I.16 Phylogenetics and Comparative Methods David D. Ackerly OUTLINE GLOSSARY 1. The role of phylogenetics in ecology 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 species 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. Fossils 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 taxon 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 lineage. 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 Family having many trees & having a ten- dency to separated sexes: for the 32 trees belong D terminal polytomy taxa to nine Families, & the trees with separate sexes (’tips’) to five Families. E MRCA of —Charles Darwin, manuscript for Natural root or F and G basal F Selection (unpublished) node G H In the quote above, Darwin observes an interesting pattern among plant species of Great Britain. He notes clade containing that among trees, the proportion of species that have species E, F, G, and H individuals of separate sexes (as in humans and most Figure 1. Example of a phylogenetic tree for eight taxa (A–H), illus- vertebrates) 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 adaptation to promote cross- fertilization in trees: because trees are large and have phylogenetic distance. The phylogenetic distance be- many flowers, the chance that an insect 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 nÂn 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 biology, 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 polytomies Throughout the past 150 years, since the publica- as either hard or soft but do not always make the tion of Darwin’s On the Origin of Species, 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 life—as well as the justed to represent relative or absolute time. cumulative legacy of the past. Evolution 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 penguin 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 adaptations must be understood in his- In the discussion below, it is assumed that a phy- torical context: penguins are birds, 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 (loons, 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, comparative biology has grown scientific hypothesis, it is subject to revision and im- rapidly as a new generation of methods emerged, com- provement.