Studies of organismal form and function rely on multipletypes of scientific investigation, including theory, description,experimentation and comparison. Comparing species is anancient human enterprise, done for a variety of reasons(Sanford et al., 2002). Since Charles Darwin, the ‘comparativemethod’ – comparing populations, species or higher taxa – hasbeen the most common and productive means of elucidatingpast evolutionary processes (Harvey and Pagel, 1991; Brooksand McClennan, 2002). Comparative methods have been usedextensively to infer evolutionary adaptation, that is, changes inresponse to natural selection (for alternate physiologicalmeanings of ‘adaptation’, see Garland and Adolph, 1991;Bennett, 1997). They are most often promoted and criticized(e.g. Leroi et al., 1994) within this context. However,comparative methods are not used to infer adaptation alone(Garland and Adolph, 1994; Sanford et al., 2002), but are alsoemployed to analyze the effects of sexual selection (e.g.Hosken et al., 2001; Nunn, 2002; Smith and Cheverud, 2002;Aparicio et al., 2003; Cox et al., 2003), which may benonadaptive or even maladaptive with respect to naturalselection. These methods can also be used to compare rates ofevolution across clades or the amount of morphospaceoccupied by clades or by ecologically defined groups (Garland,1992; Clobert et al., 1998; Ricklefs and Nealen, 1998; Garlandand Ives, 2000; Hutcheon and Garland, 2004; McKechnie andWolf, 2004). Of particular interest for the present review, theyare also widely used to explore trade-offs (e.g. Clobert et al.,1998; Vanhooydonck and Van Damme, 2001) and to examinefunctional (mechanistic) relationships among traits (e.g.Lauder, 1990; Iwaniuk et al., 1999; Mottishaw et al., 1999;Autumn et al., 2002; Hale et al., 2002; Gibbs et al., 2003;Johnston et al., 2003; Herrel et al., 2005), including allometricscaling with body size (e.g. Garland, 1994; Reynolds and Lee,1996; Williams, 1996; Clobert et al., 1998; Garland and Ives,2000; Nunn and Barton, 2000; Herrel et al., 2002; Perry andGarland, 2002; Rezende et al., 2002, 2004; Schleucher andWithers, 2002; McGuire, 2003; Al-kahtani et al., 2004;McKechnie and Wolf, 2004; Muñoz-Garcia and Williams, inpress).Comparative methods have been radically restructured overthe past two decades, and now routinely incorporate bothphylogenetic information and explicit models of character3015The Journal of Experimental Biology 208, 3015-3035Published by The Company of Biologists 2005doi:10.1242/jeb.01745Over the past two decades, comparative biologicalanalyses have undergone profound changes with theincorporation of rigorous evolutionary perspectives andphylogenetic information. This change followed in largepart from the realization that traditional methods ofstatistical analysis tacitly assumed independence of allobservations, when in fact biological groups such asspecies are differentially related to each other according totheir evolutionary history. New phylogenetically basedanalytical methods were then rapidly developed,incorporated into ‘the comparative method’, and appliedto many physiological, biochemical, morphological andbehavioral investigations. We now review the rationale forincluding phylogenetic information in comparative studiesand briefly discuss three methods for doing this(independent contrasts, generalized least-squares models,and Monte Carlo computer simulations). We discuss whenand how to use phylogenetic information in comparativestudies and provide several examples in which it has beenhelpful, or even crucial, to a comparative analysis. We alsoconsider some difficulties with phylogenetically basedstatistical methods, and of comparative approaches ingeneral, both practical and theoretical. It is our personalopinion that the incorporation of phylogeny informationinto comparative studies has been highly beneficial, notonly because it can improve the reliability of statisticalinferences, but also because it continually emphasizes thepotential importance of past evolutionary history indetermining current form and function.Key words: allometry, comparative method, evolutionary physiology,model of evolution, phylogeny, statistical analysis.SummaryCommentaryPhylogenetic approaches in comparative physiologyTheodore Garland, Jr1, Albert F. Bennett2,* and Enrico L. Rezende11Department of Biology, University of California, Riverside, CA 92521, USA and 2Department of Ecology andEvolutionary Biology, University of California, Irvine, CA 92697, USA*Author for correspondence (e-mail: [email protected])Accepted 13 June 2005IntroductionTHE JOURNAL OF EXPERIMENTAL BIOLOGYevolution. Indeed, Sanford et al. (2002) suggest that this newemphasis be termed the ‘comparative phylogenetic method’.As outlined in Blomberg and Garland (2002), this revolutionin comparative phylogenetic methodology followed fromseveral conceptual advances: (1) adaptation should not becasually inferred from comparative data; (2) the incorporationof phylogenetic information increases both the quality andeven the type of inference from comparative data alone; (3)because all organisms are differentially related to each other,taxa cannot be assumed to be independent of each other forstatistical purposes; (4) statistical analyses of comparative datamust assume some model of character evolution for effectiveinference; (5) taxa used in comparative analyses should bechosen in regard to their phylogenetic affinities as well as thearea of functional investigation; and (6) even phylogeneticallybased comparisons are purely correlational and inferences ofcausation drawn from them can be enhanced by otherapproaches, including experimental manipulations.To expand on some of these points, ‘quality’ in point 2includes the simple fact that adding an independent estimate ofphylogenetic relationships to a comparative analysis increases– often greatly – the amount of basic data that is brought tobear on a given question, whereas ‘type’ refers to analyses thatare simply impossible without a phylogenetic perspective, suchas reconstructing ancestral values or comparing rates ofevolution among lineages. Although phylogenetic informationand a suitable analytical method may allow any comparativedata set to be ‘rescued’ from phylogenetic nonindependence(e.g. avoid inflated Type I error rates; point 3),phylogenetically informed choice of species (point 5) canaccomplish more, such as actually increasing statistical powerto
View Full Document
Unlocking...