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Phylogeny and Coadaptation of Thermal Physiology in Lizards: a Reanalysis Theodore Garland, Jr.; Raymond B. Huey; Albert F. Benn

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Phylogeny and Coadaptation of Thermal Physiology in Lizards: a Reanalysis Theodore Garland, Jr.; Raymond B. Huey; Albert F. Benn Phylogeny and Coadaptation of Thermal Physiology in Lizards: A Reanalysis Theodore Garland, Jr.; Raymond B. Huey; Albert F. Bennett Evolution, Vol. 45, No. 8 (Dec., 1991), 1969-1975. Stable URL: http://links.jstor.org/sici?sici=0014-3820%28199 112%2945%3A8%3C1969%3APACOTP%3E2.O.CO%3B2-S Evolution is currently published by Society for the Study of Evolution. Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.j stor.org/journals/ssevol.html. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is an independent not-for-profit organization dedicated to creating and preserving a digital archive of scholarly journals. For more information regarding JSTOR, please contact [email protected]. http://www.jstor.org/ Wed May 4 20:38:45 2005 Evolutron, 45(8), 199 I, pp. 1969-1975 PHYLOGENY AND COADAPTATION OF THERMAL PHYSIOLOGY IN LIZARDS: A REANALYSIS THEODOREGARLAND, JR., Department of Zoology, University of Wisconsin, Madison, WI 53706 USA RAYMONDB. HUEY, Department of Zoology, NJ-15, University of Washington, Seattle, WA 98195 USA AND ALBERTF. BENNETT Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine. CA 92717 USA Key words. -Australia, coadaptation, comparative method, lizard, phylogeny, physiology, Reptilia, sprint speed, thermal biology. Received December 3, 1990. Accepted April 9, 199 1 Traditional comparative studies examine evolution- for sprinting (To) (the body temperature at which an- ary associations of traits by comparing different spe- imals can run fastest) for 12 species of Australian skinks. cies, regardless of their phylogenetic relationships. A These values were compared to previously published problem with such an approach is that trait values for determinations for lower (CTMin) and upper (CTMax) each species are not statistically independent. This is critical temperatures for the species (Bennett and John- so because species partially share evolutionary histo- Alder, 1986). We applied two different analytical meth- ries(Felsenstein, 1985). Another problem is that "equi- ods. First, following suggestions by Clutton-Brock and librium" patterns seen among extant (or tip) species Harvey (1 984), we tested for correlations using generic may not be reflective of preceding evolutionary "trans- averages of traits (N = 6), because a nested ANOVA formations" (Lauder, 198 1). To help circumvent these by taxonomic level indicated that 9 1% of the variance difficulties, two of us (Huey and Bennett, 1987) de- in Tp occurred among genera. Second, to examine veloped a method to analyze the correlated evolution coadaptation in an historical framework, we developed of continuous traits within an explicitly phylogenetic a phylogenetic approach, overlaying the thermal data context. This method was developed specifically to ex- on a phylogeny of the six genera and applying a "min- amine "coadaptation" of physiolo~caland behavioral imum evolution" algorithm to estimate ancestral val- traits relating to the thermal biology of a group of Aus- ues at nodes. Coadaptation was again suggested by sig- tralian scincid lizards. Subsequently, Martins and Gar- nificant regressions involving inferred changes (most land (1 99 I) have used computer simulation to compare recent nodes to generic tips, N = 6) in To vs. Tp and the statistical properties of the Huey/Bennett approach, in CTMax vs. T,. and some improvements thereof, with those of tradi- Because both tests indicated significant positive cor- tional nonphylogenetic analyses, and of the indepen- relations between thermal preferences and measures of dent contrasts method of Felsenstein (1985). In addi- thermal sensitivity, we concluded that thermoregula- tion, new information on the relationships and tory behavior and physiology were at least partially divergence times of the Australian lizards in our orig- coadapted. This conclusion appeared robust because inal study has become available. We have therefore both tests appeared conservative: although 12 species reanalyzed our data according to this new information. were measured, only six generic averages or inferred Most of the previously significant correlations between changes (hence 4 degrees of freedom instead of 10) were traits have been altered, with implications not only for used for significance tests. However, new phylogenetic our own study but also for the design and interpretation information (Baverstock and Donnellan, 1990; Greer, of comparative studies in general. Our reanalysis is 1990, pers. comm.; Hutchinson et al., 199 1; S. C. Don- timely, because interest in phylogenetically based nellan, pers. comm.) suggests that there are closer to methods for analyzing comparative data has expanded three statistically independent taxa, not six (Fig. 1). rapidly since 1987 (e.g., Felsenstein, 1988; Bell, 1989; Moreover, new phylogenetic methods enable us to cal- Burt, 1989; Donoghue, 1989; Grafen, 1989; Lauder culate more accurate significance tests and better es- and Liem, 1989; Gittleman and Kot, 1990; Maddison, timates of evolutionary correlations (Felsenstein, 1985, 1990, 1991; Harvey and Pagel, 1991; Lynch, 1991). 1988; Grafen, 1989; Martins and Garland, 199 1). Huey and Bennett (1987) examined the hypothesis We apply three new analytical techniques: (I) simple that evolutionary changes in preferred body tempera- correlation analysis of species values, using empirical ture (T,) (determined in a laboratory thermal gradient) null distributions derived from computer simulation should be positively associated ("coadapted") with for significance testing (Martins and Garland, 199 I), evolutionary changes in functional thermal limits and rather than probabilities derived from conventional the thermal sensitivity of sprint running speed. To in- tests of correlation coefficients (e.g., Zar, 1984); (2) dex the latter, we estimated the optimal temperature revised minimum evolution analyses that estimate NOTES AND COMMENTS Sphenomorphus group Millions of Years Before Present FIG. I. Hypothesized phylogenetic relationships and estimated divergence times for 12 species of Australian scincid lizards (based on Baverstock and Donnellan, 1990; Greer, 1990, pers. comm.; Hutchinson et al., 199 1; S. C. Donnellan, pers. comm.). For purposes of phylogenetic analyses of thermal data, species trichotomies within Ctenotus and Sphenomorphus were resolved by assuming that species closer in To(conceptually, the independent variable) were also closer phylogenetically. This assumption has a loose parsimony justification (Pagel, manuscript : cf Felsenstein, 1983). Absolute timing of the divergence of the Egernia-Leiolopisma group from the Sphenomorphus group (60 million years) and the diversification within the Sphenomorphus group (10 million years) is based on immunological distance and a molecular clock assumption (Baverstock and Donnellan, 1990; S. C. Donnellan, pers. comm.). Timing of the split between Egernia and Leiolopisma groups is assumed, based on the fact that morphological analyses (Greer, 1990, pers. comm.) indicate Egernia and Leiolopisma as sister taxa, whereas immunological data do not resolve the Egernia-Leiolopisma-Sphenomorphus group tri- chotomy. Species within a genus (Sphenomorphus, Hemiergis, Leiolopisma) were arbitrarily assumed to have diverged one million years ago, except for the three Ctenotus, which are in different species groups (Greer, 1990) and so were assumed to have split at two million year intervals. Timing of other splits is arbitrary. whether inferred changes in traits are correlated along with N - 2 = 10 df indicate that correlations greater branches (Martins and Garland, 199 I), and (3) inde- than +0.497 (I-tailed) are significant at a < 0.05 (see pendent contrasts methods (Felsenstein, 1985, 1988; Zar's, 1984, Table B. 16). (One-tailed tests are appro- Grafen, 1989). These three approaches generally yield priate for the stated hypothesis of positive coadapta- the conclusion that the original analyses-though in- tion of thermal variables.) Judged in this way, three of tended to be conservative-were not conservative six intercorrelations are significant [T,with To (r = enough, such that evidence for coadaptation of some 0.585) and CTMax (r = 0.885), and To with CTMax traits is weaker than previously thought. (r = 0.6 19)], suggesting coadaptation between behavior and thermal sensitivity. Huey and Bennett (1987), working with generic averages, found similar patterns Simple Correlation Analysis of significance. Thermal data and hypothesized phylogenetic rela- The foregoing significance tests make no attempt to tionships ofthe 12 species studied by Huey and Bennett correct for phylogenetic nonindependence and there- (1 987) are given in Table 1 and Figure 1, respectively. fore tend to overestimate the significance of correla- [Huey and Bennett (1987) also used a generic mean tions (Felsenstein, 1985; Grafen, 1989; Martins and value for Mabuya for T,, CTMax, and CTMin. As no Garland, 199 1).
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