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The General Lineage Concept of Species, Species Criteria

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The General Lineage Concept of Species, Species Criteria The General Lineage Concept of Species, Species Criteria, and the Process of Speciation A Conceptual Unification and Terminological Recommendations - Kevin de Queiroz Speciation, the process through which new species come by contemporary biologists. Next, I present evidence that into being, is one of the central topics of evolutionary all modem species definitions describe variants of a single biology. It links the great fields of micro- and macroevo- general concept of species. I then discuss how the time- lutionary biology and intersects a wide variety of related extended nature of species and the diversity of events that biological disciplines, including behavioral biology, ecol- occur during the process of speciation provide the basis ogy, genetics, morphology, paleontology, physiology, for the diversity of alternative species definitions. Based reproductive biology, and systematics. For this reason, a on a distinction between species concepts and species persistent controversy regarding the definition of the term criteria, I propose a revised and conceptually unified ter- species may seem disconcerting. The continual proposal minology for the ideas described by contemporary spe- of new species definitions-commonly characterized as cies definitions, and I discuss the significance and limi- alternative species concepts-seems to suggest that there tations of different classes of species definitions. Finally, is no general agreement about what species are, and if I examine an interpretation of species criteria that places this is the case, then the possibility of understanding how alternative criteria in direct conflict and thus contains the species come into being also seems unlikely. At the very key to resolving the species problem. least, there seems to be considerable potential for mis- interpretation and confusion about what different biolo- gists mean when they talk about species and speciation. Alternative Species Definitions But the situation is not really as troublesome as it may appear. Although real differences underlie alternative spe- Over the last half century, biologists have established a cies definitions, there is really less disagreement about minor industry devoted to the production of new defini- species concepts than the existence of so many alternative tions for the term species. In this section I present a sum- definitions seems to suggest. Each species definition has mary of those definitions, using a terminology proposed a different emphasis, but the various phenomena that they by the authors of those definitions and others comment- emphasize are all aspects or properties of a single kind of ing on their work (see also Haffer, 1986; Hauser, 1987; entity. In other words, almost all modem biologists have Panchen, 1992; King, 1993; Ridley, 1993; Smith, 1994; the same general concept of species. Differences among Vrba, 1995; Hull, 1996; Shaw, this volume; Harrison, this the many versions of this general concept are at least partly volume). My purpose is not to catalog modern species attributable to the complex and temporally extendednature definitions exhaustively but rather to represent their di- of species and the process or processes through which they versity, and my use of an existing terminology is not in- come into existence. In many respects, considering spe- tended to endorse that terminology-indeed, I propose ciation as a temporally extended process is the key to under- what I believe to be a more useful one later in this chap- standing the diversity of species definitions. ter-but rather to reflect current views on the historical In this chapter, I provide a general theoretical context and conceptual relationships among alternative species that accounts for both the unity and the diversity of ideas definitions. References in the headings are for the terms represented by alternative species definitions. First, I themselves (as opposed to their definitions); emphasis has review the major categories of species definitions adopted been removed from quoted passages. 58 SPECIES CONCEPTS Biological Species Concept (eg,Mayr, 1942,1963). shared by conspecific organisms, rather than the repro- This term has been applied to definitions that emphasize ductive isolation between heterospecific organisms. For interbreeding, specifically, the idea that species are popu- example, "members of a species share a common specific lations of interbreeding organisms. Although such defi- mate recognition system" (Paterson 1978:369); "a spe- nitions have ancient roots (e.g., the writings of Buffon, cies [is] that most inclusive population of individual bi- discussed by Mayr, 1982) and were more or less clearly parental organisms which share a common fertilization articulated by authors at the beginning of the twentieth system" (Paterson 1985:25). century (e.g., Poulton, 1903; Jordan, 1905; see Mayr, 1955), they are most commonly associated with the New Evolutionary Species Concept (e.g., Wiley, 1978, Systematics (e.g., Huxley, 1940) of the Evolutionary 1981). This term has been used for definitions empha- Synthesis (reviewed by Mayr and Provine, 1980). Some sizing the extension of species through time and attempt- examples are as follows: "groups within which all sub- ing to accommodate both the observation that some popu- divisions interbreed sufficiently freely to form inter- lations appear to maintain their distinctness despite grading population~wherever they come in contact, but interbreeding with other populations and the idea that between which there is so little interbreeding that such asexual organisms form species. "An evolutionary species populations are not found" (Wright, 1940: 162); "the is a lineage (an ancestral-descendant sequence of popu- largest and most inclusive Mendelian population . [a] lations) evolving separately from others and with its Mendelian population is a reproductive community of own unitary evolutionary role and tendencies" (Simpson, sexual and cross-fertilizing individuals which share in a 1961: 153; see also Simpson, 1951). "A species is a single common gene pool" (Dobzhansky, 1950:405); "groups lineage of ancestral descendant populations of organisms of actually or potentially interbreeding natural popula- which maintains its identity from other such lineages and tions, which are reproductively isolated from other such which has its own evolutionary tendencies and historical groups" (Mayr, 1942:120; see also Mayr, 1963, 1970). fate" (Wiley, 1978:18; see also Wiley, 1981). Other names given to this class of definitions are "inter- breeding-population concept" (Mayr, 1942), "genetical concept of species" (Simpson, 195 I), "reproductive spe- Ecological Species Concept (Van Valen, 1976). This cies concept" (Van Valen, 1976), and "species concepts term was proposed by Van Valen (1976) for his modi- based on interbreeding" (de Queiroz and Donoghue, fication of Simpson's (1961) definition; it emphasizes the importance of ecologically based natural selection 1988). Some authors (e.g., Paterson, 1981, 1985, 1986; Lambert and Paterson, 1982; Masters et a]., 1987) see an in maintaining species: "A species is a lineage (or a important distinction between two subcategories of "bio- closely related set of lineages) which occupies an adap- tive zone minimally different from that of any other logical" or "genetical" species concepts (see below); others (e.g., Mayr, 1988) do not. lineage in its range and which evolves separately from all lineages outside its range" (Van Valen, 1976:233; see also Andersson, 1990). Isolation [Species] Concept (e.g., Paterson, 1985). This term has been applied, by advocates of the altema- tive "recognition concept" (see below), to the views on Cohesion Species Concept (Templeton, 1989). This species articulated by Dobzhansky and Mayr, which em- term was proposed by Templeton (1989) for his own defi- phasize reproductive isolation between organisms of dif- nition, which synthesizes components of the evolution- ferent species. Mayr's (1942, 1963, 1970) definition, ary, ecological, isolation, and recognition definitions. It quoted above, falls into this category, as does the follow- emphasizes the mechanisms that maintain evolutionary ing definition of Dobzhansky: "Species are . systems lineages by promoting genetic relatedness and determin- of populations; the gene exchange between these systems ing the boundaries of populations with respect to mico- is limited or prevented in nature by a reproductive iso- revolutionary processes such as gene flow, genetic drift, lating mechanism or perhaps by a combination of sev- and natural selection. "The cohesion concept [of] species eral such mechanisms" (Dobzhansky, 1970:357). is the most inclusive population of individuals having the potential for phenotypic cohesion through intrinsic &he- Recognition [Species] Concept (e.g., Paterson, 1985). sion mechanisms" (Templeton, 1989: 12). See Templeton This term has been applied to the views on species (1989, table 2) for a summary of proposed cohesion articulated by Paterson (e.g., 1980, 1981, 1985, 1986, mechanisms. 1993a; see also Lambert and Paterson, 1982,1984; Mas- ters et a]., 1987; Lambert and Spencer, 1995) as an alter- Phylogenetic Species Concept (e.g., Cracraft, 1983). native to the "isolation concept." Species definitions This term has been used for at least three distinct classes associated with the "recognition concept" emphasize the of species definitions associated with the taxonomic ide- unification of species rather than their separation from ology known as
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