Comment on “How the Horned Lizard Got Its Horns”

ecently, Young et al. (1) purported toidentify the mechanism behind the originand maintenance of horns in horned lizards(Phrynosomatidae: Phrynosoma)bydemon-strating directional selection for increasinghorn length in one population of Phrynosomamcalli from the southwestern United States. Indrawing their conclusions, Young et al.asserted rather than demonstrated the currentfunction of the trait of interest (that is, theyassumed that horns are an antipredatory de-fense mechanism). In addition, Young et al.assumed that current function reflects pastselection. In doing so, they have failed torecognize the crucial distinction betweenadaptation and exaptation (2, 3). Thesecriticisms could have been avoided had theauthors given due consideration to the phylo-genetic definition of adaptation (3–5), whichuses robust criteria for identifying adaptation.Numerous definitions of adaptation havebeen proposed, including adaptation as aprocess and adaptation as a state of being (thatis, current utility and current fitness). Neitherdefinitionacknowledgesthehistoricalaspectofadaptation(2). An adaptation is any feature ofan organism that enhances current fitness andwhose modification was a result of selectionfor its current role. Incontrast,anexaptationisa trait that has current utility but that did notarise as a result of selection for its current role(2, 3). Inthisview,anadaptationisastatementabout the origin and maintenance of a trait.Brandon (4)suggestedfourcriterianecessarytoidentify adaptation in this operational frame-work: 1) evidence that selection has occurred onthetraitinquestion,2)existenceofafunctionalexplanation for putative fitness differencesassociated with the trait, 3) evidence forheritability of phenotypic differences corre-sponding to trait variation, and 4) knowledgeof phylogeny such that putative adaptations canbeshowntohaveoriginatedinselectiveregimesin which they are currently advantageous.The explanation provided by Young et al.for the origin and maintenance of large hornsin Phrynosoma satisfies potentially only oneof the criteria cited above. Their data showthat for one population, lizards with propor-tionally shorter horns for their body sizeexperience a higher probability of mortalityfrom one predator, loggerhead shrikes (Laniusludovicianus), than do lizards with propor-tionally longer horns (criterion 1). Althoughthey provide no evidence for heritability ofhorn length (criterion 3), assuming rather thanmeasuring heritability is a common practice instudies of adaptation, and we do not criticizethe authors on this rather strict criterion. Moreimportant, they argue that horns protect P.mcalli from predation by shrikes but provideno direct evidence of this (criterion 2). Unlikesnakes that ingest the entire lizard, shrikesimpale horned lizards on branches and do notingest the spiny head (1). Because thepredatory event does not involve ingestion ofthe head, the functional significance of a 10%difference in size-adjusted horn length to ashrike is not at all clear. Currently, horns mayfunction as an antipredator defense mecha-nism in P. mcalli;however,suchafunctionhas not been demonstrated in the context ofpredation by shrikes or any other organism.Moreover, many animals are known to preyon horned lizards, including other lizards,snakes, mammals, and birds (6–8). Theauthors relied on finding the carcasses ofimpaled lizards with heads intact, but becauselizards ingested by other predators were notobserved (and thus their horn lengths couldnot be measured), the relative strength ofselection on horn length in P. mcalli byshrikes (or any other predator) is unknown.The use of size-adjustedhorn lengthis alsoproblematic. Avian and mammalian predatorsneed not consume the head of horned lizards.Snakes and lizards, on the other hand, gener-ally cannot dismember their prey and mustconsume the entire prey item. Consequently,they are gape-limited predators. For suchpredators, absolute rather than proportional orsize-adjusted horn length likely determineswhether the head can be ingested. Risk ofinjury resulting from attempts to swallow thehead of horned lizards may deter such preda-tors. However, that risk is likely the result ofhorn configuration (e.g., orientation and abso-lute size) rather than proportional length. Wealso note that inferring the functional impor-tanceofatraitbasedonevidenceofdirectionalselectionisadhoc.Inthecaseofhornedlizardsand loggerhead shrikes, behavioral tests andobservations of the putative function areneeded to support the claim that horn length(especially size-adjusted horn length) directlyaffects predation by shrikes.Finally, even if the current functional roleofa traitisknown, the questionoftheoriginofthis trait remains unanswered, which leads tocriterion 4 of the phylogenetic definition ofadaptation. Without additional evidence, anytrait whose current function is advantageous(i.e., affects current fitness) is equally likely tohave been coopted for its current function(exaptation) as selected for its current function(adaptation). To distinguish adaptation fromexaptation, some knowledge of phylogenetichistory coupled with a reconstruction of pastselective regimes is needed. Young et al.address neither of these issues and, in theabsence of proper phylogenetic analyses(3, 5), their conclusions remain speculative.For example, it is plausible that horns arosein the context of sexual selection or crypsis(9, 10)andonlylaterfunctionedindefenseagainst predators. The data of Younget al.cannot refute either of these alternativehypotheses. Inability or failure to distinguishbetween these two alternative hypotheses isthe essence of Bjust-so stories[ (11)andisprecisely what prompts criterion 4 of thephylogenetic definition of adaptation.The elaborate horny protrusions on theskulls of horned lizards are a synapomorphyof this monophyletic clade (12, 13) thatnaturally lead to questions concerning theorigin and maintenance of this conspicuoustrait. Although we agree with Young et al.that the origin and maintenance of horns inPhrynosoma is a question of much interest,we argue that the explanation they haveprovided fails to meet the criteria for iden-tifying adaptation and ignores three decadesof discussion of the problems associated withthe adaptationist paradigm. Therefore, thequestion implied in the title of their article—how the horned lizard got its horns—remainsunanswered and, in the absence of anhistorical perspective, is unanswerable.Salvatore J. AgostaArthur E. DunhamDepartment of BiologyUniversity of PennsylvaniaPhiladelphia, PA 19104, USAE-mail: agosta@sas.upenn.edu;adunham@sas.upenn.edu