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Home , Basal (phylogenetics), Lineage (evolution), Phylogenetics, Polytomy

I.16 and Comparative Methods David D. Ackerly

OUTLINE GLOSSARY 1. The role of phylogenetics in See figure 1 for illustrations of main terms. 2. Phylogenies and the analysis of trait correlations branch lengths. These may indicate either the number 3. Phylogenetic signal: Pattern and significance of inferred character changes or a measure of rela- 4. Phylogenetics and community ecology tive or absolute time along any particular branch 5. Prospects for the future connecting two nodes. If the molecular data un- derlying a phylogeny do not violate a molecular The study of ecology frequently draws on comparative ob- clock, a single rate may be imposed such that branch servations and experiments that rely on the similarities lengths will represent relative time, and contem- and differences among and the correlations among poraneous taxa will be placed at the same distance species traits and the environment. In such studies, con- from the root (i.e., the same age). If a molecular sideration of the phylogenetic relationships among species clock is violated, rate-smoothing methods have provides valuable information for statistical inference and an been developed to obtain the best-supported esti- understanding of evolutionary history underlying present- mate of relative time. and biogeographic or day ecological patterns. From a statistical perspective, re- paleoecological information may then be used to lated species do not necessarily provide independent data calibrate these branch lengths and convert them to points for hypothesis tests, due to inheritance of shared char- units of absolute time. Rate-smoothing and cali- acteristics from common ancestors. This similarity can be bration methods are fraught with difficulty, and addressed through a variety of statistical techniques, in- branch lengths should be treated with caution. cluding the widely used method of phylogenetic independent (Note that branch lengths may also be set arbitrarily contrasts. Independent contrasts play a particularly valuable for convenience when one is drawing trees, in which role in the analysis of trait and trait–environment corre- case they have no intrinsic biological meaning.) lations and may point toward alternative interpretations of character states. Phylogenetic trees are reconstructed comparative data. In community ecology, measures of the based on analysis of a matrix of characters,where phylogenetic clustering or spacing of co-occurring species each character can take on one of two or more provide a useful tool to test alternative processes underlying states (binary or multistate, respectively) for each community assembly. Co-occurrence of close relatives most in the group. Phylogenies can be reconstructed likely reflects ecological filtering, in which related species from molecular and/or morphological data, although with similar traits share the ability to tolerate local condi- the former are now much more common. Analyses tions. The reverse pattern of phylogenetic spacing of co- that include morphological data are advantageous as occurring species may reflect a variety of processes, and they make it possible to incorporate taxa or fossils additional observations of species traits in relation to envi- for which molecular data are not available. ronment and interacting taxa will be necessary to address . This refers to a single line of ancestor–descendant underlying processes. Use of comparative methods has in- relationship, connecting nodes within a phylogeny. creased dramatically with the rapid growth in phylogenetic most recent common ancestor (MRCA). The MRCA is information and computing power and will continue to play the most recent node that is shared by any two taxa an important role in ecological research. in a tree. 118 Autecology

branch In Great Britain there are 32 indigenous trees[:] node of these 19 or more than half ...have their sexes A separated—an enormous proportion compared with the remainder of the British flora: nor is this B wholly owing to a chance coincidence in some C one having many trees & having a ten- dency to separated sexes: for the 32 trees belong D terminal taxa to nine Families, & the trees with separate sexes (’tips’) to five Families. E MRCA of —Charles , manuscript for Natural root or F and G F Selection (unpublished) node G H In the quote above, Darwin observes an interesting pattern among plant species of Great Britain. He notes containing that among trees, the proportion of species that have species E, F, G, and H individuals of separate sexes (as in and most Figure 1. Example of a for eight taxa (A–H), illus- ) is much higher than among the flora as a trating some of the terms in the glossary. This tree is ultrametric, meaning that all terminal taxa are equidistant from the root of the whole, most of which is composed of shrubs and her- tree. baceous plants. He explained the high frequency of separate sexes as an to promote cross- fertilization in trees: because trees are large and have phylogenetic distance. The phylogenetic distance be- many flowers, the chance that an would carry tween two nodes or taxa refers to the sum of branch pollen from one flower to another of the same indi- lengths from one tip (or internal node) down to the vidual is quite high. If all the flowers on a tree are of the MRCA and back up to another tip (or node) of a same sex, these repeated visits by pollinators will not tree. The phylogenetic distance matrix is an nn lead to high levels of self-fertilization. matrix (for n taxa) of such distances among all Darwin’s observations provide a nice example of pairs of taxa, with 0s in the diagonal. what we now call comparative , which draws phylogeny. A phylogeny, or phylogenetic tree, is a on comparisons of the similarities and differences branching diagram showing the hierarchy of evo- among species to test ecological and evolutionary hy- lutionary relationships among a group of taxa (ex- potheses. In addition, what Darwin recognized intui- tant and/or extinct). Terminal taxa or tips are tively is that a simple count of the number of species connected by branches to internal nodes that in- exhibiting different characteristics might not be ade- dicate a hypothesized ancestor. A clade includes all quate to support his argument. If many of the species of the taxa (extant and extinct) that descend from a are drawn from the same family (that is, closely related node. Phylogenies can be either rooted or un- in evolutionary terms), they are likely to share many rooted, where the root represents the hypothesized ecological characteristics. Thus, a group with many ancestor of all taxa on the tree. tree species may also contain many species with sepa- polytomy. This refers to a node with three or more rate sexes, reflecting their descent from a common daughter nodes. A soft polytomy indicates uncer- ancestor. But if the evolutionary argument is sound— tainty, where the true bifurcating relationships that trees should evolve separate sexes because of the among the daughters are unknown. A hard poly- problem of self-fertilization—then this combination of tomy represents a hypothesis of near simultaneous traits should evolve independently in many different divergence where the sequence of individual speci- taxonomic groups, and this is indeed what Darwin ation events cannot be meaningfully resolved. Most observed. phylogenetic comparative methods treat Throughout the past 150 years, since the publica- as either hard or soft but do not always make the tion of Darwin’s , comparative distinction explicit. biology has played a central role in ecology and evo- ultrametric. An ultrametric tree is one in which all lutionary biology. In essence, each species alive today terminal taxa are contemporaneous; more precisely, (or in the past) represents the outcome of a long, nat- the sum of the branch lengths from the root to each ural experiment. The results reflect the contemporary tip is the same for all tips. Phylogenies of extant taxa ecology of a species—interactions with the abiotic en- will be ultrametric if branch lengths have been ad- vironment and with other forms of —as well as the justed to represent relative or absolute time. cumulative legacy of the past. works slowly, Phylogenetics 119 and most features are passed down from ancestor to win’s example above) and the study of community descendant with little change. A appears beau- ecology. In addition, I provide a brief discussion of the tifully adapted to the challenges of surviving and re- concept of phylogenetic signal, a general term for the producing under the extreme conditions of Antarctic similarity among close relatives. life. But these must be understood in his- In the discussion below, it is assumed that a phy- torical context: are , and this experiment logeny is available for each group under consideration. in polar living started with very specific initial condi- Most phylogenies are based on molecular data, par- tions, including egg-laying, a feathered pelt, forelimbs ticularly DNA sequences, sometimes combined with modified into wings, and so on. Comparative research, morphological or other characteristics. The computa- placing penguins in the broader context of other birds tional methods used to search for the best-supported and viewing them side by side with their closest rela- phylogeny are continually being improved and are tives (, albatrosses, petrels, and shearwaters) is beyond the scope of this chapter. Regardless of the critical to an understanding and appreciation of their method used, it is important to recognize that every contemporary ecology and behavior. phylogeny is a hypothesis of relationships, and like any In the past 30 years, has grown scientific hypothesis, it is subject to revision and im- rapidly as a new generation of methods emerged, com- provement. Phylogenies may also contain different de- bining the historical perspective outlined above with grees of uncertainty, both in terms of the topology (the the quantitative tools of experimental statistics. The pattern of who is related to whom) and the lengths of emergence of modern phylogenetics triggered these the branches, which represent the amount of evolu- developments. The word phylogeny refers to the evo- tionary change or the amount of time elapsed between lutionary relationships among a group of , different nodes of the tree. This uncertainty can be illustrated as a branching tree where the tips (or leaves) incorporated into comparative analyses; in many cases, may represent individuals, populations, species, or the results are quite robust across a range of possible groups of species, and the internal branching points are alternatives, so strongly supported and fully resolved their common ancestors. The study of phylogenetics phylogenies are not a prerequisite for comparative has been revolutionized by the combination of molec- analysis. An overview of some terminology used to ular biology (providing a trove of data), conceptual describe phylogenies is provided in the Glossary. advances (the theory of ), and the availabil- ity of high-speed computers. Together, these advances 2. PHYLOGENIES AND THE ANALYSIS OF TRAIT have made it possible to infer highly resolved phylog- CORRELATIONS enies for many groups of organisms. With continuous improvements in methods and the availability of data, Research in functional ecology, life history strategies, the is taking shape and revealing the hier- and related areas of ecology often addresses questions archy of evolutionary relationships among living (and of interspecific trait–trait and trait–environment asso- extinct) organisms. ciations, such as: Do with larger body sizes have larger home ranges? Do plant species of open habitats tend to have smaller seeds? How are the traits 1. THE ROLE OF PHYLOGENETICS IN ECOLOGY of invasive species different from those of native species The science of ecology studies the interactions of or- in a community? The answers to these questions help ganisms with their environment and the consequences us to understand how species traits influence distribu- of these interactions for where species live and how tion, abundance, and interactions with other species in they interact. To address these questions, it is often a community. They also have important applications useful to compare different species, either through ob- in , restoration ecology, and the servations or experiments. The similarities and differ- management of invasive species. ences in how species respond to their environment or A variety of statistical methods can be applied to interact with each other can provide important eco- test hypotheses of trait associations, depending on the logical insights. When data are gathered on different type of data available and the of the hypothesis. species, understanding how they are related to each These include correlation, regression, analysis of vari- other (i.e., their phylogenetic relationships) contributes ance, contingency table analysis, and others. One of the valuable information that can affect data analysis and basic assumptions of virtually all statistical tests is that interpretation. In this chapter, I focus on two areas of each data point represents an observation that is in- ecological research where phylogenies play a particu- dependent with respect to the underlying null hypoth- larly important role: the analysis of correlations among esis. This assumption is not required in to species traits and environmental conditions (like Dar- calculate the various statistics; rather, it is essential to 120 Autecology deriving the statistical significance of the outcome. For widely used of all comparative methods. The method conventional statistics, this significance value (or p- of independent contrasts rests on the assumption that value) represents the probability of observing the data the evolutionary change in a trait that occurs along if the underlying null hypothesis is true. When that each lineage leading up to present-day species repre- probability is too low (conventionally, we use a cutoff sents an independent event with respect to the changes value of 5%), we reject the null hypothesis and accept occurring in other branches. Independence, in this that there is a significant effect or relationship. For context, refers to the statistical notion that the changes maximum-likelihood tests, which are playing an in- are independent manifestations of underlying pro- creasingly important role in ecology and comparative cesses, although the same processes (e.g., natural se- methods, the assumption of independence is used to lection as a result of climate change) may be affecting assess the likelihood of the best-fit model relative to multiple lineages in a group. If the trait changes that alternative models or hypotheses, given the observed occur in two lineages arising from a common ancestor data. are independent, then, as Felsenstein demonstrated The fundamental argument underlying the devel- based on statistical theory, the difference between the opment of many comparative methods arises from the trait values of the two descendants will also represent a observation that related species are ecologically and statistically independent observation. These differences phenotypically similar to one another. This will not are calculated by subtracting the trait value of one hold for every trait, as instances of rapid divergence species from the value of its closest relative, and they and of are widespread and im- are referred to as PICs (there is an additional step in- portant. But on average, species resemble their close volving the branch lengths on the phylogeny, which I relatives more than they do more distant taxa, and this do not describe here). In addition, Felsenstein showed similarity reflects descent from recent common ances- that one can continue to calculate contrasts at deeper tors. Because of this inherited similarity, it is argued nodes of the tree, based on an iterative process of av- that in statistical terms species do not represent inde- eraging the trait values at successively deeper nodes. In pendent data points, violating this basic assumption of a fully resolved phylogeny, N species will be connected significance testing. One can also approach this prob- by N 1 common ancestors, so N trait values mea- lem in terms of the underlying historical processes. Trait sured on the species will provide N 1 contrasts; these associations among extant species arise through a his- contrasts can be used as the variables in correlation, torical sequence of correlated changes occurring along regression, and multivariate statistical analyses. each branch of the phylogeny; ideally, we would like to A study that I conducted with Peter Reich in 1999 estimate the correlation between these changes to more illustrates the application of independent contrasts and directly measure evolutionary linkages between the how they can impact the analysis of trait associations. traits. It is now well established that the correlations We examined correlations among several functional observed among living species (at the tips of the phy- attributes of leaves, including leaf size, leaf lifespan logeny) do not provide a reliable estimate of this his- (the length of time a leaf persists on a plant), and torical pattern of correlated evolutionary changes that specific leaf area (SLA, the ratio of leaf area to leaf dry have occurred along the branches of the phylogeny. mass; higher values indicate thinner or less dense Although some researchers are strongly motivated by leaves). Global studies of leaf function have found that the statistical arguments, and others more by the his- leaves with higher SLA tend to have faster metabolic torical questions, both perspectives lead one to the use rates and shorter leaf lifespan, and this strategy is fa- of phylogenetic comparative methods. vored in more fertile habitats. The opposite set of traits The selection of a comparative method to conduct is observed in leaves with low SLA. In addition, it is associational analyses depends on the nature of the data sometimes observed that leaves with low SLA and and the hypothesis. One of the most common problems long leaf lifespan are smaller, and small leaves are of- is the correlation (a measure of the strength of associ- ten viewed as an adaptation to low-water or high- ation) between two traits measured on a continuous temperature environments. In particular, the needles of scale (e.g., body size or seed size). Correlation coeffi- conifers (pines, , etc.) are smaller in area and cients range from 0 for two traits with no association have a longer lifespan than the leaves of most flowering up to 1 for traits that are very tightly linked (–1 if it is plants. a negative association). In 1985, In a data set of about 100 species, including both introduced the method of phylogenetic independent conifers and flowering plants, there are negative cor- contrasts (often referred to as PICs) to address this relations of leaf lifespan with both SLA and leaf size. question in a phylogenetic context; more than 20 years However, when we apply independent contrasts, the re- later, his method remains one of the most robust and sults change dramatically. The evolutionary correlation Phylogenetics 121

A. Species data C. Independent contrasts 3.0 0.4 Angiosperms Conifers 0.2 Angiosperm/conifer 2.5 contrast

0 2.0 -0.2

1.5 -0.4

R = -0.75 R = -0.64 1 -0.6 0 120 0.2 0.4 0.6 0.81.0 1.2 B. D. 3 2.0

1.5 2 1.0 , log) , 2 1 0.5

0 0 Leaf size contrasts size Leaf Leaf size (cm size Leaf -0.5 -1 -1.0 R = -0.42 R = 0.0 -2 -1.5 0 1200.2 0.4 0.6 0.81.0 1.2 Leaf lifespan (mo., log) Leaf lifespan contrasts Figure 2. Analysis of interspecific correlations among leaf traits, within the flowering plant phylogeny, and gray circles are contrasts using independent contrasts. Panels A and B show the correlations among conifers. The white circles represent the contrast at the of leaf lifespan with leaf size and specific leaf area, respectively. basal node between the two groups. For convenience, the sub- Black circles are data for flowering plant species; gray circles are traction at each node is arranged such that the contrast for leaf for conifers. The strength of the associations is indicated by the lifespan is positive, and then the contrast for the other trait is correlation coefficients in the lower left corner of each panel. Pa- positive or negative, depending on the trait values (subtraction must nels C and D show the corresponding relationships analyzed with be in the same direction for both traits). (From Ackerly et al., 2000, independent contrasts. Black circles are contrasts between nodes Bioscience; copyright American Institute of Biological Sciences)

between SLA and leaf lifespan, based on contrasts, is occurring in these two traits. In essence, the pattern similar to the pattern observed without using inde- observed if each species is treated as an independent pendent contrasts. But the evolutionary correlation data point reflects the influence of a single event deep in between leaf lifespan and leaf size is essentially zero the evolution of these groups; when this single event is (figure 2). Why does this result shift so dramatically? represented as one data point in the analysis (based on As noted above, most of the correlation observed be- the one contrast), its influence is diminished, and we tween leaf lifespan and size results from the marked see that there is not a consistent evolutionary tendency difference between these traits in conifers and flower- for correlated changes between these two traits. Other ing plants, the deepest split in the phylogeny for this lines of evidence are consistent with this result: there is group of plants. Independent contrasts capture this no evidence that leaf lifespan and leaf size are func- shift as a single contrast. The rest of the contrasts, tionally or evolutionary linked to each other, so the calculated among species of flowering plants or among result from independent contrasts proves more reliable. species of conifers, exhibit no correlation in the shifts We are still left with an important pattern in the 122 Autecology present day: it is true that conifers have small, long- pair of species in a study. This then opens up the full lived needles, which differ on average from the leaves power of linear models, including multifactorial anal- of flowering plants. These differences may be impor- ysis of variance or covariance, with appropriate ad- tant to understanding the ecological differences be- justment of significance tests reflecting the phylogeny. tween these two groups of plants, but they should not Although this facilitates a much broader range of hy- be taken as evidence of an ongoing functional and pothesis tests, one drawback is that the interpretation evolutionary linkage between these traits. of results in terms of underlying historical processes As shown in this example, the method of inde- is generally not as straightforward. A related of pendent contrasts addresses both the statistical and methods uses maximum-likelihood approaches to find historical issues associated with the analysis of inter- the best-fit model for a given set of interspecific trait specific trait correlations. The contrasts are statistically data, given the phylogeny and alternative hypotheses independent, so significance values are reliable. The of how the traits may be associated with each other. correlation or regression coefficients between the con- Maximum-likelihood approaches (and related Bayes- trasts provide a much more precise measure of the ian methods) have the general advantage that it is underlying evolutionary pattern compared to a corre- easier to invoke alternative underlying models of trait lation of trait values from present-day species. How- evolution. Further discussion of these methods, and the ever, like all statistical methods, independent contrasts issues of branch lengths and evolutionary models, is invoke key assumptions, and these assumptions have beyond the scope of this chapter; researchers who will been the source of some controversy. The most im- be using contrasts or other methods discussed here are portant assumption is that trait evolution conforms to a well advised to seek a deeper understanding of these pattern of change known as a constant-variance ran- issues. dom walk or Brownian motion. This model assumes It is important to note that discrete characters, such that the changes occurring in each unit of time are as presence/absence of a trait or different states of a equally likely to be positive or negative and are drawn morphological character, usually require different ap- from a normal distribution, such that small changes are proaches. Traditional tests of association for dis- more likely than large ones. Because these changes ac- crete characters involve chi-square or G-tests, based on cumulate across multiple time steps, the total change contingency tables showing the frequency of different along a branch is also expected to be proportional pairs of states. Phylogenetic approaches can be used to the length of the branch. On the one hand, simula- to reconstruct historical transitions from one state to tions have shown that statistical tests based on in- the other and then to test for associations between dependent contrasts are quite robust to a variety of these transitions or between transitions in one char- deviations from these basic assumptions, particularly acter and the background state of the other character. if appropriate steps are taken to transform data or Maximum-likelihood models, such as the DISCRETE branch lengths in advance of analysis. In addition, the program introduced by Mark Pagel, provide power- Brownian motion model is a reasonable first approxi- ful solutions to this problem by testing whether the mation of a model of evolutionary change based on probabilities of transitions in different characters are our knowledge of quantitative and the inheri- associated with each other (see box 1). tance of continuous traits. On the other hand, a variety of other models of trait evolution may be considered; under some of these alternatives, species trait values are relatively independent of each other, and inde- BOX 1. SOFTWARE FOR PHYLOGENETIC pendent contrasts (or other comparative methods) do COMPARATIVE METHODS not necessarily provide a reliable measure of historical Phylogenetic comparative methods are computa- patterns. tionally intensive, and a variety of software packages There are several other classes of comparative have been introduced that implement different tests. methods that can be used for questions of trait asso- A few of the most important are briefly summarized ciations. One of the most important is known as the here. phylogenetic regression, introduced by Alan Grafen in MacClade, first introduced by David and Wayne 1989, or phylogenetic general linear models. These Maddison in 1987, set the standard for graphical approaches utilize statistical methods in which the elegance and ease of use in phylogenetic soft- user can specify the degree of independence among ware. It is primarily used for reconstructing the observations. The phylogeny is used to generate what is evolution of discrete characters, based on parsi- known as a variance–covariance matrix, which cap- mony methods, and also has limited capabilities tures the expected degree of dependence among each for continuous characters. Phylogenetics 123

Mesquite, also developed by the Maddisons, is a Many terms have been used to describe this pat- cross-platform and open-source program (http:// of slow change: phylogenetic inertia, phylogenetic www.mesquiteproject.org) with most of the fea- constraint, and phylogenetic effects. Often, these terms tures of MacClade plus a broader array of meth- convey a sense that the phylogeny itself is the cause of ods, including independent contrasts. ancestor–descendant resemblances. I find it useful to R is a freely distributed program for statistical anal- ysis and programming; individual users develop use the term phylogenetic signal, advocated in a recent and contribute libraries that implement differ- essay by Simon Blomberg and Ted Garland, to em- ent methods (http://www.r-project.org). Several phasize that the similarity among relatives is a pattern libraries are now available (ape, ade4, geiger, and by itself does not reveal the underlying processes. PHYSIM, PHYLOGR) that implement numerous An understanding of the causes of phylogenetic signal, phylogenetic comparative methods. R is a very and why it may vary in different groups and for dif- powerful program that is being adopted by many ferent traits, draws on genetics, , researchers in ecology (although it is difficult to and ecology. We know that evolutionary change re- learn at first). quires heritable, genetically based variation in a trait COMPARE , written by Emilia Martins, is a Web-based for selection to act on. Recent advances in the field of program that implements independent contrasts, phylogenetic linear models, and related methods ‘‘evo-devo’’ are shedding light on how the process of (http://www.indiana.edu/~martinsl/compare/). development can influence the expression of genetic Phylocom is a freely distributed program (http:// , explaining why some traits vary more than www.phylodiversity.net/phylocom) that is widely others and why certain attributes may appear repeat- used for phylogenetic analysis of community edly in different lineages. On the other hand, even if structure and also conducts independent con- ample is available, trasts and analyses of phylogenetic signal. may act to maintain traits in their current condition if DISCRETE and Continuous, both written by Mark an is well adapted to its current conditions. Pagel and colleagues, implement several maxi- This process is known as stabilizing selection and may mum-likelihood methods for the analysis of trait be pervasive in nature, although for a variety of tech- correlations, modes of trait evolution, and related methods. Both of these programs are now in- nical reasons it can be quite hard to detect. The ability cluded in the BayesTraits program (http://www of plants and to migrate during episodes of .evolution.rdg.ac.uk/BayesTraits.html). climate change and track the environments to which they are well adapted may also be a process that reduces the rate of evolutionary change. There is no general consensus on the relative importance of these different factors that contribute to the phylogenetic signal in 3. PHYLOGENETIC SIGNAL: PATTERN different traits, and it is very difficult to obtain all the AND SIGNIFICANCE relevant data in any particular case study. The fact that closely related species resemble each other In the context of ecological research, it can be useful —in ecological, morphological, behavioral, and other to quantify the pattern of phylogenetic signal and com- attributes—comes as no surprise to students of natural pare observed patterns to those expected under alter- history. Evolution is generally a conservative process, native evolutionary models. The Brownian motion and traits will usually change slowly, if at all, from one model, in particular, provides an important point of generation to the next. Adaptive radiations, in which comparison because it is the foundation of many com- species may diverge rapidly and take on novel adaptive parative methods. Although Brownian motion repre- traits and ecological lifestyles, are of interest precisely sents a random model of evolutionary change, it does because they are unusual: at moments of ecological generate a fairly high degree of phylogenetic signal, as opportunity, following mass or the arrival of sister taxa diverge gradually from their common an- colonists on uninhabited islands, we see the potential for cestors. In contrast, null models in which trait values rapid evolutionary change. But most of the time, evo- are randomly rearranged among the species in a study lution is slow, and few changes accumulate, even over provide a baseline measure for the complete absence of long periods of time. The lack of change is referred to as phylogenetic signal. Two closely related measures, evolutionary stasis. The importance of understanding Pagel’s l and Blomberg’s K statistic, are particularly stasis in evolution has been highlighted by paleontolo- useful, as they take on a value of 1 when patterns of gists, especially Steven Jay Gould, based on their study trait similarity conform to expectations of Brownian of the record. When stasis, or at least a slow rate of motion and greater than or less than 1 when close rel- change, plays out across the phylogeny, the result is that atives are more or less similar than expected, respec- close relatives will be very similar. tively. Another class of methods known as Mantel tests 124 Autecology is based on the correlation between the phyloge- different than may be expected. First, the degree of netic distances between species (the distance down the relatedness among co-occurring species needs to be branches of the phylogeny to the common ancestor quantified, based on the best available phylogeny. Cam and back up to another species) and the ecological or Webb and others have introduced several related phenotypic differences between them. These methods methods to accomplish this. The simplest approach is are useful for ecological characteristics such as niche simply to calculate the average phylogenetic distance overlap and co-occurrence where the degree of sim- between all pairs of species within the community. ilarity or dissimilarity between species is quantified Other approaches take into account species abundance directly. or measure the distance between each species and its Phylogenetic information can play an important closest relatives in the community, as opposed to more role in the prediction of ecological traits when there is distant relatives. The second step is to specify a broader strong phylogenetic signal. For example, in a recent pool of species from which a particular community has study, Je´roˆ me Chave and colleagues demonstrated that been assembled. This provides the source pool to con- wood density tends to be very similar among closely struct hypothetical communities that serve as a point of related tree species. Wood density is important for comparison with observed patterns. Ideally, the spatial carbon storage, a critical factor in the global carbon scale defining this pool is large enough so that it in- cycle, but it has only been measured on a small pro- cludes all of the species that could, in a reasonable span portion of tree species in the tropics. Knowledge that of time, arrive at the community of interest. However, close relatives have similar wood density will allow in practice, it is very difficult to determine exactly what more accurate prediction of carbon storage in diverse this scale should be, and researchers rely on a variety of tropical forests, even for species for which wood den- practical solutions to address this problem. Finally, one sity has not been measured directly. needs to construct an appropriate null model by which random communities can be drawn from this regional pool to determine whether the observed communities 4. PHYLOGENETICS AND COMMUNITY ECOLOGY diverge from random expectations. Simple null models Phylogenetics is playing an increasingly important role include a random draw of species, where each species is in community ecology as a tool to gain insight into the equally likely to be chosen. More complex models can processes that influence community structure. One of be constructed, in which the probability of a species the earliest theoretical principles of ecology was the being chosen is proportional to its frequency of oc- competitive exclusion theorem, formalized by Gause in currence in the landscape. The construction and anal- the 1930s, which states that two species that utilize ysis of these null models are continuing points of identical resources cannot coexist in a community. In discussion and development in this field. the 1950s, this idea, together with the knowledge that Many studies of phylogenetic community structure closely related species are usually ecologically similar have appeared in recent years, and some generalizations and therefore utilize similar resources, led to the pre- are beginning to emerge. First, empirical and theoret- diction that species from the same should co- ical studies suggest an asymmetry in the interpretation occur infrequently. This prediction was tested by cal- of phylogenetic community data. It appears that clus- culating the average number of species per genus in tering of close relatives within a community arises isolated communities, such as islands, compared to the primarily from an ecological filtering process, in which overall biota of the surrounding region. In the past 10 similar species are favored as they share adaptations years, phylogenetic approaches to community ecology that are appropriate for the particular conditions. On have been revitalized by the availability of highly re- the other hand, many different processes can lead to solved phylogenetic trees and new methods. In addi- the opposite pattern in which communities are com- tion, developments in community assembly theory posed of more distant relatives than expected. These have emphasized an alternative view that co-occurring include competition, small-scale habitat heterogeneity, species may be more similar to each other than ex- facilitative interactions among functionally disparate pected because similar traits may promote ecological species, and even a filtering process when the traits that success under particular environmental conditions. promote success have evolved independently in differ- These two perspectives provide contrasting predictions entclades.Theoreticalstudiesalsosuggestthatitismuch regarding whether communities will be composed of harder to detect patterns in which coexisting species more or less closely related species. are distantly related, compared to the opposite pattern. Three steps are required to quantify the phyloge- A second result is the realization that communities netic structure of ecological communities and test hy- will not be structured either by filtering or by compe- potheses about whether this structure is significantly tition or by any other single process. Many processes Phylogenetics 125 are likely at work, mediated by different sets of traits. are most relevant to ecological research. Measures of For example, Jeannine Cavender-Bares and colleagues phylogenetic diversity are also used as criteria to help studied the composition of oak-dominated forests in prioritize taxa and habitats in conservation biology, Florida and found that local communities were gener- and a wide variety of comparative methods are in use in ally composed of distantly related species. These spe- , including the study of adapta- cies tended to share physiological traits affecting their tion, diversification, adaptive radiations, and related water relations, with drought-adapted species occur- topics. ring together on drier sites. Moreover, these hydraulic Several important areas of challenge and opportu- traits exhibited low phylogenetic signal, so similar nity lie ahead. One is the improved resolution of species tended to be distantly related for these char- branch lengths and node ages on phylogenies, which acteristics. On the other hand, co-occurring species will be provided by including more species and more displayed a high disparity of trait values related to acorn and improvements in fossil calibration. Time- maturation and wood density. These traits exhibited a calibrated phylogenies are opening the door to linkages high degree of phylogenetic signal, but closely related between comparative methods and paleoecology and species with similar values were distributed across will facilitate investigation of a new generation of different communities. Thus, it is critical to specify the questions. A second area is the development of global traits that may be relevant to community assembly and databases for ecological traits. This will allow us to examine their distribution on the phylogeny carefully assess questions of phylogenetic signal and ecological before interpreting patterns of phylogenetic community trait correlations across the entire phylogeny of major structure in terms of particular underlying processes. and to understand how the assembly of local Finally, there is a fascinating pattern in plant com- floras and faunas relate to global patterns of ecological munities of a shift from the co-occurrence of more dis- diversity. Third, phylogenetic methods are providing tant relatives when studies focus on a narrow clade new insights into ecology and of mi- (e.g., oaks) to a pattern of clustering of close relatives crobes, fungi, and other groups that are difficult to in broader studies that encompass the full spectrum of study directly in the field. These are but a few of the flowering plants or all seed plants. A similar shift oc- growth areas at the intersection of phylogeny and curs moving from smaller to larger spatial scales. Both ecology—the most exciting advances will be those that of these patterns are consistent with a stronger role for at this point are not even anticipated. resource partitioning among closer relatives and at smaller spatial scales, whereas habitat filtering becomes more apparent at larger spatial and phylogenetic scales. FURTHER READING Blomberg, S. P., and T. Garland, Jr. 2002. Tempo and mode 5. PROSPECTS FOR THE FUTURE in evolution: Phylogenetic inertia, adaptation and com- parative methods. Journal of Evolutionary Biology 15: The potential role of phylogenetics in ecology was 899–910. heralded by several articles and books published in the Felsenstein, J. 1985. Phylogenies and the comparative late 1980s to mid-1990s. In the relatively short interval method. American Naturalist 125: 1–15. since then, many methods have been introduced or Harvey, P. H., and M. Pagel. 1991. The Comparative improved, and growth in research has been rapid. The Method in Evolutionary Biology. Oxford: Oxford Uni- number of citations in the scientific literature under the versity Press. keywords phylogen and ecology rose from 4 in 1990 Maddison, W. P., and D. R. Maddison. 1992. MacClade: Analysis of Phylogeny and . Sunder- to 87 in 1995, 130 in 2000, and 275 in 2006. An im- land, MA: Sinauer Associates. portant engine of this growth has of course been the Pagel, M. D. 1999. Inferring the historical patterns of bio- constantly expanding availability and improved reso- logical evolution. Nature 401: 877–884. lution of phylogenies for diverse groups of taxa, ac- Webb, C. O., D. D. Ackerly, M. McPeek, and M. J. Dono- companied by new methods, fast computers, and easy- ghue. 2002. Phylogenies and community ecology. Annual to-use software. This chapter highlights two areas that Review of Ecology and 33: 475–505. 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