof adaptation (e.g. Reeve & Sherman 1993; Leroi

et al

. 1994;Westoby

et al

. 1995). We argue that these criticisms concernonly some of the uses of phylogenetic patterns to test adap-tation, which are actually inappropriate. They do not concernthe very nature of this methodology and should not encour-age scepticism concerning adaptational studies in compara-tive biology.

Pattern and process or ‘the cowl does not make the monk’

Most authors, if not all, agree with the definition of adapta-tion as an ‘apomorphic function promoted by naturalselection’ (Coddington 1988: 3). In other words, because anadaptation has originally been defined as an evolutionary

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novelty in a given taxon, it can therefore be characterized asan apomorphy of this taxon. Conversely, if not apomorphic ina taxon, a character is not, strictly speaking, an adaptation atthe level of this taxon: both apomorphy and adaptation canonly be relatively assessed. Thus, most agree that phyloge-netics provides a historical pattern for determining whethera character of interest can be interpreted as a novelty for agiven taxon. This is the ‘phylogeny criterion’ of adaptation,which pertains to the pattern-part of the concept of adapta-tion. But, it is erroneous to conclude that all apomorphiesare adaptations, even if all adaptations are apomorphies(Coddington 1988: 6): it is also necessary to infer that theyhave been promoted by natural selection. This is the secondcriterion of adaptation, which pertains to the process-part ofthe concept of adaptation (e.g. Williams 1966); we propose toname it the ‘selection criterion’. This last criterion, men-tioned by Coddington (1988), has been criticized by de Pinna& Salles (1990) who disagreed with the possibility of con-sidering both the phylogenetic pattern and the process ofnatural selection at the same phenomenological level, and tomerge them in a composite approach. Their criticism has,however, been rejected by Coddington (1990) who statedthat natural selection is not considered within the frameworkof phylogenetic analysis, but merely as additional informa-tion issuing from population studies, which can be utilizedtogether with the results of the phylogenetic analysis.

Both the phylogeny and the selection criteria obviouslyalso apply to the case of exaptation (Gould & Vrba 1982),where the character is plesiomorphic but its role apomorphicand supposedly maintained by natural selection (Greene1986; Grandcolas

et al

. 1994).The most important criticism of Leroi

et al

. (1994) againstthe phylogenetic study of adaptation deals specifically withthe duality of the two criteria – phylogeny and selection cri-teria — and the need to consider both of them to detect adap-tation fully. However, this criticism should be mostly addressedto the ‘convergence approach’, as it is termed by Coddington(1990, 1994), which is aimed at identifying adaptation mainlyby repeated convergence — using only the phylogeny criterion(e.g. Harvey & Pagel 1991) — rather than to any phylogenetictest of adaptation in the ‘homology approach’ which is aimedat refuting or corroborating adaptive hypotheses using bothphylogeny and selection criteria (Coddington 1990, 1994).Leroi

et al

. (1994) argued that several particular processesmay obfuscate the pattern significance and prevent identifi-cation of an adaptation only as a repeatedly derived character.This criticism was already formulated by Coddington (1990:385) and reiterated by Carpenter (1992) and by Wenzel &Carpenter (1994). If only homoplastic (convergent) phyloge-netic patterns are adduced as an indication of adaptation,only the ‘phylogeny criterion’ is used. In other words, that acharacter has evolved repeatedly by convergence does not

indicate that it has necessarily a higher selective value in itshomoplastic state than in its symplesiomorphic state (contraPagel 1994). Patterns cannot be taken as a direct indicationof the occurrence of processes. Being pragmatic [as argued byPagel (1994)], one should better consider an apomorphy as aputative adaptation in need of being assessed as such bypopulation studies (Ridley 1983: 7; Brooks & McLennan1991: 184; Coddington 1994).

Clearly, these criticisms stress the need for applying as faras possible the second criterion but do not show that the firstcriterion is less important and that phylogenetics is useless tostudy adaptation. We need now to understand how to imple-ment the selection criterion to detect adaptation fully.

The character and its function, role, current utility, performance, selective value, selective regime: a question of terms

Many terms are utilized to describe how characters areused by the organisms and what is the advantage conferred tothe organism by the character in terms of increased fitness.Before trying to decipher how authors use the ‘selection cri-terion’ and discussing how this criterion should be used, it isnecessary to distinguish between the different prevalentterms (and their possible different meanings), qualifying theconcepts directly related to this ‘selection criterion’.

‘Function’ is probably the most often used and also themost misleading term. In a traditional definition, transmittedfrom early ethology to current natural history, function is theway a given structure is used by the organism (e.g. Tinbergen1951). This meaning was employed by Grandcolas

et al

.(1994, 1997a). However, ‘function’ is also employed to mean‘all physical and chemical properties of a structure that relateto its form and organization’ (Lincoln

et al

. 1982), or evencombines both the way the character is used and the selectivevalue of this use: ‘the function of a trait is the increase inreproductive success which it confers on its possessor geneticconstitution …’ (Clutton-Brock 1987: 220). This plethora ofdifferent meanings seems to cause misleading semantic shiftseven in the clearest issues. For example, Coddington (1994:57) clearly summarized his views in his fig. 1, showing thatthe ‘function’ of a character may be phylogenetically recon-structed, just as the character itself. According to the samefigure, the selective value is not reconstructed on the tree andis figured only below the tree. One can suppose that functionand selective value are quite independent from each other.However, the author (Coddington 1994: 56) previously com-mented that ‘rigorous adaptational hypotheses include spe-cific descriptions of the nature of the selection presumed tohave operated, because the core criterion of adaptation is

function

’ [italics added]. This sentence does not make clearwhat the author defines as ‘function’: if it is the core criteriondefining what kind of selection operates, ‘function’ can be


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interpreted as more related to selective value than beingsimply the way the character is used by the organism. Indeed,the way the character is used is theoretically no more relatedto selective value than the character itself. An inexperiencedreader can therefore suppose that perhaps two differentmeanings of the term ‘function’ are used there (Coddington1994: 56, 57).

Conversely, ‘role’ is certainly the term most devoid of con-notations, simply being the way the character is used, withouthypotheses of any particular conferred advantage.

The term ‘performance advantage’ (e.g. Greene 1986;Arnold 1994), sometimes abbreviated to ‘performance’, seemsat first glance less ambiguous than ‘function’. The perform-ance of a character would confer an advantage of fitness forthe organism which displays it. However, its common mean-ing as well as its abbreviation as ‘performance’ may be mis-leading. Its common meaning suggests that the better theperformance, the higher the fitness conferred: performanceseems often to be used in many citations as a synonym ofselective value, except that this synonymy fallaciously con-founds the cause (performance) and the possible effect(selective value). The common meaning is nonsensical in thisrespect, because even a high performance may be completelydisadvantageous in some circumstances. For example, con-trary to what is assumed by Andersen (1995) in his case study,performance

sensu stricto

has no obligatory relationship withfitness: water striders may row instead of walk on the watersurface (Andersen 1995: 283, 290), they certainly move fasterin this way. But do they have more progeny with a higher sur-vival rate? Moving fast could make them more conspicuousto predators detecting moving targets or make them morelikely to be swamped, and thus can possibly decrease their fit-ness. When Andersen (1995: 280) stated

If the apomorphic state of an attribute can be shown to have a supe-rior performance relative to its plesiomorphic state, and can be inferredto have evolved after historic changes in environmental conditions,then, and only then, is the trait or attribute an adaptation

.He replaced performance advantage with performance

sensustricto

. Thus, he could not make further reference to the neo-darwinian concept of adaptation and he could not test it usingcladistics.

‘Current utility’ is certainly less equivocal as most authorsuse it with approximately the same meaning as selectivevalue (e.g., Baum & Larson 1991: 6). However, there is againa semantic shift between common sense which suggestsutility, and the current scientific sense which includes fitnessconsiderations.

‘Selective regime’ has recently been used in the presentphylogenetic context by Baum & Larson (1991). They definedthe selective regime as ‘the aggregate of all such environmentaland organismic factors that combine to determine how naturalselection will act upon character variation’ (Baum & Larson

1991: 4). Larson & Losos (1996: 199) proposed a similar def-inition: ‘critical aspects of organismal/environmental inter-action that are postulated by a hypothesis of adaptation to besignificant factors influencing natural selection of the charactersbeing studied …’. Both pairs of authors used it as a substituteto a precise measurement of selection level. They recognizedthat ‘it is difficult in practice to make an assessment of thecomprehensive selective regime’ and that ‘instead, criticalaspects of the environment/organism interaction are identi-fied and postulated to be major factors influencing the poten-tial action of natural selection on the character variation understudy’ (Baum & Larson 1991). ‘Selective regime’ is thus anundetermined combination of

ad hoc

hypotheses on the envi-ronment/organism interactions.

Among the terms used by the authors, most are ambiguousand should be employed together with preliminary caveats.Or, possibly, other terms devoid of ambiguity should be pre-ferred. ‘Role’ and ‘selective value’ can be recommended asbeing devoid of ambiguity for indicating, respectively, theway a character is used and the advantage it confers in termsof fitness for the organism.

How to deal phylogenetically with the ‘selection criterion’ for testing adaptation

Although most authors recognize the pattern/process dualityof the concept of adaptation, few indeed apply both necessarycriteria in the same way — and especially the selection crite-rion — to detect fully adaptation.

Coddington (1990) used the example of rhinoceratid hornsand of their supposed predatory defence value to illustrate hismethodological concepts but, in the present sense, he did notmake totally clear how to use the ‘selection criterion’. A pos-teriori to the reconstruction of the evolutionary sequence ofthe horns in rhinoceros, he recommended measuring in thefield the fitness conferred by different kinds of horns to rhi-noceros in selected environments (Coddington 1990: 382). Itis not mentioned whether these fitness measures must beoptimized on the phylogenetic tree to obtain their phyloge-netic pattern, or if they must be used only as a narrativeassessment that the apomorphic state has possibly a higherselective value.

Greene (1986: 3) took a clear position in this respect. He statedthat the evolution of both the character’s states and their select-ive values must be reconstructed on the tree and according tohim, ‘determining if features and performance advantages arecoincident …’ should test convincingly for adaptation.

Baum & Larson (1991) followed the concepts of Greene(1986) and thus intended to reconstruct the phylogeneticpattern of selective value. These authors proposed to use thenotion of selective regime to implement this reconstruction.Taking into account selective regimes allows the constraint ofmeasuring selective values in populations to be avoided.


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From this small and non-exhaustive sample of authors,one can see that the ‘selection criterion’ of adaptation is notapplied in a single way. The primary difference between thesedifferent approaches rests on whether the phylogeneticpattern of selective values is searched for or not.

This difference calls for an elementary comment: evolu-tion is basically descent with modification and phylogeneticsanalyses the relationships between taxa which result fromevolution. The first characteristic of phylogenetic charactersis thus their capacity (most often only postulated) to be inher-ited. Only the intrinsic characters of taxa which have a majorheritable component may be analysed in a phylogenetic per-spective. For this reason, traits which are totally extrinsic totaxa cannot be utilized in the analysis because they cannot have

per se

an informative value concerning descent with modifi-cation (Nelson 1970; Dupuis 1984; Mickevich & Weller1990; Geiger

et al

. 2001; Grandcolas

et al

. 2001; Kluge 2001).Indeed, this is the case for the selective value which should

not be used or even mapped a posteriori on a phylogenetictree. The selective value of a trait depends more on the envi-ronment than on the trait itself or on its role. In this way, theselective value is not just one more ‘non-traditional’ phylo-genetic character such as behaviour, or even host (for para-sites) or distribution area. We do not argue that selectivevalue is too variable or labile to be phylogenetically recon-structed as claimed by Frumhoff & Reeve (1994), as far as thisclaim makes sense (Schultz

et al

. 1996).Selective value differs greatly from those non-traditional

characters which depend directly on the behaviour of species,behaviour dictated by heritable neurological patterns andheritable ecological or physiological preferenda of species.For example, the habitat choice of a species results from suchheritable preferenda. To a certain extent, the occupancy of ahost by a parasite, or the occupancy of a distribution area bya taxon, also depend on such preferenda (by the addition ofindividual behaviours in all populations). On the contrary, theselective value of a character does not depend on such pref-erenda because it is the value that a character can confer in atotally extrinsic context. This context is independent from anycharacters of the taxon. If the character is indeed itself herit-able, its value in terms of conferred fitness is definitely not.

Eldredge & Cracraft (1980: 278) earlier emphasized thatnatural selection is a concept ‘designed for, and limited to,within-population situations’. They suggested that only thephenomenological level, respectively, population or clade,renders appropriate or not the application of the conceptof natural selection. We argue further that, by definition,selective value is not an intrinsic and heritable feature oforganisms and cannot be considered in a phylogeneticperspective. Its extrapolation to the past, using parsimoniousreconstructions, has no common sense: a selective value is nottransmitted by inheritance from an ancestor to a descendant.

Thus, it has no reason to be inferred present in all the descend-ants of the same ancestor which showed it, and it cannot beused to assess the monophyly of a clade by virtue of its apo-morphic value. Its phylogenetic reconstruction is

per natura

impossible. A more general comment concerning cladisticsand historical reconstructions may be made at this occasion.Cladistics has been used to perform diverse historical recon-structions, outside the field of phylogenetics (e.g. linguistics,ecological communities). These reconstructions deal withproblems of evolution (even if it is not biological evolution

sensu stricto

), i.e. with characters conserved and transmitted(possibly with modification) by replicators during the past,owing to diverse mechanisms (e.g. cultural or inertial). In anycase, cladistics deals with transmitted characters which aredifferent from the selective value which is neither conservednor transmitted by taxa by any means. Reconstructing thehistory of selective values is not equivalent, more or less, toreconstructing the history of some cultural or inertial traits:it is not a task for cladistics.

Let us consider again the well-known example of rhino-ceratids, prominently re-analysed by Coddington (1988, 1990),to illustrate this statement. Rhinoceros show the characters‘one horn–two horns’ of which the role is defined as ‘defenceagainst predators’, both character and role being heritable,with possible different(ial) selective values with respect topredation. However, the selective values of these characters/roles depend totally on the environment of rhinoceros. Dorhinoceros suffer presently from attacks of predators thatcan be inhibited or stopped by the use of horns, and did therhinoceros suffer from these predators in the past? This ques-tion concerning the past deals not only with the presence ofspecific predators, but also with their past spatial distribution(were these predators sympatric or syntopic with rhino-ceros?), their past (relative) abundance (were these predatorsas abundant as presently?), their past degree of satiation (werethese predators repleted with prey more profitable and locallymore abundant than rhinoceros and let the rhinoceros be lesspredated?), etc.

If the study of rhinoceros was aimed at studying the evolu-tion of their habitat choice, it would not have been a problemto analyse habitat phylogenetically: rhinoceros have plausiblyheritable preferenda concerning their perception of environ-ment, exposure to the sun, water availability, food character-istics, etc. which make habitats some kind of heritable andintrinsic features.

In short, predators (= context) and the resulting selectionpressures are not heritable characteristics of rhinoceros, so theycannot take part in the phylogenetic analysis of rhinocerosand/or be parsimoniously reconstructed. Contrary to herit-able characters, their distribution on a tree provides noinformation about their evolutionary rate of change (Schultz

et al

. 1996).


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Without indication of selective value, an apomorphy cannever be assessed as adaptive. What is thus the possibility forapplying the ‘selection criterion’ effectively to detect adapta-tion? Selective value can only be measured in populationsusing variation in different individuals or populations of thespecies considered: a selective advantage conferred by thecharacter’s state is characterized as increasing the fitness.This is a populational measure, possibly quantified, forexample, as ‘the average number of surviving progeny of onegenotype compared with the average number of survivingprogeny of competing genotypes’ (Lincoln

et al

. 1982).One could suppose that, even if it is not phylogenetically

analysed, the selective value of a character’s state could betaken into consideration at the present time in the way men-tioned by Coddington (1990), checking that the supposedlyadaptive apomorphy has actually a higher selective value thanthat of the corresponding plesiomorphy. In our opinion, thisis a misleading procedure which no longer has a relationshipwith the phylogenetic analysis, but rather with a very partic-ular model of evolution. It is equivalent to analysing phylo-genetically the selective value and assuming that it has notchanged since the time of the appearance of the taxa and oftheir apomorphies, an

ad hoc

hypothesis less than reliableconcerning a variable and non-heritable feature.

The same kind of misleading procedure was proposed andemphasized by Baum & Larson (1991), who replaced themeasure of selective values with the use of selective regime(discussed

supra

). Using selective regime leads further intothe field of unwarranted hypotheses: selective values are notonly extrapolated to the past, but they are also not reallymeasured in the present time. Their value is hypothesizedaccording to arbitrary selected environmental and organismicinformation, which is at best an argument no more relevantthan current opinion. Even if one agrees that both phylogenyand selection criteria are necessary to corroborate that a char-acter is adaptive, it is scarcely acceptable to use only an

ad hoc

hypothesis to implement one of these criteria. Using the con-cept of selective regime to implement the ‘selection criterion’for want of population studies is analogous to using taxo-nomic ranks for want of phylogenetic trees to implement the‘phylogeny criterion’. Both practices are doomed to failureand to disappearance because they are based on fallaciousconcepts and they bias the analyses in an unpredictable way[see, for example, Brooks & McLennan (1991), O’Hara(1992) and Coddington (1994) concerning the misleadinguse of taxonomic ranks in comparative biology].

Moreover, from an empirical point of view, the concept ofselective regime seems too vague to be readily employed(Leroi

et al

. 1994). Looking at the studies using the conceptof selective regime, it appears that the features which aretermed so are actually the ‘role’ of the characters of interest.Baum & Larson (1991) presented an example concerning sal-

amanders, their tarsal morphology and their locomotoryhabits. They documented shifts between terrestrial and scan-sorial habits which were diversely associated with changes intarsal morphology. Locomotory habits are taken by the authorsas the selective regime for tarsal morphology. Actually, scan-sorial and terrestrial represent behavioural characteristicsand not selective regimes. They can be simply categorized asbeing several possible biological roles of tarsal morphology,in the same way that defensive behaviour may be a possiblerole of rhinoceros’ horns.

Also, Cigliano

et al

. (1996: 127) considered ovipositionhabits as being the selective regime for ovipositor valves ingrasshoppers to test for the occurrence of adaptive radiation

… Determination of the shift in the environment with respect tothe genealogical relationships of the taxa as portrayed in the phyl-ogeny. The hypothesized environmental change may be related toalterations in the ‘selective regime’ experienced by the taxa

. In the same way as in Baum & Larson’s (1991) study, ovipo-sition habits are only the ‘role’ of the ovipositor, a behav-ioural characteristic unrelated to any measure of present, pastor future selective value for the ovipositor or its use. Theadaptiveness of such a feature can a priori seem obvious but,actually, it can be disadvantageous or neutral, depending onextrinsic conditions in which the feature is used (e.g. charac-teristics of rhinoceros’ predator, substrate characteristics forscansorial salamanders or ovipositing grasshoppers).

Larson & Losos (1996: 201), arguing that selective regimeis a valuable concept, admitted that measuring ‘selection act-ing within populations [ … ] provides potentially the mosteffective test of the macro-evolutionary stability of selectiveregimes’. However, this claim and also the contention that‘the use of selective regimes can be abused’ (p. 214) does notjustify the fact that selective regime is employed for want ofselection measurement (even at the very worst). The conceptof selective regime is basically flawed because it implies toomany hypotheses while we should seek for well-establishedfacts, and because it confuses two phenomenological levels,populations and clades.

Indeed, although most authors promoting the use of selec-tive regimes claimed that Gould & Lewontin (1979) hadfruitfully revised the ‘adaptationist programme’ (Baum &Larson 1991: 1; Larson & Losos 1996: 188), they re-introducedthe adaptationist biased notion that characters with bio-logical roles (their selective regime) are currently adaptive,a notion which was specifically denounced by Gould &Lewontin (1979). Using selective regime is not different frommisleadingly arguing that a character used by an organism, ina context where it is supposedly useful, is necessarily profitableto this organism. The so-called selective regimes are phylo-genetically analysed, but the basic and unwarranted adapta-tionist hypothesis remains.

Selective regime as conceived by Baum & Larson (1991) is


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not only a biased substitute for selective values, but also anon-operational concept as most studies that intended to useit deviate towards using simple behavioural features. Behav-ioural features are characters just as morpho-anatomy ormolecules, which are simply in need of precise delineationthrough ethological studies (Wenzel 1992). As with any othercharacter, there is no reason to presume their adaptive valueor co-adaptive value towards another feature.

In conclusion, because selective values are definitely notheritable characteristics of taxa, they cannot be used in aphylogenetic analysis: their extrapolation to the past throughtheir misconceived phylogenetic reconstruction is impos-sible. And, definitely, if some selective values (and not somemisleading substitutes such as selective regimes or perform-ance) reveal congruence a posteriori with other charactersaccording to a phylogenetic analysis, this cannot indicateinheritance of the selective value, which is not transmittedfrom ancestors to descendants, but would merely represent anonsensical by-product of the distribution of a selective valuetoday in some terminal taxa together with the related synapo-morphic character of interest.

Phylogenetic inference of adaptation or phylogenetic test of evolutionary scenario?

All the previous examples deal with analysing selective valuesphylogenetically and misconstrue the relationships betweenpattern and process. The process is incorrectly deduced fromthe pattern instead of being studied independently. A partic-ular and unwarranted evolutionary model of selective stabilityis implied by these approaches. In other words, the selectivevalue measured in the present and particular circumstances isconstrained to follow a phylogenetic pattern dictated bycharacters which have no obligatory relationships with it.

An alternative approach may separately consider the phy-logenetic pattern and the evolutionary process. As empha-sized in his title ‘Testing scenarios’, Carpenter (1989) clearlycontrasted the phylogenetic patterns and the predictions ofevolutionary models, the so-called evolutionary scenarios(Tattersall & Eldredge 1977). The phylogenetic pattern isonly used in this case as a kind of null hypothesis whichpermits testing the hypothesis of adaptation. This methodo-logy was also implemented and/or emphasized by Brooks &McLennan (1991: 184), McLennan (1991), Deleporte (1993),Grandcolas

et al

. (1994, 1997a, 2001), and Desutter-Grandcolas(1997).

To explain this procedure in some detail, population stud-ies can measure the selective values of features and observetokogenesis in varied taxa: for example, assess that the trait ‘

α

’in the taxon ‘X’ has a high selective value in a situation ‘A’.They can extrapolate from these observations to macro-evolutionary events and suggest that the actual pattern of lifediversity originates through this kind of process: ‘

α

’ is an

adaptation of ‘X’ in the situation ‘A’, i.e. an evolutionarynovelty that has occurred by mutation in the ancestor of ‘X’and has been maintained and favoured by natural selection inthe situation ‘A’. This is indeed an extrapolation as the selec-tive value of ‘

α

’ measured at the present time is supposed tohave been identical in the ancestor of ‘X’ and because the sit-uation ‘A’ is also supposed to have occurred since that time.To test this extrapolation (= evolutionary scenario), we needan independent source of information which substantiatesthe extrapolation. This independent source is represented bythe phylogeny which can assess whether the evolutionarypattern of the character ‘

α

’ matches the extrapolation.As for any scientific test, the result is particularly demon-

strative in the case of refutation, because the tested hypothesiscan no longer be considered as possible (the test only dependson the accuracy of the phylogenetic reconstruction) (Wanntorp1983; Coddington 1990; Brooks & McLennan 1991: 86; Wenzel& Carpenter 1994). Conversely, the test seems weaker in thecase of corroboration, as it validates only the pattern of evo-lutionary changes for the character of interest and not directlythe processes hypothesized as being responsible for this changein the evolutionary scenario (stability of the selective value orof the environment). Actually, for this kind of test, this meansthat a corroboration (phylogenetic pattern matching modelprediction) cannot be taken as a demonstration that a charac-ter is an adaptation, but only as a strong indication that it ispossible. The validation of the hypotheses which do not relydirectly on the organisms under study but rely at least partlyon past environmental characteristics should obviously be theobject of palaeo-environmental studies [suggested in Baum &Larson (1991) as a means to check the exactness of the selec-tive regime]. That the phylogenetic corroboration of a toko-genetic hypothesis is weak is not a new statement! One candraw a parallel between testing phylogenetically adaptationand testing phylogenetically ancestor–descendant relation-ships between taxa. Engelmann & Wiley (1977) and Eldredge& Cracraft (1980) demonstrated that one can refute ancestor–descendant relationships with only one synapomorphy.They also remarked that, conversely, the corroboration ofancestor–descendant relationships (when synapomorphies lack)remains so weak that the identification of ancestral taxa isnow no more acknowledged. Why should the corroborationof adaptation be viewed as a more reasonable statement?

This does not preclude using the phylogenetic pattern as aheuristic tool to suggest future research directions (Brooks &McLennan 1991; Packer 1997): an apomorphy is a well-suitedcandidate for present-day adaptive value (Coddington 1994),and population studies may be orientated towards document-ing this possibility.

Conclusion

It should once more be emphasized that evolution should be


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studied in both clades and populations (Grandcolas

et al

. 1997b).As argued previously by Coddington (1988), both approachesare necessary and complementary. If some people want to usephylogeny for predicting selective values, they would gobeyond the operational field of phylogenetic analysis. Phylo-genetic analysis can only reconstruct the nested changes ofcharacter states among taxa. Population biology can observepresent-day processes, and provides us with instantaneousevolutionary pictures (even if technical difficulties remainsomewhat important, e.g. Endler 1986; Grafen 1988) butcannot extrapolate them back to the past without weakeningthe reliability of its conclusions (Grandcolas & Deleporte1996). Both approaches are thus doomed to cohabit in theframework of evolutionary biology to study evolution thor-oughly. Many past attempts to merge the studies of patternsand processes in an integrated framework have, however,failed (Eldredge & Cracraft 1980). To prevent future failures(Grandcolas

et al

. 1997a), we must keep in mind the powersand the limitations of each approach.

Acknowledgements

We are grateful to the persons who commented on themanuscript and made valuable and helpful suggestions:N. Andersen, J. M. Carpenter, M. M. Cigliano, J. Coddington,P. Deleporte, L. Desutter-Grandcolas, H. E. Wanntorp andJ. Wenzel.

References

Andersen, N. M. (1995). Cladistic inference and evolutionary sce-narios: locomotory structure, function, and performance in waterstriders.

Cladistics

,

11

, 279–295.Arnold, E. N. (1994). Investigating the origins of performance

advantage: adaptation, exaptation and lineage effects. In P.Eggleton & R. I. Vane-Wright (Eds)

Phylogenetics and Ecology

(pp. 123–168). Linnean Society Symposium Series. Number 17.London: Academic Press.

Baum, D. A. & Larson, A. (1991). Adaptation reviewed: a phyloge-netic methodology for studying character macroevolution.

Systematic Zoology

,

40

, 1–18.Brooks, D. R. & McLennan, D. A. (1991).

Phylogeny, Ecology, and Behavior

.

A Research Program in Comparative Biology

. Chicago: University ofChicago Press.

Carpenter, J. M. (1989). Testing scenarios: wasp social behavior.

Cladistics

,

5

, 131–144.Carpenter, J. M. (1992). Comparing methods. Review of ‘The Com-

parative Method in Evolutionary Biology’ by Paul H. Harvey andMark D. Pagel 1991. Oxford University Press.

Cladistics

,

8

, 191–196.Cigliano, M. M., Ronderos, R. A. & Kemp, W. P. (1996). Phyloge-

netic relationships of

Scotussa

and

Leiotettix

(Orthoptera: Acridi-dae).

Cladistics

,

12

, 125–138.Clutton-Brock, T. (1987). Function. In D. McFarland (Ed.)

TheOxford Companion to Animal Behavior

(pp. 220–223). Oxford:Oxford University Press.

Coddington, J. A. (1988). Cladistic tests of adaptational hypotheses.

Cladistics

,

4

, 3–22.

Coddington, J. A. (1990). Bridges between evolutionary pattern andprocess.

Cladistics

,

6

, 379–386.Coddington, J. A. (1994). The roles of homology and convergence

in studies of adaptation. In P. Eggleton & R. I. Vane-Wright (Eds)

Phylogenetics and Ecology

(pp. 53–78). Linnean Society SymposiumSeries. Number 17. London: Academic Press.

Deleporte, P. (1993). Characters, attributes and tests of evolutionaryscenarios.

Cladistics

,

9

, 427–432.Desutter-Grandcolas, L. (1997). Studies in cave life evolution: a

rationale for future theoretical developments using phylogeneticinference.

Journal of Zoological Systematic and Evolutionary Research

,

35

, 23–31.Dupuis, C. (1984). Willi Hennig’s impact on taxonomic thought.

Annual Review of Ecology and Systematics

,

15

, 1–24.Eldredge, N. & Cracraft, J. (1980).

Phylogenetic Patterns and theEvolutionary Process

.

Method and Theory in Comparative Biology

.New York: Columbia University Press.

Endler, J. A. (1986).

Natural Selection in the Wild

. Princeton: Prince-ton University Press.

Engelmann, G. F. & Wiley, E. O. (1977). The place of ancestor–descendant relationships in phylogeny reconstruction.

SystematicZoology

,

26

, 1–11.Frumhoff, P. C. & Reeve, H. K. (1994). Using phylogenies to test

hypotheses of adaptation: A critique of some current proposals.

Evolution

,

48

, 172–180.Geiger, D. L., Fitzhugh, K. & Thacker, C. E. (2001). Timeless char-

acters: a response to Vermeij (1999).

Paleobiology

,

27

, 177–178.Gould, S. J. & Lewontin, R. C. (1979). The spandrels of San Marco

and the Panglossian paradigm: a critique of the adaptationist pro-gramme.

Proceedings of the Royal Society of London

,

205B

, 581–598.Gould, S. J. & Vrba, E. S. (1982). Exaptation — a missing term in the

science of form.

Paleobiology

,

8

, 4–15.Grafen, A. (1988). On the uses of data on lifetime reproductive

success. In T. H. Clutton-Brock (Ed.)

Reproductive Success

(pp.454–471). Chicago: University of Chicago Press.

Grandcolas, P. & Deleporte, P. (1996). The origin of Protistansymbionts in termites and cockroaches: a phylogenetic analysis.

Cladistics

,

12

, 93–98.Grandcolas, P., Deleporte, P. & Desutter-Grandcolas, L. (1994).

Why to use phylogeny in evolutionary ecology?

Acta Oecologica

,

15

, 661–673.Grandcolas, P., Deleporte, P. & Desutter-Grandcolas, L. (1997a).

Testing evolutionary processes with phylogenetic patterns: testpower and test limitations.

Mémoires du Muséum national d’Histoirenaturelle

,

173

, 53–71.Grandcolas, P., Deleporte, P., Desutter-Grandcolas, L. &

Daugeron, C. (2001). Phylogenetics and ecology: as many charac-ters as possible should be included in the cladistic analysis.

Cladistics

,

17

, 104–110.Grandcolas, P., Minet, J., Desutter-Grandcolas, L., Daugeron, C.,

Matile, L. & Bourgoin, T. (1997b). Linking phylogenetic system-atics to evolutionary biology: toward a research program in bio-diversity.

Mémoires du Muséum national d’Histoire naturelle

,

173

,341–350.

Greene, H. W. (1986). Diet and arboreality in the Emerald Monitor,

Varanus prasinus

, with comments on the study of adaptation.

Fieldiana, Zoology

,

31

, 1–12.Harvey, P. H. & Pagel, M. D. (1991).

The Comparative Method inEvolutionary Biology

. Oxford: Oxford University Press.


•


490

Zoologica Scripta,

32


Kluge, A. G. (2001). Parsimony with and without justification.

Cladistics

,

17

, 199–210.Larson, A. & Losos, J. (1996). Phylogenetic systematics of adapta-

tion. In M. R. Rose & G. V. Lauder (Eds)

Adaptation

(pp. 187–220). San Diego: Academic Press.

Leroi, A. M., Rose, M. R. & Lauder, G. V. (1994). What does thecomparative method reveal about adaptation.

American Naturalist

,143, 381–402.

Lincoln, R. J., Boxshall, G. A. & Clark, P. F. (1982). A Dictionary ofEcology, Evolution and Systematics. Cambridge: Cambridge Univer-sity Press.

McLennan, D. A. (1991). Integrating phylogeny and experimentalethology: from pattern to process. Evolution, 45, 1773–1789.

Mickevich, M. F. & Weller, S. J. (1990). Evolutionary character analysis:tracing character change on a cladogram. Cladistics, 6, 137–170.

Nelson, G. F. (1970). Outline of a theory of comparative biology.Systematic Zoology, 19, 373–384.

O’Hara, R. J. (1992). Telling the tree: narrative representation andthe study of evolutionary history. Biology and Philosophy, 7, 135–160.

Packer, L. (1997). The relevance of phylogenetic systematics tobiology: examples from medicine and behavioral ecology.Mémoires du Muséum national d’Histoire naturelle, 173, 11–29.

Pagel, M. D. (1994). The adaptationist wager. In P. Eggleton &R. I. Vane-Wright (Eds) Phylogenetics and Ecology (pp. 29–51).Linnean Society Symposium Series. Number 17. London:Academic Press.

de Pinna, M. C. C. & Salles, L. O. (1990). Cladistic tests of adapta-tional hypotheses: a reply to Coddington. Cladistics, 6, 373–377.

Reeve, H. K. & Sherman, P. W. (1993). Adaptation and the goals ofevolutionary research. Quarterly Review of Biology, 68, 1–32.

Ridley, M. (1983). The Explanation of Organic Diversity. The Compar-ative Method and Adaptations for Mating. Oxford: Clarendon Press.

Schultz, T. R., Cocroft, R. B. & Churchill, G. A. (1996). The recon-struction of ancestral character states. Evolution, 50, 504–511.

Tattersall, I. & Eldredge, N. (1977). Fact, theory, and fantasy inhuman paleontology. American Scientist, 65, 204–211.

Tinbergen, N. (1951). The Study of Instinct. Oxford: Oxford Univer-sity Press.

Wanntorp, H. E. (1983). Historical constraints in adaptation theory:traits and non-traits. Oikos, 41, 157–160.

Wanntorp, H. E., Brooks, D. R., Nilsson, T. & Nylin, S. (1990).Phylogenetic approaches in ecology. Oikos, 57, 119–132.

Wenzel, J. W. (1992). Behavioral homology and phylogeny. AnnualReview of Ecology and Systematics, 23, 361–381.

Wenzel, J. W. & Carpenter, J. M. (1994). Comparing methods:adaptive traits and tests of adaptation. In P. Eggleton & R. I.Vane-Wright (Eds) Phylogenetics and Ecology (pp. 79–101). LinneanSociety Symposium Series. Number 17. London: Academic Press.

Westoby, M., Leishman, M. R. & Lord, J. M. (1995). On misinter-preting the ‘phylogenetic correction’. Journal of Ecology, 83, 531–534.

Williams, G. C. (1966). Adaptation and Natural Selection. Princeton:Princeton University Press.

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Testing adaptation with phylogeny: how to account for phylogenetic pattern and selective value together