Emília P. Martins

PHYLOGENETIC ANALYSES OF THE CORRELATED EVOLUTION OF CONTINUOUS CHARACTERS: A SIMULATION STUDY

We use computer simulation to compare the statistical properties of several methods that have been proposed for estimating the evolutionary correlation between two continuous traits, and define alternative evolutionary correlations that may be of interest. We focus on Felsensteins (1985) method and some variations of it and on several “minimum evolution” methods (of which the procedure of Huey and Bennett [1987] is a special case), as compared with a nonphylogenetic correlation. The last, a simple correlation of trait values across the tips of a phylogeny, virtually always yields inflated Type I error rates, relatively low power, and relatively poor estimates of evolutionary correlations. We therefore cannot recommend its use. In contrast, Felsensteins (1985) method yields acceptable significance tests, high power, and good estimates of what we term the input correlation and the standardized realized evolutionary correlation, given complete phylogenetic information and knowledge of the rate and mode of character change (e.g., gradual and proportional to time [“Brownian motion”] or punctuational, with change only at speciation events). Inaccurate branch length information may affect any method adversely, but only rarely does it cause Felsensteins (1985) method to perform worse than do the others tested. Other proposed methods generally yield inflated Type I error rates and have lower power. However, certain minimum evolution methods (although not the specific procedure used by Huey and Bennett [1987]) often provide more accurate estimates of what we term the unstandardized realized evolutionary correlation, and their use is recommended when estimation of this correlation is desired. We also demonstrate how correct Type I error rates can be obtained for any method by reference to an empirical null distribution derived from computer simulations, and provide practical suggestions on choosing an analytical method, based both on the evolutionary correlation of interest and on the availability of branch lengths and knowledge of the model of evolutionary change appropriate for the characters being analyzed. Computer programs that implement the various methods and that will simulate (correlated) character evolution along a known phylogeny are available from the authors on request. These programs can be used to test the effectiveness of any new methods that might be proposed, and to check the generality of our conclusions with regard to other phylogenies.

TRANSLATING BETWEEN MICROEVOLUTIONARY PROCESS AND MACROEVOLUTIONARY PATTERNS: THE CORRELATION STRUCTURE OF INTERSPECIFIC DATA

As species evolve along a phylogenetic tree, we expect closely related species to retain some phenotypic similarities due to their shared evolutionary histories. The amount of expected similarity depends both on the hierarchical phylogenetic structure, and on the specific magnitude and types of evolutionary changes that accumulate during each generation. In this study, we show how models of microevolutionary change can be translated into the resulting macroevolutionary patterns. We illustrate how the structure of phenotypic covariances expected in interspecific measurements can be derived, and how this structure depends on the microevolutionary forces guiding phenotypic change at each generation. We then explore the covariance structure expected from several simple microevolutionary models of phenotypic evolution, including various combinations of random genetic drift, directional selection, stabilizing selection, and environmental change, as well as models of punctuated or burst‐like evolution. We find that stabilizing selection leads to patterns of exponential decrease of between species covariance with phylogenetic distance. This is different from the usual linear patterns of decrease assumed in most comparative and systematic methods. Nevertheless, linear patterns of decrease can result from many processes in addition to random genetic drift, such as directional and fluctuating selection as well as modes of punctuated change. Our framework can be used to develop methods for (1) phylogenetic reconstruction; (2) inference of the evolutionary process from comparative data; and (3) conducting or evaluating statistical analyses of comparative data while taking phylogenetic history into account.

Adaptation and the comparative method

Over the past two decades, it has become widely accepted that phylogenies need to be incorporated into statistical analyses of interspecific data. However, recent debate has focused on whether it is appropriate to apply phylogenetic comparative methods (PCMs) to the study of adaptation. Although some of the criticisms are serious, it is premature to stop applying PCMs altogether. New statistical methods designed explicitly for the comparative study of adaptation overcome these criticisms and offer fresh insights into the evolution of phenotypes.

ADAPTIVE CONSTRAINTS AND THE PHYLOGENETIC COMPARATIVE METHOD: A COMPUTER SIMULATION TEST

Abstract Recently, the utility of modern phylogenetic comparative methods (PCMs) has been questioned because of the seemingly restrictive assumptions required by these methods. Although most comparative analyses involve traits thought to be undergoing natural or sexual selection, most PCMs require an assumption that the traits be evolving by less directed random processes, such as Brownian motion (BM). In this study, we use computer simulation to generate data under more realistic evolutionary scenarios and consider the statistical abilities of a variety of PCMs to estimate correlation coefficients from these data. We found that correlations estimated without taking phylogeny into account were often quite poor and never substantially better than those produced by the other tested methods. In contrast, most PCMs performed quite well even when their assumptions were violated. Felsensteins independent contrasts (FIC) method gave the best performance in many cases, even when weak constraints had been acting throughout phenotypic evolution. When strong constraints acted in opposition to variance-generating (i.e., BM) forces, however, FIC correlation coefficients were biased in the direction of those BM forces. In most cases, all other PCMs tested (phylogenetic generalized least squares, phylogenetic mixed model, spatial autoregression, and phylogenetic eigenvector regression) yielded good statistical performance, regardless of the details of the evolutionary model used to generate the data. Actual parameter estimates given by different PCMs for each dataset, however, were occasionally very different from one another, suggesting that the choice among them should depend on the types of traits and evolutionary processes being considered. Corresponding Editor: J. Huelsenbeck

The Phylogenetic Mixed Model

The phylogenetic mixed model is an application of the quantitative‐genetic mixed model to interspecific data. Although this statistical framework provides a potentially unifying approach to quantitative‐genetic and phylogenetic analysis, the model has been applied infrequently because of technical difficulties with parameter estimation. We recommend a reparameterization of the model that eliminates some of these difficulties, and we develop a new estimation algorithm for both the original maximum likelihood and new restricted maximum likelihood estimators. The phylogenetic mixed model is particularly rich in terms of the evolutionary insight that might be drawn from model parameters, so we also illustrate and discuss the interpretation of the model parameters in a specific comparative analysis.

Estimating the Rate of Phenotypic Evolution from Comparative Data

This study presents a method to estimate rates of evolutionary change in continuous characters from comparative data. The technique is similar to those introduced previously in which between-species divergence is estimated as a function of time since divergence but also takes into account the possible statistical nonindependence of trait values measured from phylogenetically related species in an approach similar to the independent contrasts methods used in interspecific data analysis. The use of Ornstein-Uhlenbeck processes is also proposed to extend the standard Brownian motion model of evolutionary change and to allow for tests of neutral evolution versus evolution under stabilizing selection. Applications of the method to test specific hypotheses of phenotypic evolution (including the adequacy of Brownian motion to describe real data), to compare rates of change of different types of characters or different groups of organisms, and to estimate branch lengths in units of expected variance of change as required by most comparative-method data analysis techniques are discussed.

PHYLOGENIES, SPATIAL AUTOREGRESSION, AND THE COMPARATIVE METHOD: A COMPUTER SIMULATION TEST

Brownian motion computer simulation was used to test the statistical properties of a spatial autoregressive method in estimating evolutionary correlations between two traits using interspecific comparative data. When applied with a phylogeny of 42 species, the method exhibited reasonable Type I and II error rates. Estimation abilities were comparable to those of independent contrasts and minimum evolution (parsimony) methods, and generally superior to a traditional nonphylogenetic approach (not taking phylogenies into account at all). However, the autoregressive method performed extremely poorly with a smaller phylogeny (15 species) and with nearly independent (“star”) phylogenies. In both of these situations, any phylogenetic autocorrelation present in the data was not detected by the method. Results show how diagnostic techniques (e.g., Morans I) can be useful in detecting and avoiding such situations, but that such techniques should not be used as definitive evidence that phylogenetic correlation is not present in a set of comparative data. The correction factor (α) proposed by Gittleman and Kot (1990) for use in weighting phylogenetic information had little effect in most analyses of 15 or 42 species with incorrect phylogenetic information, and may require much larger sample sizes before significant improvement is shown. With the sample sizes tested in this study, however, the autoregressive method implemented with this correction factor and correct phylogenetic information led to downwardly biased estimates of the absolute magnitude of the evolutionary correlation between two traits. Cautions and recommendations for implemention of the spatial autoregressive method are given; computer programs to conduct the analyses are available on request.

The effects of early and adult social environment on zebrafish (Danio rerio) behavior

Because early social experience can have a profound effect on later mate and social choices, the availability of options and decisions made early in development can have major effects on adult behavior. Herein, we use strain differences among zebrafish, Danio rerio, as an experimental tool to test the effects of social experience on behavior. By manipulating the strain composition of groups in which the subject fish are housed at different ages, we tested (1) whether mixing with dissimilar individuals influenced subsequent behavior, (2) whether prolonged mixing during the juvenile stage had a more pronounced effect than a shorter period of mixing during adulthood and (3) whether mixing had a lasting effect after animals were resorted into groups of same strain animals. We found that social experience had a profound impact on social behavior. Both Nadia and TM1 individuals engaged in more frequent biting after having been in mixed strain groups compared to pure strain groups. This was true of groups mixed as juveniles, as well as adults, indicating that this response was not dependent on exposure during a critical developmental period. Also, TM1 fish (but not Nadia) having recently been housed in mixed-strain groups were more willing to leave the immediate vicinity of a shoal than were TM1 fish raised in pure strain groups. This change was more pronounced in groups mixed as juveniles than as adults. In addition, the observed changes persisted after mixed groups were separated into pure strain groups for a month. Other behavioral measures including Activity Level, Predator Response and Stress Recovery were unaffected by previous social experience.

A Comparative Study of the Evolution of Sceloporus Push-Up Displays

Comparative studies are often used to infer the evolutionary histories of phenotypic traits. In this study, hypotheses suggesting that the evolution of Sceloporus push-up displays was constrained by the evolution of body size and the adoption of an arboreal lifestyle are tested with data from the literature on the push-up displays of 42 species of Sceloporus lizards and several phylogenetic comparative method techniques including independent contrasts, inferred changes, and spatial autocorrelation methods. Comparisons are made among the various phylogenetic analysis techniques and ways of modeling evolutionary change. Results suggest that components of display structure have evolved together and that the correlated evolution of display structural components has had a greater impact on the evolution of Sceloporus pushup displays than relationships between evolutionary changes in display structure and body size or display structure and microhabitat use. Increases in the complexity or communicative flexibility of Sceloporus push-up displays have been attained through altering the shape or type of head bob produced and the number of head bobs. A negative correlation between the two types of variation suggests that there is a limit or optimal length to these displays

Combining motions into complex displays : playbacks with a robotic lizard

Complex displays composed of multiple, seemingly independent, units can result from sexual selection for increasingly variable, but redundant, displays and from potentially opposing selective pressures imposed by use of the display in multiple contexts. Our playback results support the latter, multireceiver hypothesis by confirming that two aspects of the sagebrush lizard headbob display (number of headbobs and use of display-specific body postures) are independently-meaningful components that are interpreted differently by different receivers. Male receivers use species-typical body postures to distinguish between aggressive and broadcast forms of the display, whereas female receivers are more attentive to the number of headbob motions, using these to distinguish male courtship from a challenge from a female competitor. Thus, display components are likely subject to different selective pressures and the display as a whole is evolving in response to a complex selective regime. Our example differs from other complex signals that have been considered in that both display elements involve dynamic motions (turned on and off by the display producer) as opposed to static signal elements (e.g., color, size). In addition, we found evidence that display structure is highly malleable, and that lizards both produce and respond to artificial displays that violate syntactic rules identified from field observations. Finally, our experiments demonstrate that a robotic lizard can be used effectively in playback studies of visual display behavior in lizards.