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Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

6-1999

Species: Turning a Conundrum Into a Research Program

Daniel R. Brooks University of Toronto, [email protected]

Deborah A. McLennan University of Toronto

E. C. Bernard University of Tennessee

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Brooks, Daniel R.; McLennan, Deborah A.; and Bernard, E. C., "Species: Turning a Conundrum Into a Research Program" (1999). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 309. https://digitalcommons.unl.edu/parasitologyfacpubs/309

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Journal of Nematology 31(2):117–133. 1999. © The Society of Nematologists 1999. Species: Turning a Conundrum into a Research Program1

Daniel R. Brooks and Deborah A. McLennan2

Abstract: The most appropriate ontological basis for understanding the role of species in evolutionary biology is the Evolutionary Species Concept. The ESC is not an operational concept, but one version of the Phylogenetic Species Concept is. Linking the ontology of species with the epistemological basis of actual biological studies requires that we specify both a discovery mode for identifying collections of organisms that we believe are evolutionary species, and a series of evaluation criteria for assessing those entities we have discovered. Simply naming a collection of specimens, no matter how strong one’s evolutionary beliefs, is not sufficient for declaring that evolutionary species have been discovered. All operational historical species concepts represent discovery modes with minimal evaluation criteria; all operational non-dimensional species concepts represent evaluation criteria that do not specify discovery modes. Thus, both categories of knowledge are necessary and neither is sufficient for assigning species status. This leads naturally to a hierarchical research program in historical ecology, beginning with phylogenetic analysis of a group of entities postulated to be evolutionary species, which provides a productive arena for our arguments about species concepts. Key words: Evolutionary Species Concept, historical ecology, Phylogenetic Species Concept, phylog- eny, speciation.

“Why is not all nature in confusion, in- isms grouped naturally into discrete species, stead of the species being, as we see them, species into genera, genera into families, well defined?” (Darwin, 1872:161). and so on until all living things were in- cluded in a single classification of life. Pre- AShort History of the Darwinian taxonomists, like all natural phi- “Species Problem” losophers of the day, argued that the only “real” entities were those that had immu- It is not uncommon for major scientific table spatio-temporal existence. Because of concepts to have ambiguous definitions. In their unchangeable nature, such bits of re- Biology, one such term is “species.” This ality could be grouped into “classes” de- dilemma pre-dates Darwin (Stevens, 1992). fined by the fixed properties of their com- Initially, the “species” was simply a category ponents. Classic examples of such “real” in classifications, the least inclusive group of entities, which at the time were called “spe- organisms to be recognized formally. That cies,” are “hydrogen” and “gold.” Like the biosphere was organized into an in- these other natural kinds, biological species ternested hierarchy of species and groups of existed and conformed to a single hierarchi- species was thought to be self-evident. It was cal classification simply because it pleased simply the nature of the world that organ- the Creator for it to be so. In the absence of any causal principles explaining the taxo- Received for publication 20 November 1998. nomic hierarchy linking species together, 1 Symposium paper presented at the 37th Annual Meeting of the Society of Nematologists, 20–24 July 1998, St. Louis, MO. pre-Darwinian taxonomists relied on aes- 2 Centre for Comparative Biology and Biodiversity, Depart- thetics, intuition, and personal judgement ment of Zoology, University of Toronto, Toronto, Ontario M5S 3G5, Canada. to make decisions. E-mail: [email protected], mclennan@zoo. Darwin (1859) complicated things by sug- utoronto.ca Development of the perspective presented herein has been gesting that while organisms could indeed helped substantially by an enormous amount of published lit- be grouped naturally into species, these bio- erature appearing during the past 25 years, in addition to dis- cussions with Kare Bremer, John Collier, Joel Cracraft, Michael logical “species” were not immutable. Dar- Donoghue, Cyril Finnegan, Darryl Frost, William Fink, Vicki win’s belief in both the reality and the evo- Funk, Robert Geesink, David Hull, Arnold Kluge, Diedel Kor- net, Brian Maurer, Richard Mayden, Jack Maze, Brent Mishler, lutionary nature of biological species was Stan Salthe, Geoffrey Scudder, Jonathan Smith, Hans-Erik based on several empirical observations. Wanntorp, Quentin Wheeler, E. O. Wiley, and Rino Zandee. The authors especially thank Virginia Ferris for the invitation to First, comparing fossil and living species sug- participate in the symposium on species concepts. This study gested that the species populating the was supported by operating grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada. planet today are not the same as those popu- This paper was edited by E. C. Bernard. lating the planet in the past. Second, the 117 118 Journal of Nematology, Volume 31, No. 2, June 1999 world today is not populated by a small num- Darwin’s comments: “Hence, in determin- ber of species widely distributed in many dif- ing whether a form should be ranked as a ferent habitats in many different parts of the species or a variety, the opinion of natural- world; different species live in different parts ists having sound judgement and wide expe- of the world. And third, all living and extinct rience seems the only guide to follow. We species fit into a single hierarchical classifi- must, however, in many cases, decide by a cation that looks like a genealogy. Using majority of naturalists, for well-marked and perhaps the original form of the “Wiley Cri- well-known varieties can be named which terion” (Brooks and McLennan, 1991), Dar- have not been ranked as species by at least win suggested that if it looked like a geneal- some competent judges” (Darwin, 1872). ogy, it was one. Such concerns still preoccupy the minds This conclusion led Darwin to his first of some taxonomists (Grant, 1985). In the theory—that all species on this planet were second half of the 20th century, evolutionary related to each other through a single com- taxonomy (Mayr, 1969) epitomized the pre- mon history of descent with modification: Darwinian view that taxonomy was partly sci- phylogeny. It is not mere happenstance that ence and partly art form, with a sizeable the only illustration Darwin ever placed in component of personal judgement and in- any edition of Origin of Species was a phylo- tuition involved in trying to justify taxo- genetic tree (Bowler, 1996). Darwin had cre- nomic decisions in terms of evolutionary ated a dual role for species in biology. In principles. Phenetics, or numerical tax- addition to being units of classification, spe- onomy (Sneath and Sokal, 1973; Levins, cies were now also units of evolutionary pro- 1979), by contrast, abandoned all efforts to cess; identifying and classifying species was provide a link between taxonomy and evo- not simply a matter of convenience, it was lution by advocating purely empirical classi- explanatory. From the statements about spe- fication procedures having no particular cies in Origin of Species, it is clear that Darwin connection with evolutionary principles. recognized this duality. Biologists have at- Hull (1965) presciently described taxonomy tempted to resolve this dualism in a variety at this time as the inheritor of 2,000 years of of ways during the past 140 years, but it still stasis resulting from the notion that all units exists. For example, Ereshevsky (1992) of classification had to have uniquely defin- stated “Biological systematists attempt to ing (and hence unchanging) characters, an provide a taxonomy of the world’s organic indication that the Darwinian revolution still diversity. Evolutionary biologists attempt to had not penetrated deeply into taxonomic explain why that diversity exists.” practice. Following the publication of Origin of Spe- Other biologists have dealt with Darwin’s cies, taxonomists, by and large, continued to dualism by attempting to replace the pre- concentrate on species as units of classifi- Darwinian taxonomic concept of species cation and tended to ignore evolutionary with one based strictly in evolutionary principles, invoking these principles only to mechanisms or by trying to eliminate the justify taxonomic decisions made follow- species concept altogether. Darwin wrote ing traditional (pre-evolutionary) practices. musingly about the possibility that the spe- Stevens (1992) noted that, at the end of the cies recognized by taxonomists were not evo- 19th century, the primary taxonomic guide- lutionary units, but by the late 1930s this lines for dealing with species were (i) they viewpoint began to gain momentum and fo- should be easily recognizable to laymen, (ii) cus. The Synthetic Theory of Evolution taxonomic nomenclature should be stable, (e.g., Dobzhansky, 1937; Mayr, 1942; Simp- and (iii) there should not be too many son, 1944) sought to synthesize Genetics, names. This led some to assert that species emphasizing the ways in which species inter- were whatever good taxonomists said they acted with their abiotic and biotic surround- were (Regan, 1926; Dobzhansky, 1937; Gil- ings, with Paleontology, emphasizing the mour, 1940; Camp, 1951), echoing one of historical pattern of the origin, diversifica- Species and Research Programs: Brooks, McLennan 119 tion, and extinction of species. The intro- species. Without such integration, taxonomy duced a new dualism into the question of has no scientific basis and evolutionary biol- species in evolutionary biology. The geneti- ogy has no way to determine its units of cal perspective viewed species as reproduc- study. As a paleontologist, Simpson was par- tive units, whereas the paleontological per- ticularly interested in making certain that spective viewed species as historical units. the development of evolutionary biology in- Biologists interested in seeing “evolution cluded the “deep history” evidence pro- in action” concentrated more and more on vided by fossils. He did not view species as local inbreeding populations (or demes), either “stages” or “products” of evolution claiming that these groups of “replicators” but rather as “active participants” in evolu- were the most inclusive level of evolutionary tion, identifying them as historical lineages processes (e.g., Ehrlich and Raven, 1969). that carried part of the past with them and After all, Dobzhansky (1937) had asserted also responded to long-term selection pres- that species were “stages” in evolution, sures. which only appeared well delimited to us For founding neo-Darwinians like Simp- because we were unable to see them son, two problems arose from viewing spe- through significant periods of time, while cies solely as reproductive units. First, the Mayr (1942) suggested that they were “prod- collection of demes construed as repre- ucts” of evolution. A critical step in develop- senting a species often exhibits more geo- ing this view was the emergence of what graphical and ecological cohesion and tem- Mayr (1942, 1963, 1988) called populational poral persistence than the demes themselves thinking. Advocates of populational thinking (demes can disappear and re-form without treat species as assemblages of organisms destroying the species), suggesting that held together by reproductive bonds that there is reality to collections of demes. Sec- are exclusive to them, which can develop ond, if species are not real, then neither is like an individual organism (but do not have speciation, and evolution is reduced solely to die of old age), and “reproduce” by some- to processes involved in reproductive ex- thing analogous to binary fission. This ap- change within individual demes—that is, proach allowed biologists to move away from changes in gene frequencies in populations. a static or typological view because it treated This view gives no explanation for the ori- species as collections of organisms charac- gins of the diversity of demes and collections terized by both common and variable traits. of demes that the population geneticists Emphasis on populational thinking, how- were studying. Speciation, then, is a real evo- ever, undermined the belief that species lutionary process involving collections of were central to evolutionary theory. Popula- demes but manifested at the level groups of tion geneticists soon learned that the actual demes irreversibly split from each other into reproductive structure in many species lies two or more sets of descendant demes. at the level of local breeding units (demes), not at the level of the entire species. This led The Eclipse of History in many to conclude that only demes and Species Concepts populations were real, with species being taxonomic artifacts. One of the earliest and From 1955 to 1975 a major modification most influential advocates of this perspec- of neo-Darwinism occurred. Spearheaded by tive was Julian Huxley, editor of The New Sys- luminaries such as Robert MacArthur and tematics (Huxley, 1940), and ironically, a de- E. O. Wilson, the ‘Evolutionary Ecology’ scendant of Darwin’s most influential and movement changed neo-Darwinism from a vocal advocate, Thomas Huxley. synthesis of Genetics and Paleontology to a Simpson (1944, 1953, 1961) was among synthesis of Genetics and Ecology. Advo- the few founders of the New Synthesis who cates of this new view claimed that the focus actually advocated a synthesis by integrating of evolutionary processes was interacting the taxonomic and evolutionary concepts of phenotypes (“interactors”) making up eco- 120 Journal of Nematology, Volume 31, No. 2, June 1999 logical communities rather than gene flow that reduce the probability of making a mat- among “replicators” within populations. Van ing mistake. Valen (1976) codified this perspective for Complements to isolation concepts are species concepts by rejecting “reproductive those that concentrate on what it is that concepts” of species in favor of an “ecologi- makes each species a coherent system. An cal species concept.” He asserted that each original proponent of such views has been species had its own unique niche and it was Paterson (1978, 1982, 1985, 1987), whose the niche, an ecological concept, that de- Recognition Concept defines species as groups fined the species. He also stated that evolu- of individuals held together by a common tion was ecologically controlled, since selec- and unique Specific Mate Recognition Sys- tion acts on phenotypes, that phenotypes tem (SMRS). This and related ideas (e.g., are produced by individual ontogenies re- Templeton, 1989) are cohesion concepts of sulting from reproduction, and that repro- species, following the use of “cohesion” by duction is under ecological control. Finally, Wiley (1978, 1981) (Brooks and Wiley, 1988; phenotypes are the building blocks of com- Wiley and Brooks, 1982). Cohesion concepts munities—another ecological concept. Thus, are based on the notion that while there is phylogeny was simply a by-product of ecol- an evolutionary penalty or cost to be paid ogy. for not reproducing, evolutionary benefits The Evolutionary Ecology revolution arise from the evolution of cohesion-en- eliminated history from the evolutionary hancing traits. arena, forcing biologists to define species us- All non-dimensional species concepts ing “non-dimensional” or “relational” spe- strive for a universally applicable definition cies concepts. Such concepts take the form of what species are. Isolation concepts, how- of “A is a species relative to B and C if it ever, can be judged only when we know what maintains its identity as a distinct entity rela- constitutes a mistake in breeding, and cohe- tive to B and C” (Mayr, 1988; Lo¨ther, 1990). sion concepts can be applied only when we These concepts embody no sense of the ori- know what constitutes a penalty for not re- gin of the species, or of their history. The producing. Lo¨ther (1990) noted that non- prevailing non-dimensional species concept dimensional species concepts become pro- for more than a quarter century has been gressively more ambiguous as the species be- the Biological Species Concept (BSC), proposed ing compared become more distant in space by Dobzhansky (1937, 1940, 1970, 1976) and and time. championed most strongly by Mayr (1963, Debate about whether replicators (repro- 1976, 1982, 1988). This concept centered on ductive views) or interactors (ecological the ways in which species maintained a re- views) were the primary focus of evolution productive identity distinct from other spe- continues without producing a clear consen- cies, with a species being a group of inter- sus of opinion (e.g., Futuyma, 1989; Grant, breeding or potentially interbreeding or- 1989). The evolutionary ecology revolution, ganisms reproductively isolated from all however, seemed to signal the end of the other such groups. Van Valen’s Ecological concept of species as historical units and, Species Concept is also non-dimensional, with it, Simpson’s (1944) hopes for an inte- centering on the ways in which species main- gration of taxonomic and evolutionary spe- tain an ecological, rather than reproductive, cies concepts. identity distinct from other species. We refer to these and related species concepts as iso- Ending the Eclipse lation concepts of species (Paterson, 1978, 1982, 1985, 1987). Isolation concepts are based on For those who, despite the Evolutionary the assumption that there is a biological Ecology revolution, continued to believe penalty to be paid by making a mistake in that species and speciation were important mating. This will tend to lead to the evolu- aspects of evolution, a major philosophical tion of traits, called isolating mechanisms, problem was determining how species could Species and Research Programs: Brooks, McLennan 121 be real without being typological or essen- phylogenetic trees. Thus, among the found- tialistic (Hull, 1965). Only then could one ers of the New Synthesis, only Simpson make a case for species as participants in (1944, 1953, 1961) included a sense of evo- evolutionary processes and, hence, as real lutionary history in his conception of what entities. Ghiselin (1974) provided the solu- species were. His suggestion became opera- tion to the problem by considering species tional when E. O. Wiley (1978) linked Sim- as if they were individual, rather than collec- pson’s views on species to the empirical tive, entities (Cracraft, 1983; Donoghue, rigor of phylogenetic systematics (Hennig, 1985; Frost and Kluge, 1994; Hull, 1976, 1950, 1966). 1978, 1980; Lo¨ther, 1990; Mayden, 1997; Frost and Kluge (1994) contrasted what Mayden and Wood, 1995; McKitrick and they termed regular science with historical sci- Zink, 1988; Mishler and Donoghue, 1982; ence. In regular science, like Chemistry, Phys- Wiley, 1978, 1980a, 1980b, 1989; Wiley and ics, and Ecology, the basic units of mecha- Mayden, 1999). Biological species are real, nisms, the entities of the science that partici- but not in the same sense that “hydrogen” is pate in the processes explained by that real. A molecule of hydrogen found any- science behave in such a way that each one where, and formed at any time, in the uni- can be defined and classified within the con- verse would be a member of the class hydro- ceptual framework of the discipline. Each gen. By contrast, an organism that looks like entity has a set of defining properties that a tiger on this planet would not be part of exist and are manifested universally. Hydro- the same species as an organism that looks gen is hydrogen anywhere in the universe; like a tiger on another planet unless the two an herbivore is an herbivore as far as eco- organisms shared a common ancestor. logical theory is concerned. Scientific en- Simpson (1944) anticipated at least some deavors that cannot be studied using the sense of Ghiselin’s view of species by empha- methods of regular science invariably deal sizing that species are historically unique lin- with historical phenomena, such as cosmol- eages extending through time. The most ogy or biological evolution. In historical sci- fundamental characteristic of a species is ence, Frost and Kluge (1994) argued, the that its members form cohesive wholes, entities are not natural kinds but historical bound together primarily by unique com- individuals. Theories in historical sciences mon ancestry as well as by unique sets of cannot define their entities precisely. They reproductive bonds or common ecology. To must therefore discover them and can do Simpson, the evolution of a single species that only by approximation. A theory of the was analogous to the development of a Big Bang might postulate that the universe single organism; just as an organism changes ought to be expanding and would stipulate a its appearance without losing its identity discovery method, the Doppler Shift, by during development, so a species can which that expansion might be gauged. But change its appearance without losing its only after a series of such discoveries would identity during evolution. The formation of it be possible to establish whether or not new species is analogous to asexual repro- there was any regularity to the expansion of duction, in which new individuals are dis- the universe. For example, are all the enti- tinct from old individuals because the new ties involved moving at the same speed in individuals form independent evolutionary the same direction? As we know, there is lineages. Over time, distinct historical trajec- much agreement among cosmologists that a tories emerge from the speciation process, Big Bang occurred, and much contention each differing to some degree from its an- about just how that Big Bang is unfolding cestor and closest relatives, but retaining and will unfold over time. Historical sci- some of its ancestry in the form of synapo- ences thus rely on a two-stage process involv- morphies. We take advantage of this histori- ing discovery methods and evaluation crite- cal mosaic nature of the attributes of organ- ria, both of which are necessary and neither isms that comprise species to reconstruct of which is sufficient for robust explanation. 122 Journal of Nematology, Volume 31, No. 2, June 1999

The theory of evolution is a historical Williams (1991) and Maynard Smith and theory, which stipulates that there should be Szathmary (1995). entities that share a unique phylogenetic Wiley (1978, 1981) stated that any general history. We have decided to call those enti- species concept must (i) encompass species ties species. Species function in evolutionary persistence through time (which makes theory as the basic units of the origin, diver- them diagnosable taxonomic units) as well sification, and extinction of biodiversity and as their divergence (their evolutionary role), as the largest inclusive grouping of organ- (ii) recognize that species are cohesive isms that participates in any evolutionary wholes, and (iii) recognize the inherent his- process. Species are the unique historical toricity of species. Kornet’s (1993) rigorous lineages that make up the hierarchy of phy- logical analysis concluded that species func- logenetic diversification. Species are derived tion in evolutionary theory as mutually ex- from ancestral species via a number of dif- clusive, non-arbitrary (discovered, not im- ferent possible mechanisms of speciation, the posed sensu Frost and Kluge, 1994) histori- irreversible splitting of ancestral lineages cal entities. In a similar vein, Frost and into descendant ones. With the advent of Kluge (1994; Kluge, 1990) consider species phylogenetic systematic methods, which to be genealogical systems (implying cohe- provided a strong empirical method for re- sion) existing as lineages of reproductive covering the phylogenetic hierarchy, came connection extended through time, preserv- the possibility of discovering the basic units ing a unique mixture of genetic informa- of that hierarchy and asking empirical ques- tion. Following these authors, therefore, we consider the Evolutionary Species Concept tions about their origins. to be the fundamental ontological species We will refer to the Evolutionary Species concept for evolutionary biology. As an on- Concept (Simpson, 1944; Mayden and Wood, tological concept, however, the ESC is not 1995; Wiley, 1978, 1980a, 1981; Wiley and operational; it does not specify either discov- Mayden, 1999) and related concepts (the ery modes or evaluation criteria. What is Phylogenetic Species Concept, the Cladistic Spe- needed is an operational surrogate for the cies Concept, and the Composite Species Con- ESC. cept) (Cracraft, 1983, 1992; de Queiroz and In practice, most taxonomists propose Donoghue, 1988, 1990; Donoghue, 1985; El- species names in ways that do not require a dredge, 1985; Eldredge and Cracraft, 1980; particular species concept. We can accept Endler, 1989; Kornet, 1993; McKitrick and such typologically based names as scientific Zink, 1988; Mishler and Donoghue, 1982; hypotheses, but we cannot say that they rep- Ridley, 1989) as historical concepts of species. resent explicit hypotheses of evolutionary Historical concepts integrate well with con- species because, for the most part, the nam- cepts of species as ontological individuals. ing of species by taxonomists follows pre- Eldredge and Gould (1972) and others evolutionary practices (traditions, or histori- (Brooks and Wiley, 1988; Wiley and Brooks, cal constraints on the discipline) (Stevens, 1982), for example, have referred to species 1992). as homeostatic systems held together by co- “There can be no doubt that we learn the hesion provided by common evolutionary use of universal words, that is their applica- history. Lo¨ther (1990) asserted that species tion to individuals, by ostensive gestures and should be considered ontological indi- by similar means.” (Popper, 1968:65). viduals because they are material supra- Nor is it sufficient for us to say that be- organismal systems, spatiotemporally orga- cause we wish to be discovering evolutionary nized and forming an integrated whole. species, our descriptions become hypoth- Prominent evolutionary biologists who have eses of evolutionary species. recently acknowledged the historical nature “Nobody would dream of justifying the va- of species, though not explicitly advocating lidity of a logical inference, or of defending an historical concept of species, include it against doubts, by writing beside it in Species and Research Programs: Brooks, McLennan 123 the margin the following protocol state- ment. ‘Protocol: In checking this chain of inferences today, I experienced an acute feeling of conviction.’ ” (Popper, 1968:98). Thus, until Latin binomina are subjected to a discovery mode appropriate for discern- ing evolutionary species, we do not know whether or not a taxonomist has discovered something that might be an evolutionary species. The operational surrogate for the Evolutionary Species concept, therefore, be- gins with phylogenetic analysis of the collec- tions of organisms given names by taxono- mists.

The Species Problem as a Research Program Discovering species Phylogeneticists use characters as approxi- mations or as extensions (perhaps even metaphors) (E. O. Wiley, pers. comm.) of the entities themselves, the species. Thus, it should not be a surprise that there are several different views on the number of species discovered by any given phyloge- netic tree. Phylogenetic trees comprise two components—apomorphic characters and branches. Any intellectual arena that in- cludes 2 variables (A and B) can give rise to as many as three different viewpoints (only A, only B, both A and B). Not surprisingly, biologists have proposed three distinct cat- FIG. 1. Differences among the three major historical egories of historical species concepts (Baum species concepts with respect to the number of species recognized on a phylogenetic tree. A) Each terminal and Donoghue, 1995). These are embodied and non-terminal branch has a single apomorphic in two forms of the Phylogenetic Species Concept character change; the PSC-1, PSC-2, and CSC all recog- (which we will call the PSC-1 and the PSC-2) nize seven terminal and six non-terminal species. B) and the Composite Species Concept (CSC) (this Three terminal branches lack autapomorphies; the PSC-1 and CSC consider those indistinguishable from view differs slightly from the taxonomy of their common ancestor. C) Four non-terminal species concepts in Mayden, 1997). These branches have more than one synapomorphy; the CSC views differ primarily with respect to how recognizes a distinct species for each. they subdivide a phylogenetic tree and how they deal with the issue of ancestral species. terminal branches, for a total of 13 species. Figure 1 illustrates the similarities and dif- In Figure 1B, species B, C, and G lack apo- ferences among these species concepts. In morphies. Once again, all three species con- Figure 1A, the phylogenetic tree for species cepts recognize A–G as separate species. The A–G is supported by a single apomorphic PSC-2 would again recognize the six non- trait for each non-terminal and terminal terminal branches as separate species, for a branch. All three species concepts recognize total of 13 species. The PSC-1 and CSC, how- A–G as seven species; in addition, all three ever, would recognize only 10 species, since recognize six ancestral species—the six non- B, C, and G are not distinguishable from 124 Journal of Nematology, Volume 31, No. 2, June 1999 their common ancestors. Finally, in Figure The origin and fixation of each apomorphic 1C, four of the non-terminal branches of the trait, it is argued, requires permanent lin- phylogenetic tree have more than one apo- eage splitting; therefore, each apomorphic morphic trait. Once again, all three con- trait indicates the present or prior existence cepts recognize A–G as separate species. of a distinct species. In this regard, the CSC Also once again, the PSC-2 recognizes six differs sharply from the PSC-1 and PSC-2, ancestral species, for a total of 13. The PSC-1 both of which permit evolutionary change recognizes only 10 species, since B, C, and G within a single species lineage, or anagenesis, are not distinguishable from their common a process that cannot occur in the CSC. Ana- ancestors. Finally, the CSC recognizes 15 to- genesis is important for estimating times tal species, one for each apomorphic trait and rates of divergence, and for distinguish- on the phylogenetic tree. These three ex- ing the reproductive and ecological roles of amples demonstrate that the fundamental species (Futuyma, 1989). Consequently, the differences between the approaches have to CSC also presents an a priori constraint on do with how many ancestral species will be the kinds of phenomena evolutionary biolo- recognized. We will see later in this contri- gists may study. bution that these distinctions sometimes, The PSC-1 is the most conservative ap- but not always, are important to research on proach in terms of evidence, requiring evi- species and speciation. dence of both lineage splitting and charac- The PSC-2 is the most consistent of the ter evolution to recognize a species. And yet, historical species concepts since it takes into it is the most open to scientific scrutiny since account only the branching structure of the it does not rule out any putative evolution- tree; it will differ from the PSC-1 only in not ary processes a priori. It can even be chal- permitting the existence of persistent ances- lenged by the postulates of additional spe- tors. The PSC-2 recognizes B, C, and G as cies made by the other two concepts. For the different species from their ancestors on the PSC-2, the hypothesis that a particular ter- basis of evidence of lineage splitting but in minal taxon is not a persistent ancestor can the absence of evidence of character evolu- be corroborated by finding an apomorphy tion (Fig. 1B,C). In terms of evolutionary for the terminal taxon. In such a case, the investigations, however, this species concept number of species recognized by the PSC-1 rules out the possibility of any speciation would increase toward the number recog- modes that involve descendant species nized by the PSC-2. Likewise, for the CSC “budding off” from the ancestral species, the hypothesis that each apomorphy on a with the ancestral species continuing to per- branch was accompanied by lineage splitting sist. If we adopted the PSC-2, we would have would be corroborated each time a new to reject, a priori, a substantial number of taxon that possessed only a subset of the possible modes of speciation. Thus, despite apomorphies of what was considered previ- the attractiveness of stability, we reject the ously to be a single species is found. In such PSC-2 because, in the words of Popper a case, the number of species recognized by (1968:250), “Yet we should abstain from is- the PSC-1 would increase toward the num- suing prohibitions that draw limits to the ber recognized by the CSC. It therefore ap- possibilities of research.” pears that all species recognized by the The CSC is the complement of the PSC-2, PSC-1 are recognized by the PSC-2 and CSC, recognizing species on the basis of evidence and empirical corroboration of the postu- of character evolution alone. It therefore lates of additional species stemming from permits one to recognize species in the ab- either the PSC-2 or CSC will always narrow sence of evidence of lineage splitting. This the gap among all three. Or, to put it an- sets the upper limit on the number of pos- other way, if we say that in the absence of sible species for a given set of organisms and character differences, two species are the their characteristics, providing insight in same, the PSC-1 and PSC-2 become the what we may be missing or may have missed. same concept. Likewise, if we say that in the Species and Research Programs: Brooks, McLennan 125 absence of evidence of lineage splitting, without character change through 2 specia- there has been no permanent lineage split- tion events. The PSC-2 would recognize five ting, the CSC becomes the PSC-1. This species because the ancestor of B + its sister makes the PSC-1 the primary historical spe- and the ancestor ofC+Acould not be the cies concept, with the PSC-2 and CSC em- same species. In such cases, the PSC-1 will bodying challenges to any hypotheses about recognize the correct number of species in- numbers of persistent ancestors or numbers volved, even if the phylogenetic analysis fails of unrecognized irreversible lineage splits. to indicate the correct number of indepen- All three historical species concepts rec- dent speciation events. ognize only those non-persistent ancestral Frost and Kluge (1994) suggested that species for which there is evidence of char- both the CSC and PSC-2 may overestimate acter evolution. As first noted by Wiley the number of species by including entities (1980a), this is due to a limitation of the that do not represent permanent or irrevers- method of phylogenetic systematic analysis, ible lineage splitting (see also Kornet [1993] from which the assessment of species stems. and discussion later in this contribution). As Figure 2A shows the historical sequence of our ability to discriminate groups of organ- two speciation events producing terminal isms at the molecular level improves, this species A, B, and C. The common ancestor will become a non-trivial concern. Frost and of A, B, and C is indicated by an apomorphic Kluge (1994) believed it is contradictory to trait; likewise, B and C exhibit autapomor- say that a species can survive itself; that is, it phic traits. Figure 2B shows the phylogenetic is logically inconsistent to recognize persis- tree for these taxa and characters resulting tent ancestors. However, as we have shown from phylogenetic systematic analysis. For above, the way in which the PSC-2 and CSC Figure 2B, the PSC-1 and CSC would recog- may overestimate lineage splitting is by nize three species (A, B, and C), with A be- counting only lineages or only apomorphic ing a persistent ancestor; the PSC-2 would traits, thus postulating taxa in the absence of recognize four species, since A and the an- evidence of lineage splitting and character cestor cannot be the same species. For Fig- evolution. If we should not recognize spe- ure 2A, the PSC-1 and CSC would still rec- cies unless there is evidence of both lineage ognize three species (A, B and C), with A splitting and character evolution, as embod- being an ancestral species that persisted ied by the PSC-1, it is logically inconsistent

FIG. 2. Limits of resolution of phylogenetic analysis with respect to speciation. A) Pictorial depiction of two episodes of speciation in which the common ancestor does not disappear, resulting in three distinct species. B) Cladogram of those three species derived from phylogenetic analysis. 126 Journal of Nematology, Volume 31, No. 2, June 1999 to state that there can be no persistent an- ciation. We will touch on three of these re- cestral species because the PSC-1 permits search programs in this paper, emphasizing persistent ancestors to be postulated. At the that having a phylogenetic tree is necessary same time, we must point out that there are but not sufficient for the study of speciation. substantial technical difficulties associated In other words, we need to study what spe- with designating particular species as persis- cies are in order to understand why species tent ancestors even in a phylogenetic con- are. text (Wiley, 1981). Stevens (1992) recently noted, “It is not Evaluating species clear to me that our taxonomic interests can As noted above, Frost and Kluge (1994) be squared with the taxonomic species. We stated that both discovery methods and are interested in the whole process of evo- evaluation criteria were required for assess- lution, not only in what ‘has evolved.’ ” The ing evolutionary species. Through phyloge- ESC and its operational surrogate, the PSC- netic systematics, we discover historical, mu- 1, seem to bridge this gap. For most evolu- tually exclusive, and diagnosable entities. tionary biologists, this breakthrough would Our ontology suggests that, among such en- seem to be a cause for universal rejoicing. tities, the ones that comprise evolutionary Yet it is not so. For example, Frost and Kluge species will be cohesive systems and partici- (1994) and Frost et al. (1992) believed that pants in speciation processes. Examining taxonomy ought to reflect evolutionary his- the ways in which species maintain their tory. At the same time, they asserted that identities and in which new species are considerations of evolutionary processes formed thus constitutes valuable research should not intrude on systematic practice. aimed at evaluating our understanding of This perspective views the relationship be- species and the evolution of biodiversity tween pattern and process in science as one (Brooks and McLennan, 1991). of antagonism rather than complementarity. If one proceeds from a non-dimensional But if we are to maintain that there is no species concept, these phenomena can be necessary connection between systematics studied only indirectly by means of models and the unifying principle of biology, what is used as exemplars or metaphors of possible the point of systematics? We believe this po- evolutionary phenomena. For example, sition is impossible. For example, Frost and studies of the modes by which species origi- Kluge’s (1994) own assertion that there nate are often done by comparing two spe- can be no persistent ancestors invokes pro- cies presumed to be “closely related” (this hibitions about certain evolutionary mecha- usually means they are congeneric, con- nisms, thereby giving weight to alternative flating taxonomy with phylogeny) and mechanisms. which exhibit certain geographic and demo- We also believe this position is undesir- graphic features predicted by theories of able. It appears that in the absence of guide- particular modes of speciation. If data com- lines provided by the overarching/unifying paring those two species conform to theory, theory, decision-making about species based it does not matter if the species are, in fact, solely on patterns must eventually resort to sister species (i.e. actual products of a par- authoritarianism to maintain their position ticular speciation event). What is important as species. We do not think this will generate is the use of a system defined not by evolu- support for systematics. For example, de- tion but by the investigator, using naturally spite Frost and Kluge’s (1994) recommen- occurring biological units as variables in a dation that the term “speciation” be retired model of how speciation might work. Such or used only to refer to studies of the modes studies are interested in finding natural- of initiating irreversible splits in historical appearing support for models of speciation lineages, biologists working on several dif- rather than explaining the origins of any ferent types of research programs will con- particular species. Likewise, studies of the tinue to say that they are interested in spe- evolution of the traits by which species main- Species and Research Programs: Brooks, McLennan 127 tain their individuality need only document ciation, in which two existing species fuse to the ways in which any particular species form a third. Harlan and DeWet (1963) pro- maintains itself as a single evolutionary sys- posed the term “compilo-species” for cases tem and then use those traits as the expla- in which one species absorbs another; how- nation for the emergence of the species in ever, examples of this phenomenon have the first place. Such studies are fueled by the not been documented to date. The second is belief that it is impossible to reconstruct past phyletic speciation, in which forms in a gradual evolutionary events. progression within a single lineage are as- If one begins with a historical species con- signed species status at different points in cept, however, these investigations can be time. As noted above, we consider each in- performed in a more direct manner. This dividually evolving lineage to be a single spe- approach emphasizes explaining actual spe- cies; therefore, phyletic speciation repre- ciation events. By dealing with actual specia- sents evolutionary change within a single tion events, the investigator gains informa- species, termed anagenesis. The third class, tion about the workings of different specia- additive speciation or cladogenesis, is character- tion modes that can be used, in part, to test ized by an increase in the number of species. and refine models of speciation. This, in The majority of speciation models, although turn, permits us to ask questions about the based on several different mechanisms, are relative frequency of occurrence of different models of additive speciation. The most im- modes based on empirical observations portant thing to remember about speciation rather than theoretical possibilities. Pro- is not that it produces species, but that it ceeding from a historical species concept produces sister species, so you cannot formu- also provides a way to examine theories late explanations about speciation modes about the evolution of cohesive and isolat- based on analysis of a single species. Rather, ing traits without having to stipulate their you need to examine sister species and existence and significance a priori. clades. Wiley (1981; see also Bush, 1975a, 1975b; Modes of initiating speciation Endler, 1977; Felsenstein, 1981; Lande, The fusion of ecology and population ge- 1980, 1981; Mayr, 1954, 1963; Templeton, netics in the 1960s produced a world view in 1980, 1981, 1982, 1989; White, 1978; Wiley which a number of fundamental evolution- and Mayden, 1985; Wright, 1978) suggested ary processes, including speciation, were that various models of additive speciation simply demographic accidents, whose prob- could be studied if phylogenetic, biogeo- ability was based on variables such as popu- graphic and population biological data were lation structure, patterns of isolation, and available, and if three assumptions could be differential selection pressures. In such met. First, character evolution must provide cases, it is not necessary to isolate each par- a reliable basis for reconstructing sequences ticular speciation event; all one needs to do of speciation events; that is, speciation has is find situations that conform to various left a trace of its action which we can detect. models, even if the species involved are not This assumption requires the operation of sister species. The historical ecological per- one of two processes—character evolution spective, however, is that each speciation tightly coupled with speciation (punctuated event has its own explanation, though the equilibrium) or character evolution that oc- realm of possible modes is small enough curs at the same or higher rate than lineage that we can refer to a set of speciation mod- splitting. Thus, even if the divergence of par- els. The emphasis is on explaining indi- ticular characters is not driving the diver- vidual speciation events and only asking if gence of the lineages, there will be a histori- there are general trends after we have accu- cal trail of character anagenesis highlighting mulated a significant number of cases. speciation events. Although the second con- Mayr (1963) recognized three general dition represents the traditional perspective classes of speciation. The first is reductive spe- of evolutionary biologists, the recent advent 128 Journal of Nematology, Volume 31, No. 2, June 1999 of punctuated equilibrium models (El- not been obscured by rampant dispersal of dredge and Gould, 1972) has strengthened the descendant species. Pairs of sister spe- the proposition of a causal relationship be- cies or clades that show such dissemination tween character modification and specia- may be identified by large-scale sympatry; tion. The first assumption is violated if gene however, uncovering such sympatry creates flow is halted permanently between popula- a problem because it is difficult to determine tions at a faster rate than character change is whether the current distribution pattern ex- occurring. If this happens, the traits present isted during the speciation of the group, or in each species will represent a combination whether it represents widespread dispersal of (i) characters that existed prior to the following speciation in isolation. This high- isolation of the populations, providing infor- lights an important and often misconstrued mation about common ancestry (symplesio- aspect of the relationship between specia- morphies) and (ii) evolutionary modifica- tion and dispersal. The third assumption tions that occurred subsequent to the popu- does not state that dispersal is unimportant, lation’s isolation, providing information it states only that post-speciation dispersal about the unique status of the population does not overwhelm speciation patterns. (autapomorphies). Since derived traits are Like many biological assumptions, this is a not shared between populations under necessary starting point because without it these circumstances, sequences of specia- we have no a priori justification for attempt- tion events will be difficult or impossible to ing to reconstruct speciation patterns, and determine. thus no hope of studying the process. Unlike The second assumption is that there have many biological assumptions, data are avail- been no extinctions in the clade. If we are to able to examine the validity of this supposi- use phylogenetic trees to study particular tion. For example, Lynch (1989) examined modes of speciation, we must have confi- the distributions of 66 pairs of sister species dence that sister species are each other’s and concluded that sister species rarely ex- closest relatives and not, in reality, more dis- hibit significant geographic overlap. tantly related due to the extinction of sev- It is probably true that many groups will eral unknown intermediate species. Con- not satisfy all the assumptions; however, un- sider the following hypothetical example. til a larger database is established, it is im- Two groups of fish, demonstrated to be sis- possible to determine whether these non- ter species on the basis of a phylogenetic conformists need be accorded the status of analysis, are located on either side of a an overwhelming majority or a confounding mountain range. Based on these observa- minority. We are confident that enough tions, we might hypothesize that the disjunct clades will emerge that satisfy the assump- distribution was caused when the upheaval tions given above to enable us to investigate of the mountains separated the ancestral particular speciation models directly. species into two populations, which subse- quently diverged in isolation. Unfortunately Cohesion and Isolation: for our theory, a group of enthusiastic pale- Maintaining “Specieshood” ontologists discover an abundance of fossil evidence, suggesting that at least two other Fertilization systems and specific-mate species fall between the extant representa- recognition systems (SMRSs) lie at the core tives. Hence, the current disjunction of of both cohesion and isolation concepts of fishes B and C was probably derived through species. A fertilization system includes mate a series of speciation and extinction events, recognition, courtship events (premating only one of which need have been associ- mechanisms) leading to fertilization, and ated with the tectonic activity. recognition of gametes in fertilization (post- The third assumption postulates that the mating events); an SMRS is the subset of influence of geographical separation during attributes of a fertilization system that pro- the evolutionary divergence of a clade has mote cohesion in particular social and eco- Species and Research Programs: Brooks, McLennan 129 logical contexts. Thus, for cohesion con- terson, 1978, 1982, 1985, 1987). In such cepts a species is the “most inclusive popu- cases, however, the other two classes of co- lation of biparental individual organisms hesion-enhancing processes also can oper- which share a common fertilization system” ate and, in the absence of adaptation to spe- (Paterson, 1985); for isolation concepts a cific habitats, promote the emergence and species is “a reproductive community of maintenance of the species as a distinct evo- populations (reproductively isolated from lutionary system. Other species may origi- others) that occupies a specific niche in na- nate under conditions of secondary contact ture” (Mayr, 1982). From this starting point with species with which there is a possibility we can derive three general classes of phe- of making mistakes in mating. In such cir- nomena that enhance species cohesion. Sex- cumstances, adaptation to specific habitats ual selection promotes cohesion through ef- and sexual selection enhancing cohesion fects on pre-mating events. Changes in the are called pre-mating isolating mechanisms rest of the genetic components of the fertil- (Mayr, 1963). In a complementary manner, ization system (gamete recognition, fertiliza- changes in the other parts of the fertiliza- tion, ontogeny) promote cohesion through tion system under such conditions that en- effects on post-mating events. Finally, adap- hance cohesion are called post-mating isolat- tation to specific habitats promotes cohe- ing mechanisms (Mayr, 1963). Finally, some sion through effects on the social and envi- species may originate under conditions of ronmental context of pre- and post-mating primary contact with species—often their events. sister species—with which there is a possibil- These three classes of phenomena can en- ity of making mistakes in mating. Once hance cohesion in two ways. First, the worst again, all three classes of cohesion-enhanc- thing that can happen to a species is to go ing processes can operate under such con- extinct. Individual organisms contribute to ditions to promote the emergence and the maintenance of a species by breeding. maintenance of the species as a distinct evo- Thus, for all species there is an evolutionary lutionary system. penalty for individuals not breeding. All co- Thus, it appears that the distinction be- hesion-enhancing processes have the effect tween cohesion and isolation concepts of of reducing the probability of not breeding. species does not involve different evolution- Second, there is also an evolutionary penalty ary mechanisms so much as it involves ques- for organisms that make mistakes in breed- tions of the degree and timing of geographi- ing (mating with a member of a different cal contact between an emerging species species). All cohesion-enhancing processes and other species with which it might make also have the effect of reducing the probabil- a mating mistake. For isolationists, such as ity of making a mistake in mating. When Mayr, geographic isolation (by dispersal or there is only the possibility of being penal- by vicariance) leads to post-mating isolating ized for not breeding, we refer to cohesion mechanisms as a result of genetic diver- concepts of species. When there is also the gence under selection or by drift; secondary possibility of being penalized for making a contact leads to selection for pre-mating iso- mistake in breeding, we refer to isolation lating mechanisms when it is evolutionarily concepts of species. costly to make mating mistakes. For cohesive Some species originate under conditions species advocates, such as Paterson, geo- of spatial separation from those species with graphic isolation leads to the emergence of which there is a possibility of making mis- a unique SMRS (a synonym for the suite of takes in mating and never come into contact features that make a species a cohesive in- with those species. When adaptation to spe- formation system); at secondary contact, or- cific habitats under such conditions leads to ganisms having one SMRS do not recognize the evolution of a new SMRS (also possibly those having another, so there are no mat- including pre- and post-mating phenom- ing mistakes. Viewed in this way, we can see ena), we have the Recognition Concept (Pa- that “isolation” is a special case of “cohe- 130 Journal of Nematology, Volume 31, No. 2, June 1999 sion,” based on secondary contact with any ing right now. These splits should be rela- species sharing enough plesiomorphic com- tively numerous, localized, locally differenti- ponents of the mating system that mating ated, and highly similar due to their close mistakes could be made, in a system where common history, so naturally replicated ex- there is an evolutionary penalty for making emplars will abound. These are the best sys- mating mistakes. tems for population biologists to study. In general, we expect a host of demographic Macro- and Micro-species phenomena, such as local extinctions and fusion with other such splits as a result of Some biologists studying species and spe- dispersal and gene flow, to limit the number ciation still disavow historical approaches, of such micro-species that experience per- reiterating the belief that phylogenies per- manent splits. These lineages experiencing mit us only to see what happened in the permanent (irreversible) splits, the macro- past, and that does not help us understand species, tell us what actually happened and what is happening now or what might hap- may give us insights into constraints on the pen in the future. Some systematists, in re- evolutionary future. They indicate which of turn, have adopted an equally reductionist the micro-species become macro-species in view, namely that it is only through historical their own rights, establishing yet more sets approaches that we learn anything about of micro-species. These species should be species and speciation. We believe that both less numerous than the micro-species and components are necessary, but not suffi- should be better individuated because they cient, for providing truly robust evolutionary embody a history of irreversible change. explanations. We suggested above that Kor- These are the species that systematists find net’s Composite Species Concept (CSC) was easiest to characterize, and they are the ones not our choice as the general historical spe- with which we can most easily do macroevo- cies concept because it does not allow ana- lutionary analyses. Because they define the genesis or vicariance. Kornet’s proposal, historical context within which the micro- however, embodies a critical element for dynamics are played out, we will be better truly integrative studies of species and spe- able to understand, from a phylogenetic ciation, and gives us insight into the funda- perspective, the conditions under which mental relationship between micro- and they emerged than the processes that main- macroevolution. tain them today. The evolutionary ecology revolution es- For example, isolationists, such as Mayr, tablished a perspective whereby evolving postulated that geographic isolation (by dis- species are commonly viewed as collections persal or by vicariance) leads to post-mating of populations distributed horizontally isolating mechanisms as a result of genetic across geography (e.g. Brown and Gibson, divergence by selection or drift. Secondary 1984; Brown, 1995). Kornet (1993) viewed contact between isolated and partially differ- them as lineages sub-divided into smaller entiated populations would lead to selection lineages extending through time. Some of for pre-mating isolating mechanisms when it those lineages experience permanent, or ir- is evolutionarily costly to make mating mis- reversible, splits from each other; many oth- takes. So, we may be able to identify circum- ers do not. From a purely historical stand- stances in which there is selection pressure point, Kornet (1993) considered only those for pre-mating isolating mechanisms. That, lineages experiencing permanent splits to however, does not mean that any such thing be different species. will evolve. If pre-mating isolating mecha- Those species experiencing non-perma- nisms do not evolve under such circum- nent, or reversible, splits represent the stances, we expect the populations split realm of possibilities for what might happen apart by geographic isolation to re-establish in the future—the realm of what is happen- levels and forms of genetic exchange char- Species and Research Programs: Brooks, McLennan 131 acteristic of the parental species, in which Conclusions case we would find that the split was not permanent. “Theories are nets cast to catch ‘the These macro-species can be considered world’ . . . We endeavour to make the mesh emergent, historical macrostates whose mi- ever finer and finer.” (Popper, 1968:59). crostates are the micro-species contained Darwin (1859, 1872) worried that not all within them. As macrostates, these historical taxonomic species corresponded to systems lineages do not themselves participate in affected by natural selection and that not all any active processes—they are the statistical systems affected by natural selection were average or summation of their constituent species. We believe that the various non- micro-species. Those micro-species, in turn, dimensional species concepts proposed cap- do not participate directly in any macroevo- ture different parts of the world of biological lutionary phenomena. Only those that diversity. Because species are produced by achieve the status of permanent splits, that individual speciation events, we should not experience irreversible splitting from their expect any particular non-dimensional con- ancestral lineage, do so. Such macro-species, cept to apply to all species, perhaps not even in turn, provide the historically constrained to all members of a given clade. We also arena within which the dynamics of new mi- believe that, in general, both population bi- cro-species are played out, and from which ologists and systematists recognize real new macro-species may emerge. causal units of evolution. Neither one, how- Kornet’s (1993) distinction between non- ever, is reducible to the other, and robust permanent (reversible) splits (micro-species) explanations about both the origin and and permanent (irreversible) splits (macro- maintenance of these systems through time species) thus provides us with a clear view of require information from both micro- and a major component differentiating micro- macroevolutionary sources. and macroevolution. That component is not Not having a universally agreed-upon spe- magnitude but rather quality. It embodies cies concept has not impeded our learning time, and history, because it is the difference much about species and their origins. Nei- between reversible and irreversible phenom- ther has it been, nor should it now be, an ena (Wiley and Brooks, 1982; Brooks and impediment to describing and naming taxo- Wiley, 1988). Adopting this view helps us nomic entities. The study of species has “make up for lost time” in evolutionary bi- been powered by disagreements among bi- ology, helping end the eclipse of history. ologists. It is thus important for biologists to And there is nothing mysterious about the continue to argue about, and apply, many reversible/irreversible distinction. Maynard different operational species concepts in or- Smith and Szathmary (1995) recently sug- der to continue to expand our realm of gested that biological processes become ef- knowledge about evolution. The hierarchi- fectively irreversible whenever two or more cal research program outlined in this con- individually improbable events affect a given tribution is one effort to catch biological di- system sequentially in time. To this we would versity in a net of “mesh ever finer and add that both micro- and macro-species can finer.” The alternative is to doom biologists be affected irreversibly by extrinsic factors to the role of the blind trying to describe an (the nature of the conditions), most notably elephant. tectonic activity or major changes in envi- ronmental conditions or environmental Literature Cited harshness (Cracraft, 1985). Such influences Baum, D. A., and M. J. Donoghue. 1995. Choosing can be singular and need not be improbable among alternative “phylogenetic” species concepts. Sys- tematic Botany 20:560–573. a priori (though they may be probabilistic Bowler, P. J. 1996. Life’s splendid drama. Chicago: rather than deterministic in their occur- University of Chicago Press. rence). Brooks, D. R., and D. A. McLennan. 1991. Phylogeny, 132 Journal of Nematology, Volume 31, No. 2, June 1999 ecology and behavior: A research program in compara- and clines. 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