Phylogenetic Species, Nested Hierarchies, and Character Fixation

Cladistics 16, 364–384 (2000) doi:10.1006/clad.2000.0141, available online at http://www.idealibrary.com on

Phylogenetic Species, Nested Hierarchies, and Character Fixation Paul Z. Goldstein*,1 and Rob DeSalle† *Division of Insects, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, Illinois 60605; †Department of Entomology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024 Accepted July 15, 2000; published online January 1, 2001

Cladistic mechanics and ramifications of various species concepts rooted in phylogenetic theory are explored. Published discussions of the phylogenetic species concept (PSC) have been hampered by persistent misconceptions surrounding its ontology and applicability, and by confusion of various incompatible versions of species concepts claiming to follow from Hennig’s (1966), Phylogenetic Systematics, Univ. of Illinois Press, Urbana work. Especially problematic are topology- or tree-based versions of species diagnosis, which render diagnoses dependent on relationships depicted as hierarchically structured regardless of any lack of underlying hierarchy. Because the applicability of concepts such as monophyly, paraphyly, and polyphyly rests ultimately on the underlying hierarchical distribution of characters, representations of tokogenetic or reticulating systems as nested hierarchies are necessarily inaccurate. And since hierarchical representations—even if accurate—of nonrecombining genetic elements need not coincide with the organisms that bear them, tree-based diagnoses are further hampered, except potentially as retrospective tools. The relationship between tree-based species delineations

and the criterion of character fixation is explored. Fixation of characters by which one identifies phylogenetic species is further distinguished from the fixation of character state differences, and the implications of that distinction are explored with reference to the interpretation of speciation events. It is demonstrated that character fixation in alternative species need not coincide with the achievement of reciprocal monophyly. While the PSC retains shortcomings, some of the more frequently criticized aspects of the PSC are functions of sampling that are no more problematic than for any basic systematic endeavor. 䉷 2000 The Willi Hennig Society

INTRODUCTION Since the publication of Hennig’s (1966) work, there have appeared several versions of species concepts originating within phylogenetic theory. Most have in common the notion of species as primary units of evolutionary study. However, as the power of phylogenetic information to address evolutionary questions has become increasingly well recognized, and as the generation of molecular phylogenetic data in particular has become increasingly facile, phylogenetic methods have enjoyed growing popularity outside the realm of

1

To whom correspondence should be addressed. Fax: (312) 6657754. E-mail: [email protected].

364

0748-3007/00 $35.00 Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Species Hierarchies

systematics proper. Specifically, methods for generating nested hierarchical depictions of relationship are applied with increasing frequency at intraspecific and even within-population levels (Avise, 1989, 1994, 1999; Avise et al., 1987; Avise and Wollenberg 1997; Crandall and Fitzpatrick, 1996; Moritz, 1994a,b, 1995). Such applications have been widely endorsed, even within the systematics literature (de Queiroz and Donoghue, 1988, 1990; Baum and Donoghue, 1995), where the idea that monophyly is universally applicable to species as well as higher taxa originated. This trend has persisted, as have a wide variety of disparate views on the phylogenetic species concept (PSC), despite recent critiques by Nixon and Wheeler (1990), Davis and Nixon (1992), Doyle (1995), Luckow (1995), and Brower et al. (1996) to the effect that hierarchical analyses can be misleading when the terminals in question are not themselves related hierarchically. This observation drew in part from Hennig’s frequently reproduced figure (1966, Fig. 6) distinguishing reticulating, tokogenetic relationships from phylogenetic relationships that are accurately depicted as nested hierarchies, i.e., monophyletic groups. Nixon and Wheeler (1990) and Davis and Nixon (1992) examined this distinction with specific reference to the PSC, formalizing the connection between character state distributions and the descriptions of the PSC by Eldredge and Cracraft (1980), Nelson and Platnick, (1981), and Cracraft (1983) as the minimal aggregate of individuals for which phylogenetic interpretation of cladistic analyses is appropriate. Most important were their twin observations that (1) hierarchical results necessarily obtain from cladistic analyses and (2) the interpretations of such analyses as hypotheses of phylogenetic relationship are confounded by any lack of underlying hierarchy. The identification of that level as that of the phylogenetic species forms the cornerstone of current thinking with respect to the PSC. Unfortunately, the application of the PSC is not necessarily as straightforward as it seems. The PSC is perhaps better thought of as a “criterion” than a concept, because the abstract requirement of understanding the boundary between hierarchical and nonhierarchical systems does not necessarily indicate an obvious means of identifying where that boundary lies (Mayden, 1997; Brower, 1999; de Queiroz, 1998). Nixon and Wheeler (1990) and Davis and Nixon (1992) observed that since the delimitation of species requires fixed attributes by which they can be recognized, and

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

365

since our assessment of phylogenetic relationship depends ultimately on the heritability of characters, a strictly character-based operation prior to cladistic analysis is desirable. Davis and Nixon’s (1992) suggestion to that end was population aggregation analysis (PAA), which identifies minimal aggregates of individuals united by fixed traits, equivalent to characters in their terminology. The purpose of PAA is to avoid presentations of spurious tree structure by aggregating units into minimally inclusive terminals defined by diagnostic features. Proponents of other phylogenetic species concepts have rejected the character-based diagnostic approach in favor of a cladogram- or tree-based operation (Donoghue, 1985; de Queiroz and Donoghue, 1988, 1990; Baum and Donoghue, 1995; Baum and Shaw, 1995; Moritz, 1994a,b, 1995; Olmstead, 1995), arguing variously that hierarchical analyses are useful at any level, that hiearchy-specific terms, such as monophyly and synapomorphy, are similarly unbounded, and that relying strictly on characters to reconstruct phylogenies is ahistorical and, by implication, “anti-evolutionary.” It follows from that characterization that character state distributions might formally be divorced from historical inference. Other authors (e.g., Maddison, 1995, 1997; Avise and Wollenberg, 1997) have emphasized the prevalence and concatenation of nested hierarchies throughout nature, in some cases arguing that conflicting depictions of such hierarchies are equally accurate in alternative contexts (O’Hara, 1993), and in others suggesting that information from elements with different histories (e.g., different genes) might be consensed to form compromise cladograms approximating coalescence events at infraspecific levels (Baum and Shaw, 1995). These latest debates have also occasioned the resurrection of numerous philosophical issues pertaining to the identification and meaning of species and species names (e.g., Frost and Kluge, 1994; Davis, 1995; Doyle, 1992, 1995; Graybeal, 1995; Luckow, 1995; Maddison, 1995, 1997; Claridge et al., 1997 and references therein; Harrison, 1998; Baum, 1999). Like much of the long history of publication surrounding the species problem, most of these authors [with the exception of Frost and Kluge (1994) and most recently Baum (1999)] chose not to confront the mountain of difficult philosophical problems surrounding species, but rather to confine

366

their discussions to particular operational or philosophical points. This paper is no exception. In this essay we confine the bulk of our discussion to the mechanics of species delimitation as they relate to treeversus character-based criteria. However, to the extent justifications for various phylogenetic species concepts have overlapped with respect to certain evolutionary and philosophical stances (see Appendices A and B), we will also emphasize distinctions between species concepts as they relate to the generalizability of phylogenetic species concepts broadly and of characterbased phylogenetic species concepts in particular. That discussion will serve as a prelude to our narrower treatment of tree mechanics and character fixation.

PLURALISM AND GENERALIZABILITY Many remain unsatisfied with the PSC (e.g., de Queiroz and Donoghue, 1990; Vrana and Wheeler, 1992; Frost and Kluge, 1994; Baum and Donoghue 1995; Baum and Shaw, 1995; Mallet, 1995; Templeton, 1998) as well as with its operational prerequisite, PAA (Brower, 1999). Objections to the PSC have taken several forms, some of which rest on unique interpretations of phylogenetic information—and its limits. Much of the discussion of species concepts during recent decades has been directed at reconciling our notions of species either with how they came to be or how their members interact, that is to say, with either origin or maintenance (Appendix A). The more intricate species concepts proposed were oriented toward the mode of species’ origins. The cohesion species concept (Templeton, 1989) focused on intrinsic cohesion mechanisms; the recognition species concept (Paterson, 1985) focused on fertilization systems; the ecological species concept (Van Valen, 1976a) incorporated putative adaptive zones; and of course the traditional biological species concept of Mayr (1942, 1957, 1963, 1969, 1970) relied on interbreeding potential and was thus limited to biparental sexually reproducing organisms. Avise and Wollenberg (1997), who favor the conceptually synthetic biological species definition of Mayr and Dobzhansky, reprised the argument that species definitions should incorporate microevolutionary information and argued against use of the PSC on grounds that it does not. Like the proponents of the cohesion,

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

recognition, and biological concepts, Avise and Wollenberg (1997, p. 7748) argued that since understanding the mechanisms of evolution requires a knowledge of genetics, then so must an understanding of the units of macroevolution—species—incorporate that knowledge lest it “disregard established genetic principles” and cited Dobzhansky (1937) to that effect. In contrast to this perspective, Allen (1980, p. 359, cited in Løvtrup, 1987) states: “The view that a biologist holds about the nature of species will determine much of what he or she believes about the . . . means by which species arise.” When the identification of species is rooted in presumptions of speciation, we are left with the inverted view that understanding speciation is a prerequisite to defining species rather than a product of that definition. Templeton (1998) appears to concede this point, despite advocating a concept encumbered by theoretical assumptions, but argues that since process gives rise to pattern, process should remain the focus of analytical hegemony. But many would argue that although process necessarily gives rise to pattern, pattern provides the most direct means of exploring process. An understanding of historical pattern must logically precede the investigation of evolutionary process (Nelson and Platnick, 1981; Rosen, 1982; Nixon and Wheeler, 1990; Rieppel, 1992). Following Rieppel (1986) and Luckow (1995), we stress that species delimitation cannot and should not be pursued in terms of speciation lest it be vulnerable to accusations of overt circularity and unrepeatability. As Luckow (1995, p. 591) stated: “[B]y making assumptions about mechanisms of speciation in order to diagnose species, we rob ourselves of the opportunity to test hypotheses about the speciation process itself.” More pointedly, she wrote (p. 597) that “species concepts that proceed from ideas about what particular processes led to speciation will never lead to any resolution of the conflict over species because they are untestable.” We would add that either incorporating process-related information on an ad hoc basis to define species or categorizing such information (as, for example, intrinsic mechanisms of cohesion and so forth) undercuts rather than strengthens the intended generalizability of such approaches. It was the stated intention of the frameworks designed around each of the so-called mechanistic species concepts to account for as much biological reality as possible. But in so doing they encountered a second

Species Hierarchies

and important pitfall to the logical foundation of species analysis: the trade-off between generality and precision, or, phrased differently, between pluralism and generalizability (Appendix A). It should go without saying that the more one incorporates into a definition, the less general it becomes. The less precise the definition, the less useful its service as a tool for empirical discovery. Under the recognition or cohesion species concepts, the incorporation of every fertilization system or isolating mechanism imaginable does not serve to enhance the business of identifying species. If anything it serves to confound that process by introducing virtually limitless fields of exploration into the equation. But the distinction between pluralism and generalizability has not always been forthcoming in reviews of species concepts. Olmstead (1995), Baum and Donoghue (1995), and Baum and Shaw (1995) all object to the premises of the original PSC, occasionally on grounds that would appear to be mutually at odds. In Olmstead’s (1995, p. 62) words: “. . . [T]wo prominent versions of the phylogenetic species concept (e.g., the “PSC” of Nixon and coworkers and the “GSC” of Baum and coworkers) suffer from the same rigid adherence to logical consistency, which proves to be a hindrance to their application.’’ Paradoxically, Olmstead sees logical consistency as an impediment to applicability, but this interpretation is not unique. Baum and Shaw (1995), in fact, also reject the necessity of a singular species concept and follow Mishler and Donoghue (1982) in arguing for pluralism. Baum and Shaw (1995) indicated that an advantage of their “genealogical species concept” was that it was generalizable because of its pluralism. Hull (1997), while arguing the desirability of a singular (or “monistic’’) species concept, failed to acknowledge that the PSC’s strength as a general tool derives from its uniquely character-based formulation (all organisms have characters). Frost and Hillis (1990) and Frost and Kluge (1994) found fault with the operational aspect of strict phylogenetic species delimitation, arguing that any operational approach to delimiting species shoehorns definitions into arbitrary pigeonholes that do not correspond to biological objects of discovery. Some of these arguments distill to the question of whether species are to be viewed as elements serving as guideposts (even arbitrary guideposts) in exploring macroevolution or as “real” entities in nature (objects of empirical discovery) that are best understood

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

367

through explorations of microevolutionary process and whose delimitation can only, therefore, be arrived at through the consilience of conclusions derived from different sources of information (e.g., Clausen et al., 1940, 1945, 1948; Clausen and Hiesey, 1958; Appendix A). To the extent authors disagree on this matter, their arguments are entirely at cross-purposes. It must be recognized that there is a discrepancy between species delimitations bearing numerous or far-reaching ontological claims and those bearing few such claims. Failure to recognize that discrepancy has led to some rather fruitless debates. Olmstead, for example, criticized population aggregation analysis (PAA; Davis and Nixon, 1992), which was intended to identify minimally suitable units for phylogenetic analysis, on the grounds that aggregates united by the method need not correspond to actual entities in nature, a purpose for which the method was never designed. The issue of species’ “reality,” explored by authors such as Frost and Hillis (1990) and Rieppel (1994), is central to decisions of how to approach species delimitation, for only if species have some form of ontological existence can we presume to “test” their boundaries. If, as most would argue, our species delimitations are to reflect reality of some kind in nature—reality that is either independent of our understanding or takes the form of a historical entity—then their discovery is not easily forwarded either by strictly operational debates or by the generation of new vocabularies (Frost and Hillis, 1990). It is only because certain species definitions, e.g., the biological species concept, carry such ontological claims that notions of cryptic or hybrid species become necessary, and it can easily be shown that any such ontological framework requires the creation of a novel vocabulary that is not easily transferred to other systems. Templeton’s concept, for example, appears to require continuous revision of what constitutes a cohesion mechanism and how one may test it (eg. Templeton, 1989, 1998). Adoption of Donoghue’s (1985), Graybeal’s (1995), or Olmstead’s (1995) suggestions requires novel terms (metaspecies, ferespecies, and plesiospecies, respectively) to accommodate entities that cannot be assigned to species under any of these frameworks (Nixon and Wheeler, 1990). Such requirements that each kind of natural entity be accommodated by a given species concept harken back to Mayr’s system, which invoked numerous such corollaries (semispecies, sibling species, etc.).

368

It is the process-based suggestions that have inevitably led to disputes over pluralism and generalizability (Appendix A). Several authors (Mishler and Donoghue, 1982, Holsinger, 1984; Harrison, 1998) have argued accurately that a variety of natural entities are currently referred to as species. While some have taken this observation as an opportunity to call for pluralism in the endorsement of various species concepts, Harrison (1998) has crafted an “ontogeny” of species concepts, with each corresponding to a stage or a range of stages on the road from initial vicariance to reproductive isolation. Mayden and Wood (1995) have also argued that different species concepts are logically applied to different kinds of natural entities. Of course context dependence is an important corollary to parameters that have been invoked in discussions of species (de Queiroz and Donoghue, 1988; Holsinger, 1984; Harrison, 1998). However, it remains to be demonstrated how such perspective shifts should impact the delineation and naming of species. Baum and Shaw (1995), Maddison (1995, 1997), Avise and Wollenberg (1997), and Harrison (1998) all observed the existence of hierarchies at multiple levels. Like Baum and Shaw (1995), Maddison (1995, 1997) explored the “forest” of trees that occurs along or within cladogenetic pathways, suggesting that such trees—whose terminals are individual, tokogenetically related organisms—collectively comprise a phylogenetic representation among species. A cladistic phylogeny is thus an amalgam (or a “cloud’’) of trees that conflict with one another at the level of individual relationships. Like Avise, Maddison is accurate so far as it goes, but his point does not in itself enhance our ability to infer common ancestry or delineate species. For the purposes of this discussion, we wish to acknowledge that there exists a range of entities in nature that vary in the degree to which they correspond to what we call “species.” However, that variance should not, in our opinion, enter into the business of identifying, naming, or proscribing those species for phylogenetic analysis, operations we feel should logically precede the investigation of natural order. This is not to say we endorse anti-evolutionary or anti-historical views. On the contrary, we view species as important and nonarbitrary empirical anchors by which evolutionary investigations can proceed. The issue is not

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

simply one of conflating cause and effect, but of identifying the appropriate forum from within which to examine pattern and process. Taking the PSC as the foundation for such a framework, as Cracraft (1983, 1987, 1989) and others have urged, allows us to explore the interaction between character fixation events and reproductive isolation. The BSC and its process-based relatives do not allow such exploration because the minimum boundary is not merely in dispute, but actually in flux. Thus it is important not only that generalizability be distinguished from pluralism, but also from inclusiveness. A general species concept is desirable for many reasons, but it is not necessary to incorporate information from every possible field of inference for it to provide a framework from within which to investigate such fields. Species need not be universally equivalent in order to be comparable, nor can they be comparable at every level if the information retrieval system imparted by systematics is ever to succeed. And while it is useful to understand where in the “life history” of a given species (to borrow Harrison’s phrase) a particular species concept might best apply, the acceptance of one uniform concept does not obviate such understanding. Although the study of how reproductive isolation arises is an important one, equating it with the study of speciation per se is perhaps an oversimplification. It does no harm to the microevolutionary study of reproductive isolation to consider it from within a character-based framework, but the damage done to the endeavor of systematics by equating species with process-based definitions is crippling.

PHYLOGENETIC SPECIES AND MONOPHYLY Central to any discussion of phylogenetic species is the interpretation of monophyly. As discussed in the Introduction, disputes over the boundaries of the term monophyly lie at the root of current disagreements over different “versions” of phylogenetic species. Thus various recent authors have appreciated salient features of the PSC, but at times adopted lines of argumentation that confound those features (Appendix B). Baum and Shaw (1995), for example, recognized that

Species Hierarchies

“species reside at the boundary between reticulate and divergent genealogy,’’ but advocate a terminology that denies that boundary. Mayden (1997) and Mayden and Wood (1995) recognize the boundaries of applicability for such concepts as monophyly and paraphyly but advocate the evolutionary species concept of Wiley (1978) on the grounds that it accommodates more of a range of biological entities and has more of a “lineage perspective.” O’Hara (1993) recognized the dichotomy as well, but effectively endorsed a pluralistic approach as a solution to it. The most common source of confusion in discussions of the PSC appears to be the conflation of tree-based and character-based criteria, a distinction highlighted—albeit with opposite interpretations—by Baum and Donoghue (1995) and Luckow (1995). Mallet’s (1995) interpretation was not unusual. He did not distinguish character-based from tree-based versions of “the” PSC (Cracraft 1997; Goldstein et al., 2000; Appendix B), and this led him to question the rationale of the PSC as circular, since it does not make sense that one would need to know the relationships among things before being able to identify the things in question. While his point is accurate so far as it goes (it echoes Nixon and Wheeler’s 1990 message to the same effect), it does not apply to the original definition of the PSC, but rather to variants of it—specifically those of Donoghue (1985), Baum and Shaw, (1995), and Ridley (1989)—the authors who themselves chose not to apply the distinction between hierarchical and nonhierarchical systems. Mallet (and others) simply confused several contemporary but unrelated species concepts that are “phylogenetic” in some very broad sense (see Baum, 1992; de Queiroz, 1998). Characterizations similar to Mallet’s have since become embedded in the conservation literature as well. The most recent (1997, p. 61) edition of Meffe and Carroll’s Principles of Conservation Biology refers to Cracraft’s (1983) PSC as the “cladistic” species concept and confuses it with the monophyletic species concept of Donoghue (1985): The phylogenetic species concept (PSC), sometimes called the cladistic species concept . . . argues that classification should reflect the branching, or cladistic, relationships among species or higher taxa, regardless of their degree of genetic relatedness . . . The PSC is based on the concept of shared derived characters, called synapomorphies. If two or more individuals or populations share a derived character (defined as a unique character

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

369 not found in other, more distantly related groups), then they are assumed to be more closely related than individuals or populations lacking that character.

Although these authors may have misapprehended the original PSC, their characterization echoes the broad interpretations of monophyly (and related terms) adopted by various systematists. But as Hennig and others since have explained (Platnick, 1977; Willmann, 1983, cited in de Queiroz and Donoghue, 1988; Ax, 1987), the notions of monophyly and paraphyly, and the attendant character-based terms “synapomorphy” and “symplesiomorphy,” have no place in reticulating, nonhierarchical networks representing relationships among interbreeding individuals. At issue here is the relationship between characters and hierarchic groupings and the range of systems to which such groupings are applicable. Nixon and Wheeler (1990), Davis and Nixon (1992), Luckow (1995), and Cracraft (1997) were careful to tie their conceptualizations of species explicitly to characters and to stress that only in this way can observed characters serve as empirical tests of species. Baum and Donoghue (1995) redirected the discussion by distinguishing “character-based” approaches from “history-based” approaches, implying that advocates of the former are somehow anti-evolutionary because of their reliance on observations alone. In the remainder of this paper, we explore this distinction by focusing on the alleged shortcomings of the PSC that have to do with understanding the relationships—hierarchical and otherwise—among individuals prior to character fixation. Several phylogenetic species concepts and many of the intraspecific applications of phylogenetic methods have chosen not to take into account the issue of underlying hierarchy (or lack thereof), interpreting cladistic analyses as phylogenetic reconstructions regardless of any lack of underlying hierarchical structure. As such, terminal proscription is rarely discussed in papers devoted to intraspecific phylogeography because the alleged strength of the approach therein is to recover hierarchical relationships below traditional taxonomic boundaries. Several authors (especially de Queiroz and Donoghue, 1990, and Avise, 1999) have explicitly defended the use of cladistic methods at low levels of inference, arguing that species should be “held to the same standard” as higher taxa (de Queiroz and Donoghue, 1990) or that such applications are accurate

370

so long as they are confined to nonrecombining, necessarily hierarchically inherited genomic elements (mitochondrial and chloroplast DNA; Avise, 1999). At the heart of this argumentation is the fact that all life is believed to be connected through patterns of common ancestry. Because of this, so the argument goes, the lines between nested hierarchies and reticulating networks are blurred, if not nonexistent, and hierarchy-recovery operations are equally well suited at all levels. This interpretation denies the discontinuous nature of cladograms as well as the asymmetry between species and higher taxa. That asymmetry is central to phylogenetic systematics. Without a boundary to the reticulating networks, there can be no nested hierarchy and no monophyly. Were systematists to adopt the schema of tokogenetic networks as the framework on which to organize nature, then species, genera, families, and phyla would be both logically and graphically equivalent. Having denied the relevance of characters to inferring history, not only could there be no clear delineations of species, but indeed all of life would have to be considered one polymorphic species (Nixon and Wheeler, 1990, 1992). The proper asymmetry between species and higher taxa has most often manifested in philosophical discussions of whether species are to be viewed as individuals versus classes (e.g., Nelson, 1985; Hull, 1976, 1978, 1980; Rieppel, 1986; Van Valen, 1976b; Wiley, 1989; Ghiselin, 1974, 1987, 1989; Kluge, 1990).2 But it also bears directly on graphic representations of species. The bottom line is that equating reticulating systems with hierarchic systems by the loose application of monophyly and apomorphy serves neither the reconstruction of history nor the resolution of the species problem. Unfortunately, as alluded to earlier, the identification of an actual boundary between reticulate and hierarchical systems is more than elusive, and at least one author (Brower, 1999) has argued convincingly that the best we can do is try to identify which side of the boundary we are on, in any given study rather than pinpoint the

2 That debate has subsided, there appearing to be at least some general agreement that species are individuals. However, it is worth noting that species appear to have properties of both individuals and classes, such that neither term suffices to describe them (Farris, 1985). An analogy may be drawn to the dual nature of light, which exhibits both wave-like and particle-like behavior.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

boundary itself. The problem is perhaps best characterized by what has been termed Woodger’s paradox (Medawar and Medawar, 1983; Hall, 1992; Rieppel, 1994). Woodger argued that since any given organism may belong to only one species, the evolutionary transition between one species and another must occur between two successive generations. Hence, there must be a point where parent and offspring belong to different species. We will return to Woodger’s paradox in the context of character fixation. Following de Queiroz and Donoghue (1988, 1990), Baum (1994), Baum and Shaw (1995) and Baum and Donoghue (1995) attempted to remedy the boundary problem by proposing a new term—exclusivity— designed to replace monophyly in reticulating networks. As has been pointed out by Luckow (1995), Baum’s definition of an exclusive group—one whose members are more closely related to one another than to any individuals outside the group—is identical to Hennig’s (1966) definition of a monophyletic group. Notwithstanding the noble intentions of Baum and Shaw (1995) and Baum and Donoghue (1995) to approach traditional phylogeny reconstruction within reticulating systems, such an approach entails a logical impossibility. The concept of monophyly—and the basis of phylogenetic reconstruction—is the premise of identifying relative recency of common ancestry. The reason that terms such as monophyly and paraphyly lose their meaning when applied to nonhierarchical systems is that, at least for biparental organisms, the idea of relative recency of common ancestry is confounded by the reticulating network that best depicts interconnected parentage. Like Olmstead (1995), who expressed disdain for definitional hegemony, and de Queiroz and Donoghue (1988, p. 317), who referred to the “unnecessary restriction of the concept of monophyly,” Baum (1992) regarded this problem as one of semantics. In fact, the problem is far from semantic, but rather fundamental to understanding the nature of hierarchical structure. Baum’s coining a new term did not solve the problem because the problem is graphic, not definitional. Following Baum (1992), Graybeal (1995) clarified the notion of exclusivity concisely, characterizing the term as necessitated by the uncoupling of two concepts of monophyly below the species level: Farris’ (1974) definition of a monophyletic group (a group that includes a common ancestor and all of its descendants)

Species Hierarchies

and Hennig’s (1966) definition (a group of species in which every species is more closely related to every other species than to any species that is classified outside the group). The latter definition of course represents the arena of ambiguity for reticulating systems. Graybeal suggested that reticulating systems meeting both of these definitions of monophyly are “exclusive.” By definition, however, the second criterion is never met in reticulating systems until cladogenesis has occurred and, once again, we are left with a term that is synonymous with monophyly. The concept of monophyly is attached to a graphic way of representing common ancestry wherein each terminal has a unique and unambiguous placement with respect to other terminals; it is simply not designed to handle other situations. As Bremer and Wanntorp (1979, pp. 624–625) phrased it, “a hierarchical description of a fishing net would be a kind of description indeed but it would certainly be a very poor one.” Another way of phrasing this problem is that polarity—which sits at the nexus of monophyly and apomorphy—is necessarily ambiguous in reticulating networks (Luckow, 1995). This discrepancy is not a shortcoming of the concept, nor can it be remedied by consensing alternative cladograms or by redefining the word, because the problem is not determining the least inclusive monophyletic groups, as de Queiroz and Donoghue (1988) suggest, but finding a criterion for identifying the least inclusive terminals that is external to the analysis. Monophyly at and below the species level has to a growing degree been championed as a possible criterion for species delimitation, particularly in the conservation literature. This practice stems in part from the observation of Avise and his colleagues that for mitochondrial elements, hierarchical relationships among nonrecombining haplotypes in a given population follow a progression from polyphyly, through paraphyly, to monophyly as individual haplotype lineages fail to perpetuate and characters become fixed (Neigel and Avise, 1986; Avise et al., 1987; Avise and Ball, 1990). The practice also appears to derive from the repeated observation that “gene trees” (cladograms based on data from one gene) need not be congruent with each other or with “species trees” obtained by other means, and this in turn has led to suggestions that species delimitations be based on degrees of congruence among such differently generated topologies.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

371

In the case of two “bifurcating” populations, Avise dubbed the stage “reciprocal monophyly” at which point neither species is “paraphyletic” with respect to the other. Interestingly, the Avise progression is partly illustrated in Hennig’s own (1966, p. 31) Fig. 6. Assuming the four females in the “first” ancestral generation of that figure represent distinct mitochondrial haplotypes, cladistic analyses of successive generations in each descendant species (Figs. 1 and 2 ) illustrate the progression from polyphyly to monophyly as mitochondrial haplotypes are extinguished.3 Given four mitochondrial haplotypes in an ancestral generation corresponding to the four females in Hennig’s original figure, and assuming, for the purposes of this example, that the relationships among those haplotypes can be recovered in every successive generation, we can examine the correspondence (or lack thereof) of such “phylogenies” to the organismic relationships themselves and the concordance (or lack thereof) between character fixation and reciprocal monophyly. By descendant generation 3 in Hennig’s figure, each descendant species is “monophyletic” and reciprocal monophyly has been achieved. In this example, reciprocal monophyly and character fixation are simultaneous but this need not be the case, as will be seen. Notwithstanding the liberal use of “monophyly,” Avise’s observation is not in itself flawed, because he christened “infraspecific phylogeography” specifically with reference to mitochondrial DNA—a system that is necessarily hierarchical even in biparental networks. Attempting to interpret a cladistic analysis of successive generations based on character systems other than mitochondria is less tractable because any determinations of relative recency of common ancestry are necessarily ambiguous or spurious (Luckow, 1995). This problem arose—and has persisted—since Moritz (1994a,b) and others suggested that the requirement of reciprocal monophyly be applied to recombining nuclear elements in biparental systems. Potentially, this is a misapplication of hierarchical terminology because the underlying system is not hierarchical. The only

3 Hennig’s internodal view of species entailed a given divergence event marked by the physical or demographic separation of populations that preceded exclusive ancestry and (presumably) character fixation. This view is problematic because any allopatric population would be a species (although not recognizable as such) regardless of character distributions or relationships.

372

Goldstein and DeSalle

FIG. 1. Cladogenetic representation of four maternally transmitted haplotypes in four ancestral and three descendant generations depicted in Hennig’s (1966) Fig. 6. At the center is a redrawing of Hennig’s (1966) Fig. 6. Individuals are numbered from left to right; males are represented by black circles and females by white circles. At the left is a representation of the distribution of maternally transmitted haplotypes (I–IV) maternal lineages from generation A1 through A4. To the right lies a representation of the fate of each haplotype in the three descendent generations D1 through D3. A and B indicate species (in Hennig’s usage) produced by the splitting event. The relationships among the haplotypes in the first ancestral generation (A1) are unknown; ancestral haplotype I precipitates immediately, leaving no female descendants; ancestral haplotype IV disappears after the first generation in descendant species B; ancestral haplotypes II and III survive for the duration of the diagram, each becoming fixed in descendant species A and B, respectively.

problem with applying intraspecific phylogeography to species delimitation when based on nonrecombining elements is the assumption that the “phylogeny” of mitochondrial haplotypes corresponds to the phylogeny of the species that bear them. A within-population “phylogenetic” analysis of mitochondrial elements would almost certainly reveal that any given male individual might be more closely related to maternal cousins than to his own father or son (cf. Baum, 1992; Graybeal, 1995; Goldstein et al., 2000). This example highlights an important corollary to cladistic analysis. A cladogram can be constructed using anything as terminals: organisms, rocks, furniture, etc. But the interpretation of that cladogram as a reflection of evolutionary history requires two assumptions concerning the historical relatedness of the objects in question: cladogenesis and descent with modification. Lack of underlying hierarchy confounds the evolutionary interpretation of cladograms.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

PARAPHYLETIC SPECIES AND POLYMORPHISM Simply stated, the interpretation of reticulating systems through cladograms blurs the understanding of common ancestry. A criticism of both the PSC and its attendant population aggregation analysis is that socalled “paraphyletic species’’—corresponding to Donoghue’s “metaspecies’’—may obtain. Aside from various issues of ambiguity and inaccuracy, such applications require systems of terminology to account for discrepancies between the two kinds of networks, that is, for individuals that cannot be assigned to any species in systems based on what have been termed “autapomorphic” species concepts by Nixon and Wheeler (1990). Hence Donoghue’s “metaspecies,” Graybeals’ “ferespecies,” and Olmstead’s “plesiospecies” encounter problems. The real issue is one of identifying criteria

Species Hierarchies

373

FIG. 2. The progression from paraphyly/polyphyly to reciprocal monophyly of nonrecombining maternally inherited elements (i.e., mitochondria) in three descendent generations of Hennig’s (1966) Fig. 6. The middle frame represents relationships among individuals in three descendent generations, as in the right side of Fig. 1. At left are represented the ancestor–descendent relationships of individuals in Hennigian species A, all of which bear haplotype II beginning with generation D1; to the right are those relationships among individuals in Hennigian species B. In descendant generation 1, species A is polyphyletic and species B is “paraphyletic” based on mitochondrial elements. Neither is diagnosable based on those elements. Character fixation and reciprocal monophyly occur simultaneously in the next generation, with the death of haplotype IV and the disappearance of haplotype III from descendant (now phylogenetic) species A.

for determining whether the underlying hierarchy necessary to justify phylogenetic interpretations of cladistic results exists. Heritable characters provide the only direct sources for such criteria. Woodger’s paradox, described earlier, becomes useful in highlighting the implications of using fixed characters to delineate species. The source of the paradox is an artifact of requiring not only that individuals be uniquely placed—in no more than one species—but that this placement is immutable through time. The premise of Woodger’s paradox is that species are biologically distinct entities in some unspecified sense (see above discussion of ontology), but if the matter is simply one of recognition, the paradox goes away, because a species determination for a given individual is temporally dependent, changing according to fixation events. Seen this way, classification of an individual organism most certainly can change with time as character fixation events occur. In contrast to the kind of speciation boundary required by Woodger, a temporal boundary drawn between two successive generations, it is an implication of the phylogenetic species concept

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

that “speciation” is an instantaneous event, corresponding to character fixation, coinciding with the death of the last individual with a plesiomorphic character state (Nixon and Wheeler, 1992) and, most importantly, consistent with Woodger’s premise that speciation occurs between two successive generations. This framework is consistent with Kluge’s (1990) consideration of species as historical individuals. As Woodger understood, the implication that speciation be instantaneous is a necessary outcome of hierarchical evolutionary systems. Whether or not some individuals within a particular phylogenetic species are more or less closely related to one another than to members of another phylogenetic species is irrelevant to the reconstruction of relationships among species. This is another way of restating Nixon and Wheeler’s (1990) point that the intent of delimiting phylogenetic species is to recognize minimal (elemental, fundamental) units for phylogenetic analysis and that phylogenetic relationships within those units are simply untenable. But the problem of misunderstanding the limits of

374

such terms as monophyly and paraphyly is not confined to the lack of accuracy with which hierarchical graphs depict nonhierarchical systems. Ultimately, such terms reflect character state distributions; synapomorphy and monophyly are intimately related because the determination of a synapomorphy relies ultimately on its contribution to a specific most parsimonious solution (Farris and Kluge, 1986; Carpenter, 1992). At the species level and above, monophyletic groups do indeed represent historical entities. As Farris (1991, p. 304) explained: Monophyly can be defined (though not recognized) without reference to character evidence only because monophyletic groups have real and independent historical existence. Paraphyletic and polyphyletic groups have no such existence; they are nothing but the characters by which they are delimited. Without characters, paraphyly and polyphyly mean nothing.

Within reticulating networks, it is readily seen that hierarchically portrayed monophyletic groups also have no such existence, precisely because of the nearly limitless array of possible hierarchic depictions (Maddison, 1995, 1997). Moreover, as Luckow (1995) explained, since hypotheses of relationship are based ultimately on characters, then tree-based descriptors should not logically be viewed as arbiters of character data (see also Rieppel, 1994). The problem for species delimitation thus becomes not just one of understanding where character fixation and reciprocal monophyly do not coincide, but whether this lack of coincidence means anything. Prior to character fixation, for example, in the descendant species in Hennig’s Fig. 6, cladistic analyses of even nonrecombining elements reveal polyphyly. It so happens in Hennig’s figure that the “achievement” of monophyly coincides with character fixation, but this need not be the case (Fig. 3). Again, using Hennig’s figure as an example, one can explore the coincidence of character fixation with intraspecific monophyly. Had ancestral haplotype 4 persisted for one more generation in descendant species B, then character fixation would not have been coincident with the progression to reciprocal monophyly. Descendant species A would still be diagnostic, but would species B? Species B would not be characterized by any fixed haplotype, but neither of its haplotypes would be present in species A. Species B would thus be diagnostic with respect to

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

species A, but not necessarily monophyletic with respect to any mitochondrial haplotype lineage.4 The discrepancy between the achievement of reciprocal monophyly and character fixation is asymmetrical, however, with respect to nonrecombining elements. By definition, an analysis that reveals monophyly with respect to a given haplotype is also diagnostic with respect to that haplotype. But consider the situation in which all four mitochondrial haplotypes in Fig. 4 are present in mutually exclusive pairs in each descendant species (cf. Davis, 1996, p. 508, Fig. 3). Technically, the differences are fixed, hence the phylogenetic species are diagnosable. Again, however, each is paraphyletic with respect to the other when the reconstruction is based on the maternal lineage. This example illustrates the utility of population aggregation analysis, which would cleave such groupings so that no subset polymorphism existed. Thus complications for the PSC involve the algorithmic mechanics of population aggregation analysis and its attendant phylogenetic reconstructions. Davis and Nixon’s (1992) description of population aggregation analysis emphasizes the unique power of fixed attributes (⫽ characters) to diagnose phylogenetic species; no attribute that occurs in a subset of individuals in one population can be used to diagnose another. Their emphasis on fixation, be it fixation of attributes themselves or fixation of differences (i.e., nonoverlapping polymorphisms; Davis, 1996), is relevant here. A difference between two putative phylogenetic species may be fixed without any single attribute being diagnostic, but rather with a combination of attributes being diagnostic (Fig. 4). Population aggregation analysis is fundamentally an exercise in minimizing polymorphism, which it does by aggregating individuals united by the most inclusive sets of characters. Baum (1992) raises what he considers the primary shortcoming of the diagnostic/character-based approach, the notion that characters may be diagnostic but primitive. This concern is echoed in later publications, particularly in Baum and Donoghue’s (1995) characterization of character-based approaches as ahistorical. However, this point denies the character-based

4 Perhaps this observation speaks more directly to the inconsistency of Hennig’s own species concept with phylogenetic systematics.

Species Hierarchies

375

FIG. 3. Character fixation versus Hennig’s view of species, again based on Hennig’s Fig. 6. Note that Hennig considered A and B species following (geographic) separation of populations, regardless of character state distributions. Roman numerals representing haplotypes present in ancestral generations A1 through A4 are shown on both sides of the diagram. The stippled box indicates the generation (D1) where separation occurs. Roman numerals on the left indicate haplotyes in Hennigian species A; those on the right indicate haplotypes in Hennigian species B. Single asterisks indicate polymorphism; double asterisks indicate character fixation and hence phylogenetic species. The first descendant generations in both species A and B are not diagnosably distinct. At the point at which reciprocal monophyly is reached by each descendant species, only two ancestral mitochondrial haplotypes remain, one in each population, hence the mutual character fixation is actually coincident with the progression from paraphyly/polyphyly to monophyly (Fig. 2). Because the character fixation occurs in concurrent generations of each descendant species, character fixation is further coincident with reciprocal monophyly. Had ancestral haplotype 4 persisted for one more generation in descendent species B, then character fixation would not have been coincident with the progression to reciprocal monophyly, although descendant species A would still be diagnosable. B would not be characterized by any fixed haplotype, but neither of its haplotypes would be present in species A.

formulation of phylogenetic inference. Given an imaginary phylogeny, it is easily illustrated that two apparently identical individuals do not bear a most recent common ancestor. Baum and Donoghue provide such illustrations as examples. However, as with the figures in Baum and Shaw (1995), discussed below, these illustrations collapse to two-taxon statements when the identical individuals are clustered according to fixed character states. The presumption of Baum and Donoghue’s and Baum and Shaw’s figures is that enough other character evidence exists to overwhelm their most obvious similarities and unite nonidentical individuals as sharing relatively more recent common ancestry. Unless those other data themselves consist of fixed (diagnostic) states, however, only one phylogenetic species—one terminal—actually exists, indicating that there is no hierarchy to begin with and no unambiguous relative recency of common ancestry to be recovered.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Brower (1999) raises related issues, highlighting certain properties of population aggregation analysis when applied to character strings (DNA sequences in his illustration) versus singleton characters. Brower proposed a new method, cladistic haplotype analysis (CHA), designed to redress the shortcomings of PAA, specifically to identify hiearchical systems below the level of those identifiable by fixed character states by maximizing the information gleaned from polymorphism. It is similar to PAA in its assumptions concerning population delineation and its tabulation of attribute profiles, but involves a network construction step, which is used to test whether a group of individuals (population) is connected to other such groups by more than one branch. Multiple connections indicate nonindependence in Brower’s interpretation, and aggregates so joined are not then treated as phylogenetic species. Brower was careful to proscribe the interpretation of such networks as nonphylogenetic, and the method is

376

intended to identify hierarchy beneath the level pinpointed by diagnostic characters. Brower’s critique identifies several unexplored properties of PAA, and as one of the only in-depth treatments of the method, his paper warrants some discussion. Principal among these is the way PAA treats polymorphisms and the implications of that treatment. In order to illustrate the applicability of cladistic methods below the boundary identified exclusively by diagnostic criteria, Brower compared his CHA with applications of PAA using, alternatively, individuated characters as diagnostics [his “PAA1,” equivalent to Davis and Nixon’s (1992) usage] as well as character strings, i.e., unique combinations of characters (‘‘PAA2’’). The observation that differences can be fixed as alternative character states or as alternative polymorphisms led Brower to identify a behavioral feature of PAA vis a` vis its treatment of combinations of characters. Citing an example from Davis (1996), Brower describes a situation in which two populations are diagnosably distinct by virtue of balanced polymorphisms involving two sets of alternative character states. The purpose of Davis’ example was to illustrate that PAA could be used to diagnose entities based on fixed combinations of character states, neither of which need be fixed so long as it is not present in the other population. The idea is that, no matter what the relation among these haplotypes—and in Davis’ example those relationships are coincident with the population boundaries—they may still be used to delineate phylogenetic species. As Brower observes, there are actually two issues here, namely the suitability of aggregations as terminal in phylogenetic analysis and the equation of natural populations as such terminals. It is important to keep this distinction in mind when scrutinizing Brower’s treatment of polymorphism. Brower’s primary criticism of PAA involves the identification of within-population variation that contradicts characters fixed between populations, suggesting that the initial delimitations of those populations are in fact spurious. In points analogous to those of Baum’s (1992) concerning diagnostic characters’ being primitive, Brower refers to polymorphisms that contradict the fixationbased diagnoses as homoplastic. He points out that such polymorphisms—those contradicting diagnoses of already-identified populations—would be discarded by PAA, stating (p. 200) that “the manner in

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

FIG. 4. The distinction between fixed character states within populations and fixed differences across populations. (cf. Davis and Nixon, 1992). Both A and B involve three possible character states; gray, white, and black in the case of A, and T, A, and G in the case of B. If we accept the subset polymorphism in the aggregates on the left as diagnostic, then phylogenetic analysis (sensu Davis and Nixon, 1992) is justified. Further iterations of population aggregation analysis would split these aggregates further, just as the presence of either states of the polymorphism outside the aggregate would collapse it as a potential terminal. Hypervariability may thus present an obstacle to PAA because of the algorithmic inability of software to manage subset polymorphisms and the undesirability of analyzing polythetic terminals phylogenetically.

which PAA treats homoplastic characters in DNA sequences engenders an extreme differential characterweighting procedure that can contradict a parsimonious interpretation of empirical evidence.” To illustrate this point, Brower provides an example (his Fig. 3) wherein the sampled members of two populations do not form diagnosably distinct clusters, hence diagnosis of either population under PAA1 is impossible. PAA2 recovers the groupings, but Brower argues that this contradicts the weight of the evidence, which unites subsets of different populations, hence PAA supports groupings not corroborated by CHA. Brower proposes that PAA thus has the potential to be circular because it can only diagnose populations that have been assumed under background knowledge, whereas CHA can refute such assumptions. Terminals aggregated by CHA need not be possessed of any fixed character state. Brower’s method is a promising attempt to address the issue of the reticulate–hierarchical boundary using a paradigm that is largely consistent with that of phylogenetic systematics. Coupled with parallel methods

377

Species Hierarchies

that employ the tools of population genetics (e.g. Templeton et al., 1987; Templeton, 1998), the potential now exists to approach the species boundary from both sides. Remaining debates are likely to center on the evolutionary interpretation of terminals united in networks, regardless of their diagnosability. For example, there remains a problem with applying hierarchic terms—such as homoplastic—to characters, while admitting that hierarchies themselves do not reflect phylogeny. Broadly, we see a problem with using an operational method to dictate its own boundaries. As Doyle (1995, p. 578) phrased it in reference to Baum and Shaw’s technique, “Using a method that assumes hierarchy to detect lack of hierarchy is probably ill-advised.” Although, Brower was careful to ward off phylogenetic interpretations of unrooted networks, and provided one of the first strictly graphical means of solving this problem by superimposing population boundaries on those networks, the remaining question harkens to one of the conditions identified by Davis and Nixon necessary to interpret the results of cladistic analyses as phylogenetic: descent with modification. If the results of CHA are to be interpreted as anything more than refutation of population distinctness, then the method can be said to conflate homoplasy with polymorphism. The treatment of polymorphism in phylogenetic inference is hardly unique to species-level questions (e.g., Nixon and Davis, 1991). Though it is obvious that overlapping polymorphisms in different organismal populations suggests the relative recency of common ancestry, it has yet to be demonstrated whether polymorphisms concatenated among such populations can be used to compute phylogenetic relationship without obscuring information from fixed character states. Diagnoses of separate phylogenetic species occur only when character state profiles are mutually exclusive. Fixation of a character state or combination of character states in one population without alternative fixation in another does NOT result in the two being diagnosed as separate phylogenetic species. Thus the argument that fixed states can be primitive is of concern only when such uninformative characters outnumber the informative characters. No doubt this scenario is related to Baum and Donoghue’s (1995) concern over parsimony as an optimization method, but their position goes far beyond that. It is readily understood that

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

one of the implications of using nonparsimony methods (e.g., maximum likelihood) is the incorporation of unobserved (and unobservable) character change as evidence in phylogenetic reconstruction. This particular argument has not dissuaded proponents of that method.5 But the incorporation of this kind of logic in species delineation has more troubling consequences: If the only characters and suites of characters by which species may be recognized are discarded in favor of presupposed (and non-character-based) notions of relatedness, we sacrifice the perspective of understanding what the terminals in our cladograms actually refer to. This goes directly to the point raised by Mallet (1995), namely, that if we must understand the relationships among entities before we can delineate those entities, then we have put the cart before the horse.

PHYLOGENETIC SPECIES AND ANCESTORS Simpson’s (1961) evolutionary species concept was resurrected and modified by Wiley (1978), who attempted to reconcile cladogenetic considerations with anagenetic considerations. In doing so he emphasized the incorporation of temporal considerations in the form of historical fates. He proposed the following definition of species: “A species is a single lineage of ancestral descendant populations of organisms which maintains its identity from other such lineages and which has its own evolutionary tendencies and historical fate.” Others (e.g., Mayden and Wood, 1995, p. 104) have followed Wiley in criticizing the PSC on the grounds that it is “not capable of recognizing ancestral species.” The issue of time extension in species concepts goes directly to the fallacy of requiring that species membership be fixed (Woodger’s paradox, already discussed), but also to our interpretation of cladogram nodes as ancestral species. Hennig’s was an “internodal” species concept requiring that nodes represent ancestral species and that speciation events engender extinction of those ancestors and the vicariant appearance of two descendant species (Hennig, 1966; Nixon and Wheeler, 5 To the contrary, many view the claim to “account for” unobserved information as an advantage of likelihood (Sullivan, 1995).

378

1990). Hennig’s species concept, later echoed by Brundin (1972) and Ridley (1989), thus required no change in descendant species, merely vicariance, for them to be recognized as such (Nixon and Wheeler, 1990; Appendix B)6. In contrast, species concepts resting on monophyly, including those of Rosen (1979), de Queiroz and Donoghue (1988, 1990), and Hill and Crane (1982), did require anagenetic change in both descendant species. For this and other reasons, discussed earlier, Nixon and Wheeler (1990) referred to these concepts as “autapomorphic” rather than monophyletic species concepts. Nixon and Wheeler (1992, p. 119) later added that “only arbitrary or process-based definitions of species recognize anagenetic change (involving fixation) within species” (cf. Appendix B). Baum and Shaw (1994) and Baum and Donoghue (1995) suggested that species must necessarily be “basal”. The example they use to illustrate their approach of delimiting species as basal taxa consists of two unresolved polytomies separated by a single node. However, when those polytomies are collapsed to form “genealogical species” as per the suggestion of the authors, the result is a two-taxon statement. It is a property of cladograms with only two terminals that neither can be basal with respect to the other. Baum and Shaw’s example is a poor illustration of their point, and the argument that species are necessarily basal taxa would appear to rest on an error in graphic interpretation. The retention of the term “stem species” in the paleontological literature testifies to the desire of many to incorporate temporal components in cladogram interpretation. But such is not in fact necessary. A cladogram is a representation of the relative recency of common ancestry: no more, no less. As such, species are represented by terminals themselves, not the nodes subtending them. While the nodes do represent ancestors, it is perhaps wise to interpret nodes as individual organisms rather than ancestral species. This distinction may also serve to highlight the difference between Davis and Nixon’s (1992) population aggregation analysis and Brower’s (1999) cladistic haplotype analysis. The former requires common ancestry from a single individual; the latter does not (Appendix B). The asymmetry between the entities represented by 6 As Nixon and Wheeler (1990) point out, despite Mayr’s (1974) criticisms, Hennig’s concept was closely tied to Mayr’s, based in part on reproductive potential and delimitation by breeding barriers.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

terminals and those represented by nodes is related to the asymmetry between species and higher taxa: The interpretation of nodes as ancestral species rather than individual organisms need not require anagenetic change in both descendant species when monophyly is properly applied only above the species level. However, that interpretation does require such anagenetic change under the autapomorphic species concept precisely because the notion of monophyly is misapplied. Stem species, much like paraphyletic taxa, are nothing more than imaginary constructs.

IMPLICATIONS OF HIERARCHIES: EXTINCTION, FIXATION, AND ANCESTORS

The identification of species should be fundamentally decoupled from the elucidation of relationships. If it is not, then the progress of phylogenetic systematics will be hamstrung. The fact, observed by Maddison, Avise, and others, that putative hierarchies exist everywhere indicates neither that they be viewed as continuous functions nor that they can be consensed in order to more precisely identify relationship. While the continuity of life is a recognizable fact, it is the discreteness of character systems that makes phylogenetic inference and representation possible. Though biological networks extend backward through time, the objective circumscription of entities making up those networks takes the form of characters. The perceptions that monophyly is necessarily applicable across network boundaries and that cladograms must incorporate an absolute (as opposed to a relative) temporal component are obviated by character-based analytical criteria. In our view, the “restricted” use of monophyly is an analytical and theoretical boon, not a philosophical encumbrance. The implication that speciation is an instantaneous event follows directly from the notion that species delimitation depends on distributions of characters (Nixon and Wheeler, 1992; Vogler, 1994). For two populations to be legitimately recognized as phylogenetic species, at least two individuals—each the last semaphoront of the “alternative” character state in its own

Species Hierarchies

population—must die. Only then is phylogenetic speciation said to have occurred. Many biologists are, perhaps justifiably, uncomfortable with this paradigm, dubbed “speciation by remote control” by Templeton (1999). But the paradigm relating the phylogenetic species concept to character fixation does solve a number of important problems without detracting from our ability to explore either the dynamics of population genetics or the evolution of reproductive isolation. The commonly perceived drawback of population aggregation analysis—the degree to which sampling determines the strength of any claims of character fixation—is ultimately no different from any other endeavors of systematics. As Davis and Nixon (1992) and DeSalle and Vogler (1993) described, undersampling of individuals or populations can lead to spurious determinations of character fixation. However, the endeavor of systematics is not beholden to statistical dicta of how many individuals are necessary to “justify” describing a new species. Available “samples” being what they are, claims of character fixation are hypotheses to be corroborated or refuted by the accumulation of additional data. Stability—nomenclatural or otherwise—is not a prerequisite of phylogenetic inference. Futhermore, the issue of sampling is no different for tree-based species descriptors than for character-based descriptors, since any representation of individuals sampled from within a population is sure to be paraphyletic with respect to unsampled individuals from the same population. Whether or not one adopts the PSC as a general species concept, it is an inescapably minimal criterion for the phylogenetic interpretation of hierarchical analyses. The application of hierarchy-generating methods

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

379

to nonhierarchical systems requires not that hierarchical terms be redefined. Such applications entail nothing less than discarding the fundamental goal of identifying relative recency of common ancestry. Any confusion—either in the systematics or in the conservation and phylogeography literature—over the relevance of tree-based descriptors to intraspecific systems can be addressed in part by insisting that such usage be confined to nonrecombining elements inherited from single-parent lineage (such as mitochondrial DNA) or elements inherited clonally in asexual organisms. Such systems are necessarily hierarchical and since they can be depicted accurately in a nested fashion, it is legitimate to represent them as such. A more fundamental problem with such applications is that the inferred phylogeny of mitochondrial haplotypes—even if accurate—may not be representative of the organisms bearing the analyzed elements. That notwithstanding, Avise’s repeated observation that the relationships among such elements tend to pass through a progression from polyphyletic to paraphyletic to monophyletic as mitochondrial lineages go extinct does carry potential relevance to phylogenetic species delimitation. Methods to investigate underlying hierarchy, using alternate systematic (e.g., Brower, 1999) and population genetic (e.g., Templeton et al., 1987; Templeton, 1998) approaches, certainly show promise. As we have described, the achievement of monophyly need not be coincident with the fixation of character state differences. But although tree-based descriptors may be useful as retrospective or exploratory measures to examine phylogenetic species delimited under PAA, they should not preside over character-based descriptors. Intraspecific monophyly fails as a theoretical paradigm.

380

Goldstein and DeSalle

APPENDIX A Ontological Features of Various Species Concepts, Including Versions of Phylogenetic Species Ontological features

Species concept

Author/proponent

Criterion

Emphasis

Criteria general vs contextdependent

BSC

Mayr, Dobzhansky, Avise

Potential interbreeding

EvSC

Simpson, Wiley

ISC EcSC

Hennig, Brundin, Ridley Van Valen

Lineage cohesion Lineage coheMaintenance General sion Adaptive peaks Maintenance General

RSC

Paterson

CSC

Templeton

PSC

Cracraft, Nixon, Davis, Wheeler, Luckow Brower

PSC ASC

GSC

de Queiroz, Donoghue, Olmstead, Hill and Crane Baum, Donoghue, Shaw

Maintenance Contextdependent Maintenance General

Isolating mech- Maintenance Contextanisms dependent Reproductive Maintenance Contextcohesion dependent Diagnostic Origin General characters Haplotype net- Origin General works Monophyly Origin General

Monophyly

Origin

General

Mechanistic vs theory-neutral Mechanistic

Pluralistic vs monistic

Individuals vs classes

Discrete vs continuous

Monistic

Classes

Continuous

Theory-neutral Monistic

Classes

Continuous

Theory-neutral Monistic

Individuals

Discrete

Mechanistic

Monistic

Continuous

Mechanistic

Monistic

“Individualistic classes” —

Discrete

Mechanistic

Monistic

Individuals

Discrete

Theory-neutral Monistic

Individuals

Discrete

Theory-neutral Monistic

Individuals

Discrete

Mechanistic

Pluralistic Individuals

Continuous

Mechanistic

Pluralistic Individuals

Continuous

Note. BSC, biological species concept; EvSC, evolutionory species concept; ISC, internodal species concept; EcSC, ecological species concept; RSC, recognition species concept; CSC, cohesion species concept; PSC, phylogenetic species concept; ASC, actapomorphic species concept; GSC, geneological species concept.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

381

Species Hierarchies

APPENDIX B Cladistic Features and Implications of Various Species Concepts, Including Versions of Phylogenetic Species Species concept

Cladistic Corollaries

Author/proponent

Temporal component

BSC EvSC

Mayr, Dobzhansky, Avise Simpson, Wiley

Unidimensional Time-extended

Current Prospective

ISC

Hennig, Brundin, Ridley

Time-extended

Retrospective

EsSC RSC CSC PSC

Van Valen Paterson Templeton Cracraft, Nixon, Davis, Wheeler, Luckow Brower de Queiroz, Donoghue, Olmstead, Hill, and Crane Baum, Donoghue, Shaw

Unidimensional Unidimensional Unidimensional Unidimensional

Current Current Current Retrospective

Unidimensional Unidimensional

Retrospective Retrospective

Time-extended

Retrospective

PSC ASC

GSC

Perspective

ACKNOWLEDGMENTS

The authors thank Jim Carpenter, Olivier Rieppel, John Wenzel, and Yael Wyner for comments on earlier drafts of this paper. This acknowledgment does not imply complete congruence of their views with ours.

REFERENCES

Type of change Anagenetic, Anagenetic, cladogenetic Anagenetic, cladogenetic Anagenetic, Anagenetic, Anagenetic, Cladogenetic Cladogenetic Anagenetic, cladogenetic Anagenetic, cladogenetic

Cladogram graphic

Change in both descendant species

None Internodal

Required Required

Internodal

Not required

None None None Terminal

Required Not required Required Not required

Network-based Tree-based (“monophyly’) Tree-based (“monophyly”)

Not required Required

Required

Avise, J. C. and Ball, R. M., Jr. (1990). Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surv. Evol. Biol. 7, 45–67. Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A., and Saunders, N. C. (1987). Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18, 489–522. Avise, J.C., and Wollenberg, K. (1997). Phylogenetics and the origin of species. Proc. Natl. Acad. Sci. USA 94: 7748–7755. Ax, P. (1987). “The Phylogenetic System: The Systematization of Living Organisms on the Basis of Their Phylogenesis.” Wiley, New York. Baum, D. (1992). Phylogenetic species concepts. Trends Ecol. Evol. 7, 1–2.

Allen, G. E. (1980). The evolutionary synthesis: Morgan and natural selection revisited. In “The Evolutionary Synthesis: Perspectives on the Unification of Biology” (E. Mayr and W.B. Provine, Eds.). pp. 365–382. Harvard Univ. Press, Cambridge.

Baum, D. A. (1999). Individuality and the existence of species through time. Syst. Biol. 47(4), 641–653.

Avise, J.C. (1989). Gene trees and organismal histories: A phylogenetic approach to population biology. Evolution 43(6), 1192–1208. Avise, J. C. (1994). “Molecular Markers, Natural History, and Evolution.” Chapman & Hall, New York.

Baum, D. A., and Shaw, K. L. (1995). Genealogical perspectives on the species problem. In “Experimental and Molecular Approaches to Plant Biosystematics” (P.C. Hoch and G.D. Stephenson, Eds.), pp. 289–303. Missouri Botanical Garden, St. Louis.

Avise, J.C. (1999). “Phylogeography. The History and Formation of Species,” Harvard Univ. Press, Cambridge.

Bremer, K., and Wanntorp, H.-E. (1979). Hierarchy and reticulation in systematics. Syst. Zool. 28(4): 624–627.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Baum, D. A., and Donoghue, M. J. (1995). Choosing among alternative “phylogenetic” species concepts. Syst. Bot. 20, 560–573.

382 Brower, A. V. Z. (1999). Delimitation of phylogenetic species with DNA sequences: A critique of Davis and Nixon’s population aggregation analysis. Syst. Biol. 48, 199–213. Brower, A. V. Z., DeSalle, R., and Vogler, A. (1996). Gene trees, species trees, and systematics: A cladistic perspective. Annu. Rev. Ecol. Syst. 1996. Brundin, L. (1972). Evolution, causal biology, and classification. Zool. Scr. 1, 107–120. Carpenter, J. M. (1992). Random cladistics. Cladistics 8, 147–153. Claridge, M. F., Dawah, H. A., and Wilson, M. R. (Eds.) (1997). “Species: The Units of Biodiversity.” Chapman and Hall, New York. Clausen, J., Keck, D. D., and Hiesey, W. M. (1940). Experimental Studies on the Nature of Species. I. Effect of Varied Environments on Western North American Plants. Carnegie Institution of Washington Publication No. 520. Washington, DC. Clausen, J., Keck, D. D., and Hiesey, W. M. (1945). Experimental Studies on the Nature of Species. II. Plant Evolution through Amphiploidy and Autoploidy, with Examples from the Madiinae. Carnegie Institution of Washington Publication No. 564. Washington, DC. Clausen, J., Keck, D. D., and Hiesey, W. M. (1948). Experimental Studies on the Nature of Species. III. Environmental Responses of Climatic Races of Achillea. Carnegie Institution of Washington Publication No. 581. Washington, DC. Clausen, J. and Hiesey, W. (1958). Experimental Studies on the Nature of Species. IV. Genetic Structure of Ecological Races. Carnegie Institution of Washington Publication No. 615. Washington, DC. Cracraft, J. (1983). Species concepts and speciation analysis. Current Ornithology, 1, 159–187. Cracraft, J. (1987). Species concepts and the ontology of evolution. Biol. Philos. 2, 329–346. Cracraft, J. (1989). Speciation and its ontology: The empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In “Speciation and Its consequences” (D. Otte and J.A. Endler, Eds.), pp. 28–57. Sinauer Associates, Sunderland, MA. Cracraft, J. (1997). Species concepts in systematics and conservation biology—An ornithological viewpoint. In “Species: The Units of Biodiversity” (M. F. Claridge, H. A. Dawah, and M. R. Wilson, Eds.), pp. 325–339. Chapman and Hall, New York. Crandall, K. A., and Fitpatrick, J. E. (1996). Crayfish molecular systematics: Using a combination of procedures to estimate phylogeny. Syst. Biol. 45, 1–26. Davis, J. I. (1995). Species concepts and phylogenetic analysis— Introduction. Syst. Bot. 20(4), 555–587. Davis, J. I. (1996). Phylogenetics, molecular variation, and species concepts. BioScience 46, 502–511. Davis, J. I., and Nixon, K. C. (1992). Populations, genetic variation, and the delimitation of phylogenetic species. Syst. Biol. 41, 421–435. de Queiroz, K. (1998). The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. in “Endless Forms: Species and Speciation” (D. J. Howard and S. H. Berlocher, Eds.), pp. 57 78. Oxford University Press, New York.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

de Queiroz, K., and Donoghue, M. J. (1988). Phylogenetic systematics and the species problem. Cladistics 4, 37–338. de Queiroz, K., and Donoghue, M. J. (1990). Phylogenetic systematics or Nelson’s version of cladistics? Cladistics 6, 61–75. DeSalle, R., and Vogler, A. P. (1993). Phylogenetic analysis on the edge: The application of cladistic techniques at the population level. In “Non-neutral Evolution” (B. Golding, Ed.), pp. 154–174. Chapman and Hall, New York. Dobzhansky, T. (1937). “Genetics and the Origin of Species.” Columbia University Press, New York. Donoghue, M. J. (1985). A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist 88, 172–181. Doyle, J. J. (1992). Gene trees and species trees: Molecular systematics as one-character taxonomy. Syst. Bot. 17, 144–163. Doyle, J. J. (1995). The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Syst. Bot. 20(4), 574–588. Eldredge, N., and Cracraft, J. (Eds.) (1980). “Phylogenetic Patterns and the Evolutionary Process: Method and Theory in Comparative Biology.” Columbia Univ. Press, New York. Farris, J. S. (1974). Formal definitions of paraphyly and polyphyly. Syst. Zool. 23, 548–554. Farris, J. S. (1985). The pattern of cladistics. Cladistics 1, 190–201. Farris, J.S. (1991). Hennig defined paraphyly. Cladistics 7, 297–304. Frost, D. R., and Hillis, D. M. (1990). Species in concept and practice: Herpetological applications. Herpetologica 46(1), 87–104. Frost, D. R. and Kluge, A. G. (1994). A consideration of epistemology in systematic biology, with special reference to species. Cladistics 10(3), 259–294. Ghiselin, M.T. (1974). A radical solution to the species problem. Syst. Zool. 23, 536–554. Ghiselin, M. T. (1987). Species concepts, individuality, and objectivity. Biol. Philos. 2, 127–143. Ghiselin, M.T. (1989). Individuality, history and the laws of nature in biology. In “What the Philosophy of Biology Is” (M. Ruse, Ed.), pp. 53–67. Kluwer Academic, Boston. Goldstein, P. Z., DeSalle, R., Amato, G., and Vogler, A. P. (2000). Conservation genetics at the species boundary. Conserv. Biol. 14(1), 120–131. Graybeal, A. (1995). Naming species. Syst. Biol. 44, 237–250. Hall, B.K. (1992). “Evolutionary Developmental Biology.” Chapman & Hall, New York. Harrison, R. G. (1998). Linking evolutionary pattern and process: the relevance of species concepts for the study of speciation. in “Endless Forms: Species and Speciation” (D. J. Howard and S. H. Berlocher, Eds.), pp. 19–31. Oxford University Press, New York. Hennig, W. (1966). “Phylogenetic Systematics.” Univ. of Illinois Press, Urbana. Hill, C. R., and Crane, P. R. (1982). Evolutionary cladistics and the origin of angiosperms. In “Problems of Phylogenetic Reconstruction” (J. A. Joysey, and A. E. Friday, Eds.), Chap. 10. pp. 269–361. Academic Press, London.

Species Hierarchies

383

Holsinger, K. E. (1984). The nature of biological species. Philos. Sci. 51, 293–307.

Moritz, C. (1994b). Defining ‘evolutionarily significant units’ for conservation. Trends Ecol. Evol. 9(10), 373–375.

Hull, D. L. (1976). Are species really individuals? Syst. Zool. 25, 174– 191.

Moritz, C. (1995). Uses of molecular phylogenies for conservation. Philos. Trans. Roy. Soc. London B 349, 113–118.

Hull, D. L. (1978). A matter of individuality. Philos. Sci. 45, 335–360.

Neigel, J. E., and Avise, J. C. (1986). Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. In “Evolutionary Processes and Theory” (E. Nevo and S. Karlin, Eds.), pp. 515–534. Academic Press, New York.

Hull, D. L. (1980). Individuality and selection. Annu. Rev. Ecol. Syst. 11, 311–332. Hull, D. L. (1997). The ideal species concept—and why we can’t get it. In ‘‘Species: The Units of Biodiversity” (M. F. Claridge, H. A. Dawah, and M. R. Wilson, Eds.), pp. 357–380.Chapman & Hall, New York. Kluge, A. G. (1990). Species as historical individuals. Biol. Philos. 5, 417–431. Løvtrup, S. (1987). On species and other taxa. Cladistics 3(2), 157–177. Luckow, M. (1995). Species concepts, assumptions, methods, and applications. Syst. Bot. 20(4), 589–605. Maddison, W. P. (1995). Phylogenetic histories within and among species. In “Experimental and Molecular Approaches to Plant Biosystematics” (P. C. Hoch and A. G. Stephenson, Eds.), Monographs in Systematics, Vol. 53, pp. 273–287. Missouri Botanical Garden, St. Louis. Maddison, W. P. (1997). Gene trees in species trees. Syst. Biol. 46(3), 523–536. Mallet, J. (1995). A species definition for the modern synthesis. Trends Ecol. Evol. 10(7), 294–299. Mayden, R. L. (1997). A hierarchy of species concepts: The denouement in the saga of the species problem. In “Species: The Units of Biodiversity” (M. F. Claridge, H. A. Dawah, and M. R. Wilson. Eds.), pp. 381–424. Chapman and Hall, New York. Mayden, R. L., and Wood, R. M. (1995). Systematics, species concepts, and the evolutionarily significant unit in biodiversity and conservation biology. Am. Fish. Soc. Symp. 17, 58–113. Mayr, E. (1942). “Systematics and the Origin of Species.” Columbia Univ. Press, New York. Mayr, E. (Ed.) (1957). The Species Problem. Am. Assoc. Adv. Sci. Publication No. 50, Washington, DC. Mayr, E. (1963). “Animal Species and Evolution.” Harvard Univ. Press, Cambridge.

Nelson, G. (1985). Class and individual: A reply to M. Ghiselin. Cladistics 1, 386–389. Nelson, G. J., and Platnick, N. I. (1981). “Systematics and Biogeography: Cladistics and Vicariance.” Columbia Univ. Press, New York. Nixon, K. C., and Davis, J. J. (1991). Polymorphic taxa, missing values, and cladistic analysis. Cladistics 7, 233–241. Nixon, K. C., and Wheeler, Q. D. (1990). An amplification of the phylogenetic species concept. Cladistics 6, 211–223. Nixon, K. C., and Wheeler, Q. D. (1992). Extinction and the origin of species In “Extinction and Phylogeny” (M. Novacek and Q. Wheeler, Eds.), pp. 119–143. Columbia Univ. Press, New York. O’Hara, R. J. (1993). Systematic generalization, historical fate, and the species problem. Syst. Biol. 42(3), 231–246. Olmstead, R. G. (1995). Species concepts and plesiomorphic species. Syst. Bot. 20(4), 623–630. Paterson, H. E. H. (1985). The recognition concept of species. In “Species and Speciation” (E. S. Vrba, Ed.), Transvaal Museum Monograph 4. Transvaal Museum, Pretoria. Platnick, N. I. (1977). Monotypy and the origin of higher taxa: A reply to E.O. Wiley. Syst. Zool. 26, 355–357. Ridley, M. (1989). The cladistic solution to the species problem. Biol. Philos. 4, 1–16. Rieppel, O. (1986). Species are individuals: A review and critique of the argument. Evol. Biol. 20, 283–317. Rieppel, O. (1992). Homology and logical fallacy. J. Evol. Biol. 5, 701–715. Rieppel, O. (1994). Species and history. In “Models in Phylogeny Reconsruction” (R. W. Scotland, D. J. Siebert, and D. M. Williams, Eds.), Systematics Association Special Vol. 52, pp. 31–50. Clarendon, Oxford.

Mayr, E. (1969). “Principles of Systematic Zoology.” McGraw–Hill, New York.

Rosen, D. E. (1979). Fishes from the uplands and intermontane basins of Guatemala: Revisionary studies and comparative geography. Bull. Am. Mus. Nat. Hist. 162, 267–376.

Mayr, E. (1970). “Populations, Species, and Evolution. “Harvard Univ. Press, Cambridge.

Rosen, D. E. (1982). Do current theories of evolution satisfy the basic requirements of explanation? Syst. Biol. 31(1), 76–85.

Mayr, E. (1974). Cladistic analysis or cladistic classification? Z. Zool. Syst. Evol. 12, 94–128.

Simpson, G. G. (1961). “Principles of Animal Taxonomy.” Columbia Univ. Press, New York.

Medawar, P. B. and Medawar, J. S. (1983). “Aristotle to Zoos.” Harvard Univ. Press, Cambridge.

Templeton, A. R. (1989). The meaning of species and speciation: A genetic perspective. In “Speciation and Its Consequences” (D. Otte and J. A. Endler, Eds.), pp. 3–27. Sinauer Associates, Sunderland, MA.

Meffe, G. K. and Carroll, R. (Eds). (1997). “Principles of Conservation Biology.” Sinauer Associates, Sunderland, MA. Mishler, B. D., and Donoghue, M. J. (1982). Species concepts: A case for pluralism. Syst. Zool. 31(4), 491–503. Moritz, C. (1994a). Applications of mitochondrial DNA analysis in conservation: A critical review. Mol. Ecol. 3, 401–411.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Templeton, A.R. (1998). Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol. Ecol. 7, 381–397. Templeton, A. R., Boerwinkle, E., and Sing, C. F. (1987). A cladistic

384 analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117, 343–351. Van Valen, L. (1976a). Ecological species, multispecies, and oaks. Taxon 25(2), 233–239. Van Valen, L. (1976b). Individualistic classes. Philos. Sci. 43, 539–541. Vogler, A.P. (1994). Extinction and the formation of phylogenetic lineages: Diagnosing units of conservation management in the tiger beetle Cicindela dorsalis. In “Molecular Ecology and Evolution: Approaches and Applications” (B. Shierwater, B. Streit, G.P.

Copyright 䉷 2000 by The Willi Hennig Society All rights of reproduction in any form reserved

Goldstein and DeSalle

Wagner, and R. DeSalle, Eds.), pp. 261–273. Birkhauser Verlag, Switzerland. Vrana, P., and Wheeler, W. (1992). Individual organisms as terminal entities: Laying the species problem to rest. Cladistics 8, 67–72. Wiley, E. O. (1978). The evolutionary species concept reconsidered. Syst. Zool. 27, 17–26. Wiley, E. O. (1989). Kinds, individuals, and theories. In “What the Philosophy of Biology Is” (M. Ruse, Ed.), pp. 289–300. Kluwer Academic, Boston. Willmann, R. (1983). Biospecies und phylogenetische Systematik. Z. Zool. Syst. Evolut. 21, 241–249.