Adaptation and functional integration in primate phylogenetics

Journal of Human Evolution 52 (2007) 490e503

Adaptation and functional integration in primate phylogenetics Charles A. Lockwood* Department of Anthropology, University College London, Gower Street, London WC1E 6BT, United Kingdom Received 30 December 2005; accepted 21 November 2006

Abstract In two areas of phylogenetics, contrary predictions have been developed and maintained for character analysis and weighting. With regard to adaptation, many have argued that adaptive characters are poorly suited to phylogenetic analysis because of a propensity for homoplasy, while others have argued that complex adaptive characters should be given high weight because homoplasy in complex characters is unlikely. Similarly, with regard to correlated sets of characters, one point of view is that such sets should be collapsed into a single characterda single piece of phylogenetic evidence. Another point of view is that a suite of correlated characters should be emphasized in phylogenetics, again because recurrence of detailed similarity in the same suite of features is unlikely. In this paper, I discuss the theoretical background of adaptation and functional integration with respect to phylogenetic systematics of primates. Several character examples are reviewed with regard to their functional morphology and phylogenetic signal: postorbital structures, tympanic morphology, fusion of the mandibular symphysis, the tooth comb, strepsirrhine talar morphology, and the prehensile tail. It is clear when considering characters such as these that some characters are synapomorphic of major clades and at the same time functionally important. This appears particularly to be the case when characters are integrated into a complex and maintained as stable configurations. Rather than being simply a problem in character analysis, processes of integration may help to explain the utility of phylogenetically informative characters. On the other hand, the character examples also highlight the difficulty in forming a priori predictions about a character’s phylogenetic signal. Explanations of patterns of character evolution are often clade-specific, which does not allow for a simple framework of character selection and/or weighting. Ó 2007 Published by Elsevier Ltd. Keywords: Functional complex; Homoplasy; Homology; Character weighting

Introduction Morphology is demonstrably useful for phylogenetic analysis of the order Primates, as it is for most other groups. When interpreted in the context of modern phylogenetic systematics, morphological studies support the monophyly of Primates, the division of the primate order into haplorhines and strepsirrhines, the recognition of hominoids and cercopithecoids, and the close relationship of African apes and humans. Some erroneous inferences have been drawn, some higherlevel questions are still debated, and many low-level questions have yet to be resolved, but the depiction of extant primate

* Tel.: þ44 207 679 8837; fax: þ44 207 679 8632. E-mail address: [email protected] 0047-2484/$ - see front matter Ó 2007 Published by Elsevier Ltd. doi:10.1016/j.jhevol.2006.11.013

phylogeny based on morphological data is broadly similar to that based on genetic data. At the same time, morphology has long been thought to possess qualities that undermine its value in studies of primate phylogeny. Morphology responds to natural selection, and therefore selection can elicit similar morphological responses in distantly related taxa. Morphology responds to environmental stimuli and is therefore less heritable than molecular characteristics. Morphology is also in some sense constrained, whether through genetic constraint or through stabilizing selection associated with developmental canalization. Because of such constraints, similar morphological responses to natural selection are likely to recur. Each of these attributes may conflict with the goals of phylogenetic reconstruction. Taken together, they imply that morphological data may simply convey information about similarity among organisms, rather

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than showing whether this similarity represents homology or homoplasy. However one views the phylogenetic utility of morphology, morphological characters are the only data relevant to the reconstruction of phylogenetic relationships among the vast majority of fossil taxa. Moreover, in some cases debates concerning the relationships of fossil taxa have reached a stalemate. The challenges associated with using morphological data in phylogenetic reconstruction must therefore be confronted. In this paper, I will ask whether some of the common criticisms of morphological data are flawed or overly simplistic. In particular, I will evaluate the linked concepts of adaptation and functional integration, first from a theoretical perspective, and then in the context of a series of well-known characters as case studies. The goal is to determine whether adaptive, integrated sets of characters are a source of extensive homoplasy (i.e., a problem for phylogenetic analysis). In so doing, the review of characters will also highlight how processes of selection and integration can contribute to the phylogenetic signal. What is the problem? Two themes come up frequently in discussions of homoplasy in primate morphological data sets and phylogenetic analysis of morphology in general. One is that adaptive characteristicsdfeatures that are shaped by natural selectiondare prone to homoplasy and are not expected to be reliable indicators of phylogenetic relationships. The other is that characters used in an analysis should be independent. These ideas were recognized in the early development of evolutionary theory and in classic formulations of the modern synthesis (Darwin, 1859; Simpson, 1961; Mayr, 1969). In a discussion of ‘‘adaptive or analogical characters,’’ Darwin (1859: 414) observed: ‘‘the less any part of the organisation is concerned with special habits, the more important it becomes for classification.’’ Indeed, adaptive significance is thought to be the primary detriment to morphology as a category of data in phylogenetic analysis, when compared to molecular data (e.g., Givnish and Sytsma, 1997; but see Hillis and Wiens, 2000). The criterion that characters in phylogenetic analysis should be independent is routinely accepted (e.g., Hennig, 1966; Hecht and Edwards, 1976, 1977; Farris, 1983; Felsenstein, 1983, 1988, 2002; Kluge, 1989; Skelton and McHenry, 1992; Strait et al., 1997; Emerson and Hastings, 1998; Lieberman, 1999; McCollum, 1999; Lovejoy et al., 1999; Strait, 2001). The origins of this requirement are the same that drive science to support hypotheses using independent lines of evidence. Each character in a phylogenetic analysis is an independent piece of information, and every other character serves to test the hypothesis supported by this character. If multiple characters change under the influence of a single process, this process will bias the result and increase the chance of error. Whether or not the tree is ‘‘correct,’’ redundancy among characters will give false confidence by artificially inflating support. This has the side effect of overestimating the degree of conflict between different data sets (Simmons, 1993).

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Despite widespread acceptance of the tenets above, even a cursory look through the primate phylogenetic literature shows that researchers put them into practice in very different ways. This is not simply because it is difficult to put them into practice, but also because the broad statements have many exceptions and a deep underlying complexity. Take, for example, Darwin’s statement cited above. In further discussing the subject, he qualified his argument. Although fish and whale body shapes, which are analogous, should not be used to classify the two groups together, the same types of features can be useful for demonstrating the affinity of particular whales to each other (Darwin, 1859: 427e428). The adaptive significance of the characters has not changed, but the ingroup has become more specific, and the morphological description has become more detailed. Each of these changes affects the phylogenetic utility of the characters. Clear parallels are seen in many other situations. In primates, one can simultaneously recognize homoplasy in teethdhighly adaptive structuresdand observe that tooth shape is synapomorphic of subclades such as cercopithecines and colobines. Similarly, postcranial anatomy raises suspicions that some groups evolved suspensory adaptations in parallel, but at the same time, within New World monkeys, the use of postcranial morphology to diagnose atelines has been well supported by molecular data. In short, sometimes the adaptive signal is consistent with the phylogenetic signal, and sometimes it isn’t. Because of this, and because of practical limitations or lack of firm conclusions about adaptation, morphologists continue to use characters that are suspected to be highly adaptive. Independence is a conceptually clear criterion, but empirically, it also presents many challenges for character analysis. First, what is required to demonstrate that two characters are dependent on one another? A significant correlation, or complete identity in the distribution of qualitative characters across taxa? Many features are correlated quantitatively, but characters in phylogenetic analysis are typically considered independent if they diverge to any degree in their patterns of distribution. Strait (2001) provided the most thorough empirical example of how different approaches to independence give different results in the context of phylogenetic analysis. According to his most strict criteria, few characters are redundant (i.e., wholly interdependent). Another problem is that too much effort to eliminate correlated characters may erode real support for a clade (Emerson and Hastings, 1998). Synapomorphies will be correlated if they support the same clades, even if they are genetically and structurally independent. Furthermore, characters that participate in the same functional complex are integrated and dependent on one another, but it has been argued that such similarity in a complex of characters is more likely to indicate homology (Hecht and Edwards, 1976, 1977; Bock, 1977; Luckett, 1982; Donoghue and Sanderson, 1994; and indirectly, Neff, 1986). If this is true, eliminating characters because of their interdependence would actually reduce the legitimate phylogenetic content of the data. While few authors have emphasized character complexes through explicit weighting, the common practice of atomization

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accomplishes much the same thing (Kluge and Farris, 1969). Character complexes with greater representation will impact the analysis to a greater degree. An atomistic approach can be seen in many recent analyses within primates and is arguably the dominant approach to character analysis (e.g., Begun et al., 1997; Horovitz and Meyer, 1997; Strait et al., 1997; Ross et al., 1998; Seiffert et al., 2003; Kay et al., 2004; Kimbel et al., 2004; Strait and Grine, 2004). Nonetheless, several of these studies are not entirely atomistic, as certain complexes are treated as single characters. For example, in Horovitz and Meyer’s (1997) analysis of New World monkey phylogeny, a number of character complexesdthe prehensile tail, number of offspring, and relative forelimb lengthdwere treated as single characters, and these were given the same weight as more atomized traits such as M1 mesostyle, deciduous canine cross section, and a variety of other dental traits. Strait et al. (1997) treated patterns of dental development (‘‘dental development rate’’) as a single character, although a pattern of dental development by definition includes multiple characters. Although in each case the characters were defined explicitly, the decision to make complexes equivalent to single characters occurred without much explanation. These examples demonstrate an unarticulated conceptual difference in the ways researchers view different types of character complexes. Thus, depending on one’s point of view, the problem is either that primate phylogenetic analyses fail to take the factors of adaptation and integration sufficiently into account, or that critical views about adaptation and integration in the phylogenetic context have been exaggerated. In either case, there is not yet agreement on how these factors influence character analysis in phylogenetic reconstruction, and few empirical studies have been designed to test their influence on primate phylogenetic analysis.

not sort independently, whether because of pleiotropy or linkage disequilibrium. Cheverud (1996) presented a model with selection (or more precisely, the correlated effects of selection) and genetic integration as parts of a continuum (see also Wagner, 1996). Long-term selection on individuals forms the basis of developmental or functional integration, and this may ultimately lead to loss of genetic variation that restricts further change. In a sense, this is a transition from ‘‘external selection’’ to ‘‘internal selection,’’ where the former is selection for traits related to fitness in a particular environment, and the latter is selection for correct functioning of an integrated complex of features [Table 1; see Schwenk (2001) for further explanation]. Others have also noted that factors commonly called ‘‘constraints,’’ such as developmental constraint, are actually the effect of selection for stability of a developmental pathway (Reeve and Sherman, 1993; Schlichting and Pigliucci, 1998). However, patterns of integration are not wholly a one-way process of formation. Integration as a process can be contrasted with ‘‘parcellation,’’ wherein pleiotropic effects are eliminated and character independence is promoted (Wagner, 1996; especially his Fig. 3). These mechanisms tie into the concept of a functional complex: a set of characters that can be described separately but that serve the same biological role (Bock and von Wahlert, 1965). In Fig. 1, which follows Wagner (1996), C1 and C2

Integration and phylogenetic signal

Internal selection

One way forward is to understand the causes and consequences of functional or developmental integration in more detail. This is because random patterns of homoplasydi.e., different characters exhibiting different patterns of homoplasyd should not mislead a phylogenetic analysis (Farris, 1983). Instead, adaptation is thought to be a problem when whole suites of features are convergent for the same reasons, presumably because the data set is overly influenced by a single behavioral regime (e.g., Kluge, 1989; Skelton and McHenry, 1992; Givnish and Sytsma, 1997; Larson, 1998; Lockwood, 1999; Lockwood and Fleagle, 1999). Characters can be correlated because each is subject to the same selective force, or they can be correlated in a more profound way, usually referred to as functional, developmental, or genetic integration (Endler and McLellan, 1988; Felsenstein, 1988, 2002; Cheverud, 1996; Wagner, 1996; Emerson and Hastings, 1998; Chernoff and Magwene, 1999; Strait, 2001). In functional and developmental integration, the characters interact to achieve a functional outcome, and/or their underlying developmental processes are linked (Cheverud, 1996). Genetic integration means that two characters do

Table 1 Some terms and definitions, as used in the text Term

Definition

Integration

Organization of parts into a whole, so that the parts are interdependent (following Olsen and Miller, 1958). Integrated characters may or may not be statistically correlated. Selection for functional and developmental integration (coordination) of traits, which enhances fitness regardless of environment or context (following Whyte, 1965; Schwenk, 2001). Selection for a trait that enhances fitness in a particular environment or context (‘‘typically Darwinian’’ selection, following Schwenk, 2001). A set of characters that can be described separately but that serve the same biological role (Bock and von Wahlert, 1965). Similar terms are ‘‘character complex’’ or ‘‘functional unit.’’ Suites of characters that have different morphogenetic or evolutionary precursors that are unified into a single structure in adults (following Schwenk, 2001). Morphological composites whose component characters are physically integrated and allow little to no movement (following Schwenk, 2001). A set of characters that serve the same biological role and remain stable through internal selection (following Wagner and Schwenk, 2000).

External selection

Functional complex

Structural unit

Mechanical unit

Evolutionarily stable configuration (ESC)

Definitions are provided only for the purpose of clarity, as their meaning is not discussed in detail here. Schwenk (2001) and Bock and von Wahlert (1965) give excellent reviews of such terms and their history.

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F2

F1

C1

C2

A

G1

B

G2

C

D

G3

E

F

G4

G5

G

G6

Fig. 1. Drawn following Wagner (1996: Fig. 2). C1 and C2 are character complexes that serve different functions, although as discussed in the text, F1 and F2 correspond more closely to biological roles, sensu Bock and von Wahlert (1965). Characters within C1 are expected to be more integrated with each other than they are with characters in C2, and vice versa. Pleiotropic connections stemming from genes G1eG6 are expected to follow a similar pattern. C1 and C2 are in some sense units of evolution, although, over time, patterns of integration could change, leading to the formation of a third complex (‘‘parcellation’’ or elimination of pleiotropic effects; Wagner, 1996), or consolidation of C1 and C2 into a single integrated complex.

are functional complexes. The expected pattern is that characters within a complex are more strongly integrated with each other than they are with characters in another complex (although individual characters may function in multiple complexes). As characters are progressively more integrated and dependent on one another, a series of character complexes can be described: from functional complexes and ‘‘evolutionarily stable configurations’’ (ESCs, further discussed below) to mechanical units and structural units (Table 1). The latter three character complexes are drawn from Schwenk (2001). Wagner (1996) referred to character complexes as modules, or modular units of evolution, although at the less integrated end of the scale (functionally correlated characters), individual characters may still evolve independently rather than as modules (see also Strait, 2001). These categories do not have hard and fast boundaries; instead, they provide a set of terms to describe patterns analogous to the process continuum described by Cheverud (1996). The key point in considering this variety of complexes, and the relationship of correlated characters to their use in phylogenetics, is the difference between sets of character changes that represent a change in a single developmental or physiological program, and those sets of character changes that represent several independent targets of selection. The classic problem for phylogenetic reconstruction is when a single developmental shift produces a suite of anatomical changes as homoplasy (e.g., Wake, 1991). For this reason, most discussions of integrated complexes that could be reduced to a single character have focused on process-defined complexes, such as

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heterochronic shifts that affect several features or sets of features related to sexual dimorphism (Emerson and Hastings, 1998). In primates, papionins are one of the most widely cited examples of homoplasy, and there is a suspicion that many of the homoplastic features can be ascribed to allometry and hence simple changes in body size (Disotell, 1994; Collard and O’Higgins, 2001; Leigh et al., 2003), although the actual pattern is of course more complicated (Leigh, 2007). When making decisions in character analysis, a case can be made for treating complexes as single characters when it has been demonstrated that a simple shift in genetic or developmental program has many downstream effects. However, it is necessary to seperate these situations from cases in which a number of independent characters are selected for and are therefore correlated in the resulting pattern of evolution. For example, Lovejoy et al. (1999, 2002) sought to distinguish these kinds of correlations in the evolution of human bipedalism. Even though they took a strong integrationist approach and saw a number of correlates of bipedalism as secondary consequences of changes in other features, Lovejoy et al. (2002) still identified several independent targets of selection within the functional complex of bipedalism. Such features may be correlated, but as separate targets of selection, they can also evolve independently. In this respect, functionally integrated characters are not redundant for phylogenetic analysis in the same way that genetically integrated characters are. The effects of selection and integration on the phylogenetic signal of characters were brought together by Wagner and Schwenk (2000), who articulated a basis for considering certain character complexes to be highly adaptive and highly integrated, and phylogenetically meaningful as a result. These were referred to as evolutionarily stable configurations (ESCs)dsets of characters that are adapted to perform the same function and are stable across taxa that possess the configuration (see also Schwenk, 2001). Stability in an ESC is maintained by internal selection (Table 1) and the need for characters to integrate to perform their function effectively. In a sense, an ESC is a complex single character, but the constituent parts retain some independence and can be dissociated if the ESC is lost. Hypothesizing an ESC requires several observations: the key components of the ESC must not vary significantly in the taxa of interest, the characters must vary more widely in taxa without the ESC, and the ESC should be present in multiple environmental contexts. In other words, the ESC is broadly adaptive and not tied to a particular settingda pattern that makes it useful in diagnosing clades. In sum, correlation among characters may be due to one of several processes, with different and in some cases unknown implications for phylogenetic analysis. It is also important to distinguish a pattern of correlation from the demands of integration. The former may be a sign of the latter, but correlations can also occur for other reasons, including coselection on independent characters. To say simply that correlation among characters is a problem in phylogenetic analysis is to understate the complexity of the causes of correlation. It overlooks the crucial point that many authors interpret correlation as a source of data that is informative regarding phylogeny.

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Character examples For many primate clades, molecular relationships have been determined with sufficient confidence that morphological data sets can be tested against ‘‘known’’ phylogenies, and this procedure provides empirical results to test expectations (Begun, 1992; Fleagle and McGraw, 1999; Collard and Wood, 2000, 2001, 2007; Gibbs et al., 2002; Lockwood et al., 2004; Strait and Grine, 2004; Lycett and Collard, 2005). Here, I will take a similar approach but will focus on individual characters that are relatively well-known in terms of their functional morphology and, in some cases, their correlation with other features. The characters are reviewed and described with respect to (1) their functional role, (2) the degree to which they take part in a functional complex, and (3) whether they exhibit homoplasy. The goals are first to determine whether homoplastic characters are also the ones thought to be functionally important, second, to discuss how patterns of integration affect the phylogenetic analysis of these characters, and third, to ask whether patterns of integration help to explain the characters’ patterns of evolution. I will evaluate the following structures or complexes: form of the lateral wall of the orbit (postorbital bar and postorbital septum), tympanic morphology, fusion of the mandibular symphysis, the tooth comb, strepsirrhine talar morphology, and the prehensile tail. These characters were chosen to represent a cross section of the kinds of morphological characters used in higher-level primate systematics, and also because the structural components of each have been addressed in some detail. Implications will be discussed in the concluding section of the paper. Postorbital bar and septum These traits are two states of the same characterdthe form of the lateral wall of the orbit. The postorbital bar is a synapomorphy of Primates and occurs independently in some other mammalian taxa. The postorbital septum is a synapomorphy of Anthropoidea or Haplorhini, depending on how character states are defined, and it occurs only in primates among mammals. Functional explanations of the postorbital bar and septum include protection of the orbital contents, stabilization of the eye to increase visual acuity, and resistance of biomechanical stress transferred through the face (Cachel, 1979; Cartmill, 1980; Greaves, 1985; Ross, 1995, 1996; Ross and Hylander, 1996; Ravosa et al., 2000; Heesy, 2005). Although the functions are debated, the general adaptive significance of postorbital structures is not doubted. When present, the postorbital bar is structurally homologous across mammalian taxa, as the frontal and zygomatic bones extend processes to form the bar (equines are an exception; Heesy, 2005). In this sense, it is a relatively simple structure, and it is easy to envision how it could evolve multiple times in response to similar selection pressures. Why, then, does the postorbital bar appear to be homologous across primates, instead of showing a more complex pattern of evolution?

The most complete study to date of postorbital bar function found that it stiffens the lateral orbital wall, which is necessary to allow normal oculomotor function when the orbits are strongly frontated or convergent or when they are vertically oriented relative to the palate (Heesy, 2005). Thus, the postorbital bar exists in the context of a spatial arrangement involving other skull structures, and it may be present for different reasons in different taxa. There are two contradictory implications of this pattern. On the one hand, the postorbital bar is not a ‘‘simple’’ structure at all, as it conveys information about a larger morphological complex including the orbits, the temporal fossa, and the braincase. On the other hand, it raises the problem of equifinality because the postorbital bar is structurally homologous even if it is adaptive in different circumstances. Moreover, if information about the correlates of the postorbital bar are included in a phylogenetic analysis [e.g., measures of orbit orientation as collected by Heesy (2005) and others], then the postorbital bar would be redundant with the other features. Essentially, it is either a surrogate for a larger morphological complex, or it is a functional correlate of spatial relationships reflected in other aspects of skull morphology. The postorbital bar is consistent with other primate synapomorphies and has always been a ‘‘textbook’’ diagnostic character of primates. It may only be homologous across primates because the group as a whole has relatively frontated orbits (i.e., they are all within the range of shape that promotes selection for the bony bar). Although it conveys phylogenetic information, it hides substantial quantitative variation in the factors that contribute to orbitotemporal angle (‘‘the angle between the orbital plane and the plane of the temporal fossa’’; Heesy, 2005: 365). In terms of descriptive detail, a better series of characters might be the measurements of orbital orientation themselves. To an extent, the postorbital septum (or postorbital closure) might be thought of in the same terms, as it is a qualitative character state that seems to occur in taxa with a range of different quantitative aspects of skull structure. This character is perhaps more intriguing, as it is unique to primates among mammals, and there has been substantially more debate about its structural homology. While different authors have come to terms with the postorbital septum in different ways, all have asked the same question: Is this character homologous in the taxa that possess it? To ask this question is to treat the postorbital septum as a single character. No one, to my knowledge, has sought to partition the postorbital septum into a series of characters describing, for example, the exact shape of the constituent bones. Variation in the configuration of the bones that make up the postorbital septum has, however, led some authors to argue for nonhomology of the structure in New and Old World anthropoids (Simons, 1972) or, more commonly, for lack of homology between tarsiers and anthropoids (Simons and Russell, 1960; Schwartz et al., 1978; Simons and Rasmussen, 1989; Beard and MacPhee, 1994). In the latter case, the structural differences between tarsiers and anthropoids are obvious: the tarsier has only partial postorbital closure. If the intermediacy of the tarsier is treated as evidence of its haplorhine status, then it is because,

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in a sense, the tarsier possesses the same structure as anthropoids, just to a lesser degree. Cartmill (1980) emphasized this view and argued that homology of the entire structure does not require identical contribution of its constituent elements. He used the analogy that bones vary in how they contribute to the sidewall of the braincase across anthropoids, but that ‘‘they surely do not imply that the last common ancestor of the anthropoids had a partly unossified braincase like that of reptiles, or that different anthropoid groups must be traced back to different premammalian ancestors’’ (Cartmill, 1980: 257). Cartmill further argued that homology of partial postorbital closure in the tarsier and complete closure in anthropoids is based on the contribution of the alisphenoid to the structure in all taxa (see also Fleagle and Kay, 1987; Ross, 1994). Cartmill’s depiction of the postorbital septum follows the pattern of a ‘‘mechanical unit,’’ as described by Schwenk (2001): the component characters vary, but the overall form of the mechanical unit is stable and homologous. The question remains, what process gives rise to stability in its overall form? Although adaptationist hypotheses have been put forward to explain postorbital closure, the extent to which stabilizing selection has maintained the feature is unclear. Anthropoids may be canalized to retain a common configuration of their orbits, or they may all have orbit configurations for which a postorbital septum is beneficial, because of the general utility of frontated orbits in this group. In any case, the conclusion that the details of postorbitalseptum structure yield no clues about its homology means that the only test of homology comes through phylogenetic tests. In these cases, the anthropoid postorbital septum usually emerges as homologous (Ross et al., 1998; Seiffert et al., 2003; Kay et al., 2004). Kay et al. (2004) found that, under certain assumptions, amphipithecids (which lack the septum) fall within the anthropoid group, in which case homoplasy of the septum is implied. However, that conclusion is mitigated by recent demonstration that the presence or absence of a septum is actually unknown for amphipithecids, in which case the septum may remain homologous across anthropoids (Beard et al., 2005). If we adopt the position that adaptive structures are prone to homoplasy, then the postorbital bar and postorbital septum in primates would be predicted to be poor characters for phylogenetic analysis. Both are discrete features that can reflect a range of variation in orbital position and orientation, and even if they evolved independently, the multiple occurrences would probably appear to be structurally homologous. In other words, equifinality due to separate selection events should be a serious problem with postorbital structures. And yet, based on current understanding of phylogeny from both morphological and molecular data, each of these features evolved only once in primates. Either predictions of homoplasy are simply not reliable, or there are other factors that made these characters stable once they evolved. Tympanic morphology The morphology of the tympanic element of the temporal bone has been widely discussed with respect to higher-level

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phylogeny of primates. A basic description of the tympanic is annular, or ‘‘ringlike,’’ in lemurs, platyrrhines, and early anthropoids, but mediolaterally extended, or ‘‘tubelike,’’ in lorises, tarsiers, anthropoids, and some large-bodied lemurs (MacPhee and Cartmill, 1986; Fleagle, 1999). Based on this distribution, it is evident that at least one of the conditions is homoplastic or represents different characters that have been conflated. There are essentially two characters having to do with the form of the tympanic (Beard and MacPhee, 1994; Ross, 1994): whether the tympanic is extrabullar or intrabullar, and whether it is extended laterally as a tube. Beard and MacPhee (1994: 62) identified a synapomorphy of ‘‘crura and body not expanded relative to ontogenetically early condition’’ in lemurs, but found that the extended tubelike tympanic is homoplastic in an omomyoid group (including tarsiers) and some catarrhines. They also pointed out that the tubelike tympanic may be the primitive condition. The tubelike tympanic of lorisoids is considered ‘‘not extended’’ because the meatus is not formed exclusively by the ectotympanic. Ross (1994) concluded that an extrabullar tympanic is a synapomorphy of tarsiers and all anthropoids, and that it arose independently in some lorisoids and plesiadapiforms. An extended tubelike tympanic was homoplastic in his analysis. Thus, in both of these studies, tympanic morphology showed a pattern of homoplasy that created a general consensus that the tympanic by itself is of ‘‘low phylogenetic valence’’ (Beard and MacPhee, 1994: 65). This was a pattern-based conclusion that came after phylogenetic analysis, rather than a conclusion based on inherent characteristics of tympanic morphology. The function of different forms of the tympanic is poorly understood (MacPhee and Cartmill, 1986; Coleman and Ross, 2004). Morphological differences are taxonomically deep, meaning that diverse taxa share morphological configurations despite variation in auditory acuity. Accounting for phylogenetic relationships confounded attempts by Coleman and Ross (2004) to draw correlations between hearing sensitivity and middle-ear structures. The shape of the tympanic itself may have more to do with spatial relationships in the basicranium and the positioning of middle-ear structures relative to the external ear opening than to particular hearing frequencies or sensitivities. In any case, it seems doubtful that tympanic morphology is neutral to selection, given that it is consistent across fairly large groups of primates instead of widely variable. The comparison of tympanic morphology with postorbital structures is interesting because, a priori, one might expect similar patterns of evolution in all of these structures. In each case, the characters are mechanical units comprising multiple morphogenetic precursors. Why does tympanic morphology show a pattern of homoplasy, and postorbital structures do not? Again, either the expectation itself is based on poor criteria, or there are functional reasons for the plasticity of tympanic morphology. Primates may vary more widely in the configurations of skull elements that correlate with different tympanic structures than they do in the orbit configurations that correlate with postorbital structures.

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Symphyseal fusion Fusion of the mandibular symphysis is observed uniformly in all extant anthropoids. Some researchers have given it great weight in the identification of the sister group of anthropoids (Simons, 1989, 1992; Rasmussen and Simons, 1992; Simons and Rasmussen, 1996), but the lack of symphyseal fusion in basal anthropoids makes that approach debatable (Beard et al., 1994, 1996; Ross et al., 1998; Ravosa, 1999; Kay et al., 2004). While the fused mandibular symphysis in extant catarrhines and platyrrhines appears to be homologous, fusion seems to have occurred independently in some basal anthropoids. This is a case where fossil taxa serve to reject a hypothesis of homology based on extant taxa. The character is also extensively homoplastic in strepsirrhines, occurring in some fossil adapids and large-bodied Malagasy lemurs (e.g., Ravosa and Hylander, 1994). Ravosa (1999) argued that four character states are required to adequately describe the condition of the mandibular symphysis in primates: unfused, partially fused, late-fusing, and early-fusing. Partial fusion occurs through ossification of cruciate ligaments. Late-fusing means that complete fusion is achieved after weaning, and early-fusion occurs before weaning. Ravosa concluded that a different loading regime underlies each character state. Based on an observed propensity for homoplasy, the form of the symphysis could be given low weight in a phylogenetic analysis or excluded altogether (Szalay et al., 1987; Ravosa and Hylander, 1994). This conclusion probably applies to using Ravosa’s (1999) character state description as well. Although homoplasy of early fusion is not observed, homoplasy of other character states indicates that ossification of the symphysis closely tracks loading regimes. This is evidence against using an adaptive character, based on a hypothesis of adaptation that is reasonably well-supported and a pattern of distribution that suggests adaptation as a cause of homoplasy. However, the direction of character change for the mandibular symphysis suggests a more complex interpretation. While increased ossification appears to be prone to homoplasy, decreases in ossification are never observed in primates. In a scheme that weights transformations rather than whole characters, increased ossification would be given low weight, and decreased ossification would be given an extremely high weight, essentially to force it never to occur in phylogenetic analysis. Ravosa (1999) put forward this argument for the phylogenetic utility of symphyseal fusion, suggesting that it is an irreversible transformation series. Essentially, symphyseal fusion creates a single structural unit (sensu Schwenk, 2001) from the component halves of the mandible, and canalization of this structure may lower the potential for subsequent separation. For example, although callitrichids have ‘‘no good functional reason’’ to possess a fused symphysis, they retain the structure (Ravosa, 1999: 74). Ravosa (1999) also gave greater weight to ossification of the symphysis than to some other characters, such as premolar loss, in interpreting the relationships of anthropoid taxa. The

basis for this interpretation is the necessity of change in two loading regimesddorsoventral shear and wishboningdthat combine to cause selection for a fused symphysis. Furthermore, these loading regimes correlate with the higher temporomandibular joint of anthropoids, taller ascending ramus of the mandible, and more vertically oriented masseter muscles (Ravosa, 1999). In these respects, fusion of the mandibular symphysis is a ‘‘complex’’ character because it is functionally integrated with several different aspects of skull morphology. The array of characters related to mastication that includes the fused mandibular symphysis may constitute an evolutionarily stable configuration for anthropoids. Examples of ESCs in other taxa provide an analogy for a set of characters with a clear functional basis that nonetheless maintain a stable configuration across a range of diets and rarely undergo reversal (Wagner and Schwenk, 2000; Schwenk, 2001). According to this hypothesis, fusion in strepsirrhines is a straightforward response to increased loading or a by-product of size, while the evolution of a fused mandibular symphysis in anthropoids is a more complex phenomenon related to skull shape as a whole. Whether these hypotheses are confirmed or rejected, the mandibular symphysis illustrates the context-specific nature of most arguments about how morphological characters relate to phylogeny. In a sense, each character state of the symphysis must be interpreted on its own regarding the likelihood of response to external selection, its links to other features, and its stability once evolved. Tooth comb The tooth comb is a synapomorphy of the strepsirrhine clade, although it is modified or lost through tooth reduction or loss in Daubentonia and some indrids. This structure is thought to promote grooming behavior by collecting pheromones that are transferred to the vomeronasal organ (BuettnerJanusch and Andrew, 1962; Szalay and Seligsohn, 1977; Rose et al., 1981; Rosenberger and Strasser, 1985; Asher, 1998). It presumably originated as an adaptation. All evidence suggests that the tooth comb was present in the last common ancestor of crown lemuriforms, as reconstructed from phylogenies determined by Yoder, (1994; Yoder et al., 1996) and Seiffert et al. (2003). Modification of the constituent teeth in some strepsirrhines demonstrates the retention of genetic variation in these taxa and the possibility of independent selection on each tooth. The structure can clearly be lost or undergo ‘‘reversal.’’ As a result, the tooth comb is not so much a character as a set of characters. The resulting pattern is that of a functional complex (Bock and von Wahlert, 1965) or an evolutionarily stable configuration (Schwenk, 2001), where strong selection on the constituent characters ensures integration and correct functioning of the complex. Recent phylogenetic analyses of primate morphological data have treated the tooth comb both as a set of independent character states and as a named character, the tooth comb (Ross et al., 1998; Seiffert et al., 2003). In Ross et al.’s

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(1998) data set, the character matrix shows that the four taxa in the analysis that have a six-tooth tooth comb have identical character states for all but two of the other 23 incisor and canine characters scored for these taxa (three characters were not scored because the tooth comb rendered them inapplicable; Fig. 2). In Seiffert et al.’s (2003) analysis, 14 extant strepsirrhine taxa were represented, and all possess a tooth comb. Of a total of 15 characters used to describe incisor and canine morphology, all but two are invariant across this group. One character is the number of incisors, which is reduced in the only indrid in the analysis, Propithecus. The other variant character in extant strepsirrhines is the form of the lingual cingulum of the mandibular first incisor. Otherwise, this pattern, like that in Ross et al.’s (1998) data set, suggests that presence of a tooth comb dictates incisor and canine morphology to some extent. However, of the character states associated with the tooth comb in extant strepsirrhines, only three of them are found exclusively in tooth-combed taxa. These are the tooth comb itself, a canine paracristid that is oriented in line with the buccal face of adjacent incisor, and high-crowned but very procumbent lower canines. In other words, some other taxa have at least one of the atomized traits of incisor or canine morphology without possessing a tooth comb. Apparently, evolution of features associated with a tooth comb occured in a piecemeal fashion, rather than all at once at the base of the strepsirrhine clade. Such a pattern is typical of character distributions used elsewhere to argue for the presence of ESCs (Wagner and Schwenk, 2000; Schwenk, 2001). The characters constituting the ESC are consistent among the taxa that possess it, but individual characters vary among taxa that have not evolved the entire configuration. Furthermore, while the tooth comb maintains the same function and biological role in taxa that possess it, the ‘‘environment’’ varies widely among them. The tooth comb is a mediator of social interaction, but it is present in strepsirrhine taxa that vary from relatively solitary lifestyles to multimale-multifemale groups (Fleagle, 1999). Therefore, it is not correlated with or adapted to any particular social

Lower incisors Galagoides Lemur Microcebus Nycticebus

Canines

123456789012345678901234 100102912012111010001099 100002912012111010001099 100102912012111010001099 100102912012111000001099 Tooth comb

Fig. 2. Lower incisor and canine character states for extant strepsirrhines included in Ross et al.’s (1998) phylogenetic analysis of primates. Character 13 is presence of a tooth comb, but with the exceptions of Character 4 in Lemur and Character 17 in Nycticebus, the four taxa have identical characterstate distributions for all incisor and canine characters. In taxa lacking a tooth comb, such as adapids, omomyids, and anthropoids, there is more variation among species in these character states. Characters 7, 23, and 24 were not scored (state ¼ ‘‘9’’) because the tooth comb renders the character-state descriptions inapplicable. Similar results obtain for a larger number of strepsirrhine taxa in Seiffert et al.’s (2003) analysis.

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system, although it is generally adaptive in the context of collecting liquid scents (Rosenberger and Strasser, 1985). In taxa that modify or lose the tooth comb, a testable hypothesis is that selection for masticatory function of the anterior teeth led to a breakdown of the ESC. Description of the tooth comb as a number of separate characters contrasts with the way that the postorbital septum has been treated in the same analyses, even though both structures require integration of features that are genetically independent (or at least exhibit that pattern). One reviewer of this paper responded to this example by saying it would be perfectly reasonable to eliminate all of the constituent tooth comb characters that do not vary in strepsirrhines (only in those taxa). In other words, it would be consistent to treat both the tooth comb and a structure like the postorbital septum as single characters. On the other hand, Ross et al. (1998) and Seiffert et al. (2003) retained a number of separate characters to describe the tooth comb because they were observed to vary independently among nonstrepsirrhines. To me, postorbital structures and the tooth comb illustrate an important contrast in adaptive functional complexes. Postorbital structures could conform to the ‘‘same’’ mechanical unit in response to multiple kinds of selection pressure, and this should increase the frequency of homoplasy. Individual components of postorbital structures have for the most part not been used in phylogenetic analysis. For the tooth comb, however, its constituent characters can be observed in some taxa without the full ‘‘tooth comb’’ character complex, and therefore the 15e20 incisor and canine characters are often treated independently. These characters have a pronounced effect on phylogenetic interpretation, but only when the tooth comb constrains them to form a stable complex in strepsirrhines. As isolated features outside of strepsirrhines, they are highly homoplastic. Talar morphology in strepsirrhines A number of wrist and ankle characters support a strepsirrhine clade that includes fossil adapids (Dagosto, 1985; Szalay et al., 1987; Beard et al., 1988; Dagosto, 1988; Gebo, 1988; Dagosto and Gebo, 1994). Most of these are similar across taxa and rare in nonprimate mammals. One example of these characters is the lateral talar slope (slope of the talofibular facet). A gradual slope in strepsirrhines is derived and contrasts with the more vertical orientation of the lateral surface of the talus in haplorhines, some plesiadapiforms, and tree shrews. The pattern of distribution of the laterally sloping talofibular facet is noteworthy, as it occurs in taxa with diverse locomotor repertoires. In Gebo’s (1988) analysis, this character was not implicated in climbing, foot rotation, or leaping. Leapers such as galagos and indrids diverge to some extent from other strepsirrhines but still maintain a more lateral slope than haplorhines. The talar slope thus seems to be phylogenetically informative, and Dagosto and Gebo (1994) gave it ‘‘medium weight’’ in a weighting scheme reflecting a priori confidence in

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homology and a posteriori accounting for homoplasy. The distribution of other traits sheds some light on the role of the lateral talar slope. The character matrix used by Dagosto and Gebo (1994) shows that the five talar characters are not in general highly correlated (different taxa present different combinations of character states). However, the four strepsirrhine taxa (notharctines, protoadapines, adapinans, and lemuriforms) all have the same suite of talar character states for each of the five characters (Fig. 3). In other words, talar morphology is consistent across these taxa, forming a stable configuration that is not present in haplorhine taxa. A similar pattern is present among the seven tibial characters: each of the strepsirrhine taxa has the same complex of character states, while haplorhine taxa reveal a variety of trait combinations. Dagosto and Gebo (1994: 581), following Dagosto (1985), noted that the distal tibia in strepsirrhines ‘‘is characterized by a set of traits that allow a considerable degree of rotation between the tibia and fibula during flexion and extension of the upper ankle joint.’’ This shared function probably accounts for the consistent pattern of tibial traits in strepsirrhines, and talar morphology is a part of the same functional complex.

Put in that context, the lateral talar slope appears to be an adaptive trait. However, this is a different kind of ‘‘adaptive’’ than a character that responds readily to selection. The phylogenetic information available in the lateral talar slope derives from its stability across taxa, particularly across taxa with different locomotor repertoires. What seems like a contradiction is actually an example of how an adaptive complex can maintain stability through selection for integration of its constituent parts. Talar and tibial morphology of strepsirrhines likely fits the description of an ESC offered by Schwenk (2001) and exemplified by the tooth comb, discussed above. While this is essentially a hypothesis to explain the distribution of the lateral talar slope, it reveals problems in dichotomizing adaptive and nonadaptive traits. Homoplasy may be expected in traits that are responsive to external selection. Adaptive traits that remain stable because of the need to maintain functional integration are likely to be phylogenetically informative. However, while they may be buffered against selection, they are not neutral. The lateral talar slope is a good example of such a trait, as its distribution would not immediately suggest a functional role, but its relationship to surrounding characters supports that inference.

T1

Prehensile tail

T3 T4 T5 T6 T7 A1 A2 A3 A4

Platyrrhine

Apidium

Tarsius

Omomyids

Notharctine

Lemuriform

Protoadapine

Adapinan

Primitive

A5

Fig. 3. Character-state distributions for ankle and tibial characters in taxa analyzed by Dagosto and Gebo (1994). Uniformity among the adapids and strepsirrhines supports the view that these states represent an integrated complex in these taxa. Character A2 is the slope of the fibular facet, or lateral talar slope, discussed in the text. Each shade indicates a character state, with half-filled circles indicating the presence of multiple character states in a group. Phylogenetic relationships are from Ross et al. (1998). Missing circles indicate missing data for protoadapines.

The prehensile tail is a synapomorphy of atelines and occurs independently in a different form in Cebus (e.g., Ankel, 1972; Rosenberger, 1983; Lemelin, 1995; Garber and Rehg, 1999). It is an excellent example of how character definition affects interpretations of homoplasy (Lockwood and Fleagle, 1999). Defined in broad terms, a functionally prehensile tail is homoplastic in platyrrhines and in other South American mammals. It may be favored by natural selection because of canopy structure in South American forests (Grand, 1972). If only tail function were used in a phylogenetic analysis, Cebus might emerge incorrectly as the sister group of atelines (depending on how the analysis is conducted), and the functional significance of the feature would be linked to its pattern of homoplasy. However, the structural components of the tail vary across primate taxa. In addition to the lack of a tactile surface, Cebus does not have the specializations in musculoskeletal anatomy possessed by the atelines, and its tail is relatively short (Ankel, 1972; Rosenberger, 1983; Lemelin, 1995; Johnson and Shapiro, 1998). In a phylogenetic analysis of both morphological and molecular data, Horovitz et al. (1998) used one attribute of the prehensile tail (its glabrous surface) as a character, and in this usage, atelines are the only taxa to have it. That approach is analogous to treating all characters associated with the prehensile tail as a single character. As a functional complex, however, the prehensile tail incorporates more than one character (Ankel, 1972; Lemelin, 1995). Although the anatomical details have not been explicitly incorporated into a formal phylogenetic analysis, they played a role in rejecting structural homology of the prehensile tail between Cebus and the atelines (Rosenberger, 1983).

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Issues concerning the prehensile tail follow closely on the discussion above concerning the tooth comb. Quantitative variation among atelines in characters such as tail length (Rosenberger, 1983) illustrates that genetic variation is retained to allow modification of components of the prehensile tail. Without demonstration of a genetic constraint on tail morphology, different aspects of prehensile tail morphology should be treated as independent targets of selection and coded as different if they exhibit different shapes. If this approach is taken, the fact that Cebus and atelines all have prehensile tails in a broad sense does not present a problem for phylogenetic interpretation (in essentially the same way that birds and bats having wings does not present a problem for phylogenetic interpretation). Such an approach would identify a smaller number of similarities in anatomy between Cebus and atelines, and those that do exist would be revealed as homoplastic. If the prehensile tail were excluded from a phylogenetic analysis entirely, on the basis of broad convergence in mammals, then some of the best morphological evidence for ateline monophyly would also be excluded. In other words, the prehensile tail is simultaneously functional and phylogenetically informative. Implications of character examples The characters described above provide examples of characters or sets of characters that diagnose major primate clades uniquely (postorbital closure, tooth comb, talar morphology), characters that are synapomorphic of primate clades but also found in other mammalian groups (postorbital bar), characters that are homoplastic in general but synapomorphic for some primate clades (mandibular fusion, tympanic morphology), and a character that appears to be homoplastic if defined in broad functional terms, but which is a unique synapomorphy if defined in specific anatomical terms (prehensile tail). These patterns of evolution argue against sweeping statements that adaptive characteristics are generally too susceptible to homoplasy to be useful in phylogenetic analysis. Although the adaptive component has not always been adequately demonstrated, some of these characters are clearly synapomorphic of major clades and at the same time functionally important. For morphologists the question is therefore not whether adaptive characters provide phylogenetic information, but how they provide phylogenetic information. For the strepsirrhine character examples, functional integration seems to play a key role in producing the stability necessary for a synapomorphy to be preserved across a wide range of taxa. The constituents of tooth comb and talar morphology vary widely and homoplastically outside of strepsirrhines, as seen in the phylogenetic analyses of Ross et al. (1998), Seiffert et al. (2003), and Dagosto and Gebo (1994), so none of the individual features emerge as particularly phylogenetically informative across primates as a whole. Within strepsirrhines, however, the isolated characters are for the most part stable and integrated into a functional complex. For these examples, it is important to separate the roles of external selection and internal selection in developing expectations for whether

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characters will be homoplastic. External selection may be the genuine source of much homoplasy, but internal selection (i.e., selection for integration) may lie behind phylogenetically informative complexes such as the strepsirrhine tooth comb and ankle. Other aspects of primate anatomy have long been discussed in similar terms. For example, Luckett (1982) pointed out that fetal membrane features are highly correlated with each other in haplorhine primates but not in other eutherian mammals. To him, the correlation itself was strong support of haplorhine monophyly, and he argued against those who suggested that the characters not be treated separately (Schwartz, 1978). Luckett (1982: 293e294) concluded: ‘‘The development and functional correlation of these shared, derived traits in haplorhine primates is a rare occurrence in other eutherians, and identification of such functionally integrated character complexes is of great value in corroborating hypotheses of monophyly in a weighted scheme of phylogenetic analysis.’’ Such complexes are by definition clade-specific, and the specificity of patterns of homoplasy also comes through in the other characters reviewed here (see also Lockwood and Fleagle, 1999). For the tympanic structures, postorbital bar, and symphyseal fusion, the level of homoplasy depends on how broad the ingroup is. One could hypothesize that a transition occurs in the evolution of these features, during which each complex of characters ceases to be a collection of features subject to independent selection. Instead, the complex is maintained through selection for integration and stability [i.e., they become an evolutionarily stable configuration (Wagner and Schwenk, 2000; Schwenk, 2001)]. For example, symphyseal fusion may be stable in anthropoids because of a set of functional constraints evolved in that group (Ravosa, 1999). Models of the evolution of integration also clarify the process of character evolution when functional complexes evolve (Cheverud, 1996). Assembling a structure like the tooth comb in evolutionary terms requires substantial modification of underlying covariance among characters and is in that sense ‘‘difficult.’’ On the other hand, it is ‘‘easy’’ to make use of existing patterns of covariance to produce a variety of shapes through size change or heterochronic processes or modifying an existing functional complex in relation to changing environment. These latter processes are what is thought to lie behind the oft-discussed examples of homoplasy in primates and other animals (Wake, 1991; Lockwood and Fleagle, 1999; see also discussions and references in Schluter, 1996; Marroig and Cheverud, 2001, 2005). As explanations of events a posteriori, these are hypotheses that can be tested. But what role do these observations have in making predictions about character performance (i.e., in selecting or weighting characters)? Unfortunately, even for the characters discussed here in detail, there is little correspondence between what one might ‘‘expect’’ in terms of homoplasy and the patterns of character evolution that actually occur. Postorbital structures and tympanic morphology illustrate this point well. The postorbital bar is a case in which different functional regimes can produce the same structure, as is evident in the homoplasy of postorbital bar evolution in

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mammals (Heesy, 2005). It may indeed be a good synapomorphy of primates, and it exhibits no homoplasy within this group, but such a pattern can only be observed after phylogenetic analysis. For anthropoids specifically, the same is true for the postorbital septum. On the other hand, tympanic morphology shows substantial homoplasy among primates. All three of these characters are mechanical units in that they require integration of separate morphogenetic precursors, and such mechanical units can subsume a range of variation in constituent parts (Schwenk, 2001). In other words, the form of the structure as a whole is more important than the form of its individual elements, and the functional unit becomes the character. Contrast such structures with the tooth comb, for which researchers have typically used a long list of constituent characters to describe its form, and all of the separate characters are stable in taxa that possess the tooth comb. Because mechanical units raise problems of equifinality, we might expect them to be prone to homoplasy, but for these examples, that is only true for tympanic morphology. And again, for a narrower range of taxa, tympanic morphology would still be informative. Fusion of the mandibular symphysis in primates also follows this patterndlike many characters, it is simultaneously ‘‘good’’ and ‘‘bad’’ in its phylogenetic signal. Contingency plays a role in the pattern of character evolution, and for this reason it would be wrong to overemphasize single examples. Nonetheless, the characters reviewed here highlight two contradictory themes that seem to run through the morphological phylogenetics literature. On the one hand, patterns of adaptation and functional integration often explain why morphology can be stable and phylogenetically informative. On the other, it may be impossible to discover these patterns prior to a phylogenetic analysis. What, then, are the practical implications of this discussion for character analysis and other decisions made in phylogenetic reconstruction? Three potential responses in character analysis are (1) to adopt an atomistic approach to morphology, based on the failure of a priori predictions to offer firm evidence for character selection, and assume that details will simultaneously allow independent characters to be identified and complex functional units to carry an appropriate amount of weight in the analysis; (2) to settle on a balance of a priori and a posteriori character weighting that takes into account a range of information about character complexes and the patterns of previous results; or (3) to refrain from using morphological characters in phylogenetic analysis until methods are developed to correct for the unpredictable effects of selection. The first option largely corresponds to current practice, and the second option is expressed in some analyses that attempt character weighting or character selection. The third option is the most ambitious and perhaps unachievable approach, at least if one seeks to incorporate the fossil record (see Felsenstein, 1988, 2002). Put more simply, character evolution can only be understood from an interchange among phylogenetic, functional, and developmental analyses. Even though individuals differ in their ultimate conclusions, this interchange can readily be seen throughout the recent literature and in papers published together here (Begun, 2007; Collard and Wood, 2007; Hall,

2007; Leigh, 2007; Masters, 2007; Rendall and Di Fiore, 2007; Strait et al., 2007; Williams, 2007). Conclusions When I began this study, it was with the intention of comparing the phylogenetic utility of adaptive and neutral characters. However, recognition of the near ubiquity of ‘‘adaptive’’ characters in primate phylogenetics, and the different meanings of this word, shifted the focus to character complexes. Three main conclusions result. First, the philosophy that adaptive characters are generally poor phylogenetic characters is flawed. In some cases, adaptation is the explanation for homoplasy, but the conclusion that adaptive characters are particularly prone to homoplasy does not follow logically or empirically. Instead, adaptive characters can be phylogenetically informative by virtue of stabilizing selection, particularly when stabilizing selection is ‘‘internal,’’ that is, based on integration of adaptive characters as evolutionarily stable configurations (sensu Wagner and Schwenk, 2000). Following on this argument, the second conclusion is that we will benefit from more thorough investigation of why and how integrated complexes form. Primates show examples of stable configurations of characters as synapomorphies of clades; the tooth comb is an excellent example, and the strepsirrhine ankle may be as well. In cases such as these, morphological integration is not a ‘‘problem’’ for phylogenetic analysis. Instead, it may explain the stability of phylogenetically informative characters. Finally, and somewhat to the contrary, the case studies on the whole show the difficulty in forming predictions about a character’s phylogenetic signal. Explanations of patterns of character evolution are often clade-specific, not allowing for a simple framework of character selection and/or weighting. For several of the characters discussed here (postorbital bar and septum, tympanic morphology in general, and the fusion of the mandibular symphysis) empirical patterns of character evolution would not easily be predicted. Many characters are homoplastic in some groups but phylogenetically informative in others. These are not new conclusions. While the basis of adaptation is made more explicit today, and the effects of stabilizing selection and developmental canalization are understood in more detail, the observations in this paper recall earlier discussions of character use in phylogenetics (e.g., Bock, 1977; Hecht and Edwards, 1976; Szalay, 1977; Neff, 1986). Hennig (1966: 21e22) noted that understanding of phylogeny comes through ‘‘reciprocal illumination,’’ a ‘‘checking’’ and ‘‘rechecking’’ of the data. In the process of identifying, selecting, and weighting characters, there is still ample room for evaluating the evolution of different types of structures and the expectations we form from theory. Acknowledgments I am grateful to participants in the homoplasy workshop for conversations that encouraged me to pursue the topics discussed here. The workshop was supported by the Wenner-Gren

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