Species Concepts and Phylogenetic Theory

A Debate

Quentin Wheeler, Rudolf Meier

• Publisher: Columbia University Press
• Year: 2000
• ISBN:
  9780231506625
• Topic: Biological Sciences
• Subtopic: Evolution
• Index: Biological Sciences

No question in theoretical biology has been more perennially controversial or perplexing than "What is a species?" Recent advances in phylogenetic theory have called into question traditional views of species and spawned many concepts that are currently competing for general acceptance. Once the subject of esoteric intellectual exercises, the "species problem" has emerged as a critically important aspect of global environmental concerns. Completion of an inventory of biodiversity, success in conservation, predictive knowledge about life on earth, management of material resources, formulation of scientifically credible public policy and law, and more depend upon our adoption of the "right" species concept.

Quentin D. Wheeler and Rudolf Meier present a debate among top systematic biology theorists to consider the strengths and weaknesses of five competing concepts. Debaters include (1) Ernst Mayr (Biological Species Concept), (2) Rudolf Meier and Rainer Willmann (Hennigian species concept), (3) Brent Mishler and Edward Theriot (one version of the Phylogenetic Species Concept), (4) Quentin Wheeler and Norman Platnick (a competing version of the Phylogenetic Species Concept), and (5) E. O. Wiley and Richard Mayden (the Evolutionary Species Concept).

Each author or pair of authors contributes three essays to the debate: first, a position paper with an opening argument for their respective concept of species; second, a counterpoint view of the weakness of competing concepts; and, finally, a rebuttal of the attacks made by other authors. This unique and lively debate format makes the comparative advantages and disadvantages of competing species concepts clear and accessible in a single book for the first time, bringing to light numerous controversies in phylogenetic theory, taxonomy, and philosophy of science that are important to a wide audience. Species Concepts and Phylogenetic Theory will meet a need among scientists, conservationists, policy-makers, and students of biology for an explicit, critical evaluation of a large and complex literature on species. An important reference for professionals, the book will prove especially useful in classrooms and discussion groups where students may find a concise, lucid entrée to one of the most complex questions facing science and society.

PART 1

Position Papers (Point)

2

The Biological Species Concept

Ernst Mayr

I define biological species as groups of interbreeding natural populations that are reproductively isolated from other such groups. Alternatively, one can say that a biological species is a reproductively cohesive assemblage of populations. The emphasis of this definition is no longer on the degree of morphological difference, but rather on genetic relationship. This species concept represents a complete change in the ontological status of species taxa. For those who adopt the Biological Species Concept, species are no longer considered to be classes (natural kinds) that can be defined, but rather concrete particulars in the view of the biologist that can be described and delimited but not defined. Species status is the property of populations, not of individuals. A population does not lose its species status when an individual belonging to it makes a mistake and hybridizes. The word interbreeding indicates a propensity; a spatially or chronologically isolated population, of course, is not interbreeding with other populations but may have the propensity to do so when the extrinsic isolation in terminated.

The increasingly wide adoption of the Biological Species Concept was facilitated by the discovery of two fatal flaws in the Typological Species Concept. More and more often species were found in nature with numerous conspicuously different intraspecific phena—that is, differences caused by sex, age, season, and ordinary genetic variation—with the result that members of the same population sometimes differed more strikingly from each other than generally recognized good species. Conversely, in many groups of animals and plants, extremely similar and virtually indistinguishable cryptic species were discovered, the individuals of which, when coexisting, did not interbreed with each other but maintained the integrity of their respective gene pools. Such sibling species are perhaps more common in animals than in plants, but they certainly invalidate a species concept based entirely on degree of difference. Let us examine the origins of the Biological Species Concept.

HISTORICAL CONSIDERATIONS

The Biological Species Concept developed in the second half of the nineteenth century. Up to that time, from Plato and Aristotle until Linnaeus and early nineteenth century authors, one simply recognized species, eide (Plato), or kinds (Mills). Because neither the taxonomists nor the philosophers made a strict distinction between inanimate things and biological species, the species definitions they gave were rather variable and not very specific. The word species conveyed the idea of a class of objects, members of which shared certain defining properties. Its definition distinguished a species from all others. Such a class is constant, it does not change in time, and all deviations from the definition of the class are merely accidents, that is, imperfect manifestations of the essence (eidos). Mills in 1843 introduced the word kind for species [and Venn (1866) introduced natural kind], and philosophers have since used the term natural kind occasionally for species (as defined above), particularly after B. Russell and Quine had adopted it. However, if one reads a history of the term natural kind (Hacking 1991), one has the impression that no two authors meant quite the same thing by this term, nor did they clearly discriminate between a term for classes of inanimate objects and biological populations of organisms. There is some discussion among philosophers about whether there are several types of natural kinds, but I will refrain from entering that discussion. The traditional species concept going back to Plato’s eidos is often referred to as the Typological Species Concept.

The current use of the term species for inanimate objects such as nuclear species or species of minerals reflects this classical concept. Up to the nineteenth century this also was the most practical species concept in biology. The naturalists were busy making an inventory of species in nature, and the method they used for the discrimination of species was the identification procedure of downward classification (Mayr 1982, 1992a). Species were recognized by their differences; they were kinds, and they were types. This concept was usually referred to as the Morphological or Typological Species Concept.

Even though this was virtually the universal concept of species, there were a number of prophetic spirits who, in their writings, foreshadowed a different species concept, later designated the Biological Species Concept. The first among these was perhaps Buffon (Sloan 1987), but a careful search through the natural history literature would probably yield quite a few similar statements. Darwin unquestionably had adopted a biological species concept in the 1830s in his Transmutation Notebooks, even though later he largely gave it up (Kottler 1978, Mayr 1992b). Throughout the nineteenth century quite a few authors proposed a species definition that was an approach to the Biological Species Concept (Mayr 1957a).

Late in the nineteenth century and in the first quarter of the twentieth century, taxonomists such as K. Jordan, E. Poulton, L. Plate, and E. Stresemann were among those who most clearly articulated the Biological Species Concept, as will be shown below.

As long as the inventory taking of kinds of organisms was the primary concern of the students of species, the Typological Species Concept was a reasonably satisfactory concept. But when species were studied more carefully, all sorts of properties were discovered that did not fit with a species concept that was strictly based on morphology. This was particularly true of behavioral and ecological properties. Most damaging was the discovery of the unreliability of morphological characters for the recognition of biological species.

Morphological difference had traditionally been the decisive criterion of species. Population A (e.g., continental North American savanna sparrows) was determined to be a different species from population B (e.g., savanna sparrows from Sable Island, Nova Scotia) if it was deemed to be sufficiently different from it by morphological characters. This definition was very useful in various clerical operations of the taxonomist such as in the cataloguing of species taxa and their arrangement in keys and in collections. However, for two reasons it was inadequate if not misleading for a study of species in nature. The first one is that, as is now realized, there are many good biological species that do not differ at all, or only slightly, morphologically. Such cryptic species have been designated sibling species. They occur at lesser or greater frequency in almost all groups of organisms (Mayr 1948). They are apparently particularly common among protozoans. Sonneborn (1975) eventually recognized 14 sibling species under what he had originally considered a single species, Paramecium aurelia. Many sibling species are genetically as different from each other as morphologically distinct species. A second reason a morphological species concept proved unsatisfactory is that there are often many different morphological types within a biological species, either because of individual genetic variation or different life history categories (males, females, or immatures), which are morphologically far more different from each other than are the corresponding morphological types in different species.

The morphological difference between two species fails to shed any light on the true biological significance of species, the Darwinian why question. So-called morphological species definitions are in principle merely operational instructions for the demarcation of species taxa. The realization of these deficiencies of the Typological Species Concept led, in due time, to its almost complete replacement among zoologists by the so-called Biological Species Concept.

Many of the authors who profess to adhere to the Morphological Species Concept do not seem to realize that unconsciously they base their decisions ultimately on the reproductive community principle of the Biological Species Concept. They combine drastically different phenotypes into a single species because they observe that they were produced by the same gene pool. This had already been done by Linnaeus when he synonymized the names he had given to the female mallard and the immature goshawk.

The biological significance of species is now clear. An organization of the diversity of life into species permits the protection of well-balanced, well-adapted gene pools. Numerous authors have arrived at this conclusion, and it was most recently confirmed by Paterson (1973:32) himself when he said that the study of speciation is “the study of the mechanisms by which isolating mechanisms, which protect the gene pool of a species from introgression, come into existence.” There is only one other way by which superior gene combinations can be protected, and that is by a shift to uniparental reproduction (asexuality). The question that we posed at the beginning, as to the why of speciation, is now answered, and this answer represents the consensus of current evolutionary biology.

The next question to be answered, and it cannot be emphasized too strongly that this is an entirely independent question, is, by what devices is the integrity of a species being maintained? Dobzhansky (1935, 1937) introduced the term isolating mechanisms for these devices. He called them “physiological mechanisms making interbreeding [with nonconspecifics] difficult or impossible” (1935:349). In 1937 (p. 230) he defined as an isolating mechanism “any agent that hinders the interbreeding of groups of individuals,” producing as an effect that “it diminishes or reduces to zero the frequency of the exchange of genes between the groups.”

Dobzhansky was already aware of the independence of the isolating mechanisms from other characteristics of species. “The genetic factors responsible for the production of the isolating mechanisms appear to constitute rather a class by themselves. Thus, mechanisms preventing a free interbreeding may apparently develop in forms that are rather similar genotypically, and vice versa, genotypically more different forms may remain potentially interfertile” (1935:352). Modern studies seem to indicate that in some cases just a few genes may control effective reproductive isolation, whereas in other cases even a rather profound genetic restructuring of populations may not result in reproductive isolation. This is of course an expected manifestation of the incidental nature of the origin of isolating mechanisms and of the prevalence of mosaic evolution.

All authors who have written on isolating mechanisms—for instance, Dobzhansky (1937:228–258) and Mayr (1963:89–109)—have stressed the enormous diversity of such devices. In addition to sterility genes, chromosomal incompatibilities, and ecological exclusion, behavioral properties that facilitate the recognition of conspecifics are most important in higher animals. The existence of such behavioral mechanisms has been well known to naturalists, presumably far back into the nineteenth century or even earlier. Paterson (1978:369) quoted an excellent statement by W. Peterson. Plate (1914) articulated the recognition concept by stating that “the members of a species are tied together by the fact that they recognize each other as belonging together and reproduce only with each other.” I stated that “species are a reproductive community. The individuals of a species of higher animals recognize each other as potential mates and seek each other for the purpose of reproduction” (Mayr 1957a:13). I have always stressed the importance of recognition and devoted several years to an experimental analysis of the sensory cues involved in the reproductive isolation between different species of Drosophila (Dobzhansky and Mayr 1944; Mayr and Dobzhansky 1945; Mayr 1946a, 1946b, 1950).

In view of the long-standing and widespread realization of the important role of recognition in the maintenance of the integrity of the species, it is curious that Paterson thought that he had invented an entirely “new concept of species, the Recognition Concept, which is conceptually quite distinct from the current paradigm, the Isolation Concept” (1980:330). In consequence, Paterson defined the species as the “most inclusive population of individual biparental organisms which have a common fertilization system” (1985:25). In all of his more recent publications, Paterson has stressed the great difference between his new Recognition Concept of species and the old Biological Species Concept. One is somewhat puzzled by this claim when one reads Dobzhansky’s definition of the biological species: “the largest and most inclusive… reproductive community of sexual and cross-fertilizing individuals which share in a common gene pool” (1950:405). Even though virtually all modern evolutionists define a biological species as a reproductive community, Paterson (1981, 1985) has insisted that “the Biological Species Concept is essentially equivalent to the Isolation Concept.” This claim is correct only insofar as the two concepts answer the question of the why of species. The Biological Species Concept, however, also answers the question about the how of species. Indeed, as Raubenheimer and Crowe (1987) correctly pointed out, the behavioral subset of the isolating mechanism specified by Mayr and by Dobzhansky in their supposed Isolation Concept is precisely the characteristic on which Paterson based his Recognition Concept. The fact that Paterson pleaded for the acceptance of his Recognition Concept from 1973 to 1986 in so many (at least six) publications indicates that he is rather disappointed that it has not found broader acceptance.

1. The so-called Recognition Concept does not specify, as does the Biological Concept, what the actual role of species is in nature. It answers the how but not the why question, as was pointed out above.

2. The term recognition is deeply flawed. Many authors such as Paterson, Plate, and numerous students of behavior have been aware of the recognitional aspects of such encounters. I referred to it in the following analysis: “The specific reaction of males and females toward each other is often referred to loosely as ‘species recognition.’ This term is somewhat misleading, since it implies consciousness, a higher level of brain function than is found in lower animals.… ‘[S]pecies recognition,’ then, is simply the exchange of appropriate stimuli between male and female to ensure the mating of conspecific individuals and to prevent hybridization of individuals belonging to different species” (Mayr 1963:95). This statement was followed by nine pages of discussion of such ethological stimuli classified on the basis of the principal sense organs involved.

3. Paterson’s restriction of isolating mechanisms to behavioral recognition excludes all species with postmating isolating mechanisms. Furthermore, if the term recognition is rigidly construed, this species concept would virtually exclude all plant species. However, Paterson actually used the word recognition very broadly, comparing it with the “recognition of a specific antigen by its specific antibody” (1985:25). Consistent with such a broad definition, he also considered interactions “such as [those] between pollen and stigma, or between egg and spermatozoa,” as recognition (1985:25). It is not quite clear why he did not also include here postmating isolating mechanisms effected by an interaction of incompatible chromosomes or genes.

Enlarging the concept of recognition, however, does not solve all problems. There is usually a considerable asymmetry between the sexes. Although females are usually highly discriminating, males in many, if not most, species have a rather generalized image of potential mating partners. Males of a given species in many genera of animals are ready at all times to mate with females of other congeneric species, or even with females of rather distant genera. Males would belong to different species than the females owing to Paterson’s concept because they have a different recognition pattern.

The large number of new species concepts and species definitions proposed in recent years well reflects the seemingly utter confusion in this field. It seems to me that there are four reasons for this state of affairs.

1. We have experienced in the past 250 years the gradual, but only partial, replacement of the previously dominant Morphological Species Concept, based on typological essentialism, by a so-called Biological Species Concept, as discussed above. What the scientist actually encounters in nature are populations of organisms. There is a considerable range in the size of populations, ranging from the local deme to the species taxon. The local deme is the community of potentially interbreeding individuals at a locality (see also Mayr 1963:136), and the species taxon has been referred to by Dobzhansky as the “largest Mendelian population.” The task of the biologist is to assign these populations to species. This requires two operations: (a) to develop a concept of what a species is, resulting in the definition of the species category in the Linnaean hierarchy, and (b) to apply this concept when combining populations into species taxa.

A number of recent writers on the species problem have failed to appreciate that the word species is applied to these two quite different entities in nature: species taxa and the concept of the category species. As a result, their so-called species definition is nothing but a recipe for the demarcation of species taxa. This is, for instance, true for most of the recent so-called phylogenetic species definitions. It is also largely true for Templeton’s (1989, 1994) Cohesion Species Concept. A paper often cited as a decisive refutation of the Biological Species Concept (Sokal and Crovello 1970) is perhaps an extreme example of the confusion resulting from the failure to discriminate between the species as category (concept) and as taxon.

THE SPECIES TAXON

The word taxon refers to a concrete zoological or bo...

Table of contents

• Cover 
• Half title
• Title
• Copyright
• Contents 
• List of Contributors
• Preface
• Introduction
• Part 1. Position Papers (Point)
• Part 2. Critique Papers (Counterpoint)
• Part 3. Reply Papers (Rebuttal)
• References
• Index