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Species Concepts and the Evolutionary Paradigm in Modern Nematology

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JOURNAL OF NEMATOLOGY VOLUME 30 MARCH 1998 NUMBER 1 Journal of Nematology 30 (1) :1-21. 1998. © The Society of Nematologists 1998. Species Concepts and the Evolutionary Paradigm in Modern Nematology BYRON J. ADAMS 1 Abstract: Given the task of recovering and representing evolutionary history, nematode taxonomists can choose from among several species concepts. All species concepts have theoretical and (or) opera- tional inconsistencies that can result in failure to accurately recover and represent species. This failure not only obfuscates nematode taxonomy but hinders other research programs in hematology that are dependent upon a phylogenetically correct taxonomy, such as biodiversity, biogeography, cospeciation, coevolution, and adaptation. Three types of systematic errors inherent in different species concepts and their potential effects on these research programs are presented. These errors include overestimating and underestimating the number of species (type I and II error, respectively) and misrepresenting their phylogenetic relationships (type III error). For research programs in hematology that utilize recovered evolutionary history, type II and III errors are the most serious. Linnean, biological, evolutionary, and phylogenefic species concepts are evaluated based on their sensitivity to systematic error. Linnean and biologica[ species concepts are more prone to serious systematic error than evolutionary or phylogenetic concepts. As an alternative to the current paradigm, an amalgamation of evolutionary and phylogenetic species concepts is advocated, along with a set of discovery operations designed to minimize the risk of making systematic errors. Examples of these operations are applied to species and isolates of Heterorhab- ditis. Key words: adaptation, biodiversity, biogeography, coevolufion, comparative method, cospeciation, evolution, nematode, philosophy, species concepts, systematics, taxonomy. Ever since Mayr (1942) codified a species decisions are made by inference; it is never concept in the taxonomic literature based clear what parameters are in place during on reproductive incompatibility (the Bio- the discovery operations. We get the results logical Species Concept, or BSC), nematol- (usually that one isolate is somehow differ- ogists have had to decide, consciously or ent from others) but rarely are they accom- not, whether to use it when describing and panied by any explicit mention of method- classifying nematodes. Subsequently, an ex- ology, or what the differences mean. ~ The tensive literature has been established and extensive diversity ofundescribed nematode currently there are several well-articulated species poses substantive challenges to the species concepts available to taxonomists future of nematode taxonomy. Also, recent (see Ereshefsky, 1992). However, the vast progress in systematic biology and the com- majority of species descriptions within the parative method suggest that many research last decade make no mention of species con- programs in hematology stand to benefit from cepts. Groups of nematodes are isolated and a reevaluation of the philosophical and opera- delimited as species, but a species per se is tional tenets of alternative species concepts. 2 not defined at all. Thus, many taxonomic My intent here is not to address the merit Received for publication 1 May 1997. 1 For an example of this problem as it exists in philosophy i Department of Plant Pathology, University of Nebraska- and evolutionary biology, see Dennett (1995), who views this as Lincoln, Lincoln, NE 68583-0722. analogous to playing tennis with the net down: with no roles, no E-mail: [email protected] one can understand or play the game. Ultimately there is only The author thanks J. G. Baldwin, P. De Ley, V. Ferris, J. D. confusion and nobody has any fun. Lynch, T. O. Powers, and W. Sudhaus for their helpful com- 2 This criticism is not unique to nematology and has been ments on an early version of this paper. J. G. Baldwin, E.C. addressed in other fields including ornithology (Cracraft, Bernard, and an anonymous reviewer provided invaluable con- 1983), herpetology (Frost and Hillis, 1990), and botany (Mc- structive editorial criticism. Dade, 1995). The JOURNAL OF NEMATOLOGY for March (30:1-21) was issued 2 Journal of Nematology, Volume 30, No. 1, March 1998 of species descriptions in nematology. zen (1983) posited: "Systematics has two ob- Rather, my purpose is to show that species jectives. Firstly, the clear ordering and reg- concepts are the crux of taxonomy and that istering of species diversity to facilitate prac- a taxonomy based on irrational species con- tical work with the species. Secondly, the cepts can subvert the goals of our taxonomic formulation of a scientific theory of the evo- endeavors by misrepresenting evolutionary lutionary relationships among species and history and thereby significantly hindering groups of species; therefore, the resulting efforts to recover other types of historical system should be based on phylogenetic ar- phenomena. To mitigate these problems, I guments." advocate an alternative species concept for Few systematists will take issue with this use in nematology, and a methodology for statement. Evolutionary history has pro- its application, duced species that taxonomists hope to re- Before addressing the epistemological cover in order to facilitate practical work. It question of how we can logically recognize is also the taxonomist's objective to repre- an entity as a species (the main thrust of this sent the evolutionary relationships among paper), I need to acknowledge a nontrivial species. Without altering its intent or sub- ontological assumption, that speciation oc- stance, Lorenzen's statement could be sim- curs by cladogenesis, and that the Nemata plified to read, "The reason nematologists are a monophyletic group, s If this is true, do systematics is to recover and represent evo- then for nematode taxonomy to reflect evo- lutionary history." A clear understanding of lutionary history all nematode species must these two objectives is critical because if spe- by definition be monophyletic, 4 a require- cies concepts differ in their ability to accom- ment if species are to be given non-arbitrary plish these goals, then it is possible to recognition. For example, taxonomists use a choose a concept of species least likely to fail variety of operations when naming nema- in this regard. Other species concepts can todes, some theoretical and some prag- be rejected as those more likely to confound matic. But the central underlying premise is or hinder taxonomic endeavors. that the entities we call species are either i) In the following sections I establish crite- species, ii) part of a species, or iii) a mixture ria and evaluate four prominent species con- of two or more species. This ontological dic- cepts based on their ability to accomplish tum exhausts the taxonomic possibilities the two objectives of nematode taxonomy and lets us get on with the task of addressing (Lorenzen, 1983). I will advocate an amal- epistemological problems. The epistemo- gamation of two concepts, explain the utility logical questions I will explore involve the of this new approach in terms of its ability to logical basis for recognizing a particular en- reduce error, and provide a methodology tity as a species. for its implementation. SPECIES CONCEPTS AND THE PURPOSE OF THE SPECIES PROBLEM TAXONOMY As long as the boundaries between popu- To stimulate a more unified approach to lations and species have exhibited variation, systematic endeavors in nematology, Loren- systematists have at some point had to ratio- nalize a way of distinguishing between the two. In the absence of any objective meth- 3 Epistemology deals with the nature of knowledge, or "How do we know we have species?" Ontology deals with the nature odology within the Linnean paradigm, pro- of being, or in this case, "Do we have species?" ponents of alternative species concepts have 4 By this I mean that all individuals that comprise a species must be more closely related to each other than to members of tried to establish objective solutions to the another species. It should be pointed out that there are prob- species problem (the problem of not being lems with extending the term "monophyly" to subspecific en- tities (Plamick, 1977). However, this does not appear to be able to objectively identify just exactly what problematic as long as the phylogenetic patterns among com- is or is not a species). Yet, in every case all parable organisms (semaphoronts) within a species can be rep- resented (but see Nixon and Wheeler, 1990). current species concepts at some level fail to Species Concepts: Adams 3 satisfy the objectives of taxonomy. If repro- more species than actually exist, and type II ductive incompatibility is a requirement of error predicts fewer species than actually ex- species, how can unisexual species or fossils ist. These two errors affect the way in which be accounted for? If species are based solely we meet the first objective of taxonomy, that on the similarities and differences between of accurately recovering species as products populations, exactly how similar or different of evolutionary history. A third type of error must they be? occurs when a depiction of phylogenetic re- Realizing this problem, Myers (1952) lationships among species is incongruent pointed out that definitional species con- with recovered evolutionary history. This er- cepts will always fail because taxonomic ror is distinct in
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