The Biological Species Concept and Species Taxa

In this section I trace the historical development of Mayr's views on the theoretical species concept and on species taxa which were central to his research. It has become evident in recent decades that there are only two theoretical species concepts:

(1) The typological or essentialistic species concept postulates that a species consists of similar individuals sharing the same "typological essence," is separated from other species by a sharp discontinuity, remains constant through space and time (i.e., species limits are fixed), and variation within a species is severely limited. (Regarding Mayr's conceptualization of typological versus population thinking since the late 1940s see p. 350.)7 (2) The biological species concept states that a species is a group of interbreeding natural populations that is reproductively (genetically) isolated from other such groups because of physiological and/or behavioral barriers; the limits of biological species are open.

Other "species concepts" proposed are those of the "vertical" (historical) cladis-tic "species" (W. Hennig) and of the paleontological or evolutionary "species" (G. G. Simpson) which, however, refer to portions of phyletic lineages rather than species (see p. 213). The "chronospecies" of paleontologists, i.e., artificially delimited subdivisions of phyletic lineages, are not species in the sense of biological species. Mayr (1942e: 154) stated: "The 'species' of the paleontologist is not necessarily always the same as the 'species' of the student of living faunae." The recognition concept is a different formulation of the biological species concept (Mayr 1988h). Under each of these as well as the typological and biological species concepts mentioned above authors delimit narrow, intermediate or wide species taxa, depending on whether they place the taxonomic species limits at relatively low, intermediate or rather high levels of differentiation among the geographically representative populations, respectively. Narrow species limits emphasize differences, wide species limits emphasize similarities among the various geographically representative taxa. The so-called phylogenetic species concepts are instructions of how to delimit particularly narrow species taxa, but not theoretical species concepts. Hey (2006) reviewed the long-standing discussion on species concepts under the title "On the failure of modern species concepts."

In their comprehensive treatise of speciation Coyne and Orr (2004) basically adopted Mayr's biological species concept, because the problem of speciation is "the origin of discrete groups of organisms living together in nature. [.] It seems undeniable that nearly all recent progress on speciation has resulted from adopting some version of the biological species concept" (pp. 6-7).The conceptual reasoning as to species limits in molecular population studies is also based on the biological species concept.

While a student in Berlin under Erwin Stresemann, Ernst Mayr had become a representative of the Seebohm-Hartert "school" of European systematic ornithology which had originated in the late 19th century and, during the course of 100 years, widely influenced ornithology through the work of several well-known scientists: Seebohm-Hartert-Hellmayr-Stresemann-Rensch, and later Ernst Mayr himself (Fig. 5.2). The views of these ornithologists as well as those of E. B. Poul-ton, K. Jordan, and Ludwig Plate on biological species, subspecies and speciation

7 This was the species concept of numerous 19th century biologists prior to Darwin (1859) regardless whether they believed in the origin of species through divine intervention (i.e., creation) or through autochthonous (spontaneous) generation from organic matter during periods of special environmental conditions. The views of Linnaeus himself and of several other early naturalists on species were less essentialistic than often stated (Mayr 1982d: 259; Winsor 2006).

around 1900 eventually influenced, through Ernst Mayr, the entire fields of systematic zoology and evolutionary biology.

The concepts of the naturalists of the Seebohm-Hartert "school" (Haffer 1994a) are based on the Darwinian idea of a common descent of all species and on the belief that forms (taxa) exist in extant faunas that represent intermediate stages between subspecies and species. Species are reproductive communities and speciation occurs through the differentiation of relatively small and geographically isolated populations, as discussed, e.g., by Stresemann (1927-1934: 644-645 and in earlier publications; see Haffer et al. 2000:195-198). The study of geographical variation of populations in widely distributed subspecies and species permit an interpretation of the concept of biological species and the delimitation of rather broad species taxa.

Mayr's views on the biological species concept and the process of geographic speciation developed from the publications of Stresemann (1919a,b, 1920,19271934) and Bernhard Rensch (1929, 1934). Mayr himself (1999a: 23) pointed out the decisive influence of Stresemann stating "Virtually everything in Mayr's 1942 book was somewhat based on Stresemann's earlier publications." The principles of the biological species concept and the importance of geographic speciation in evolution had been established by naturalists during the late 19th century (p. 230), but it was largely due to Mayr that this information came to the attention of the geneticists. Mayr promoted the acceptance of this species concept with its emphasis on populations and on reproductive isolation. Although not originally his own it was the support he gave it and its concise formulation that led to its rapid subsequent adoption by the majority of zoologists. Stresemann had stated:

"Forms which, under natural conditions, pair successfully through generations, represent together a species regardless of the morphological differences, [...] whereas all forms that under natural conditions maintain themselves side by side without intergradation, are specifically distinct" (1920:151-152) and "forms of the rank of species have diverged from each other physiologically to such an extent that they can come together again [after the removal of a geographical barrier] without intergradation [...]. Morphological divergence is thus independent of physiological divergence"(1919b: 64, 66). "Sexual affinity and sexual aversion, respectively, under natural conditions is considered as the test for the [specific or subspecific] relationship of two forms" (1920:151; transl.).

Stresemann knew that species can be very different from or very similar to each other, i.e., the outer appearance is not a measure of species status. In the case of insular (allopatric) distribution of related forms their status as subspecies or species should be inferred from several auxiliary criteria (p. 46).

Stresemannalwayssupported theinterpretationofthe origin of speciesfromrel-atively small and geographically isolated populations (geographical or allopatric speciation), as developed during the 19th century by Moriz Wagner and John T. Gulick. In his handbook, Aves, Stresemann stated (1931: 633-634) that the rate of differentiation of an isolated population depends on "(1) the strength of the factor initiating the change, (2) the number of generations per unit of time [...], (3) the size of the population; the smaller the number of individuals, the greater

Fig. 5.2. Research traditions ("schools") of systematic ornithology during the 19th and 20th centuries. A Typological (essentialistic) microtaxonomy; A1 Linnaeus "school," A2 PallasSchlegel "school," A3 Wilson "school;" B Evolutionary microtaxonomy; B1 Baird-Coues "school," B2 Seebohm-Hartert "school." The main publishing periods of major ornithologists are indicated symbolically. Most presently active representatives of evolutionary microtaxonomy are indicated anonymously. Abbreviations: Bech.-Bechstein, Blas.-J.H. Blasius, Midd.-Middendorff, Nau.-Naumann, Stres.-Stresemann. From Haffer (1997a)

Fig. 5.2. Research traditions ("schools") of systematic ornithology during the 19th and 20th centuries. A Typological (essentialistic) microtaxonomy; A1 Linnaeus "school," A2 PallasSchlegel "school," A3 Wilson "school;" B Evolutionary microtaxonomy; B1 Baird-Coues "school," B2 Seebohm-Hartert "school." The main publishing periods of major ornithologists are indicated symbolically. Most presently active representatives of evolutionary microtaxonomy are indicated anonymously. Abbreviations: Bech.-Bechstein, Blas.-J.H. Blasius, Midd.-Middendorff, Nau.-Naumann, Stres.-Stresemann. From Haffer (1997a)

the chances for a mutation to prevail." He reemphasized (1931:644) that speciation occurs only through spatial separation of populations (either through jump dispersal or disruption of the continuous range of the parental species) and pointed out the particularly favorable conditions for speciation on island archipelagoes like the Hawaii and Galapagos Islands. Speciation occurs in isolated populations through small mutations and natural selection. During the 1920s he had studied polymorphism in birds and had emphasized repeatedly that conspicuous morphs ("mutations") have nothing to do with the origin of new species. Regarding ecological segregation in speciating populations, he concluded (1939: 360): "The correspondence of two forms may have been reduced to a correspondence of only their ecological requirements with, at the same time, divergent differentiation of their sexual activities. Two forms at that stage of the differentiation compete with each other for space and where they meet by range expansion, they abut sharply against each other without forming hybrids. [.] Examples of such situations are probably much more common than currently known" (Haffer et al. 2000). He concluded that hybridization, after the removal of a geographical barrier between incipient species invariably leads to a secondary intergradation of these populations, and not to speciation.

However, Stresemann never prepared a general treatment of species and spe-ciation, mainly because his main interests during the late 1920s had shifted to functional anatomy and physiology8 and because he may have considered B. Ren-sch's book of 1929 as having covered the subject sufficiently well.

Bernhard Rensch (1928) introduced the concept of Artenkreis (superspecies Mayr 1931). In his book, The Principle of Polytypic Species and the Problem of Speciation (1929) Rensch showed that in many groups of animals numerous geographical taxa may be combined as subspecies of polytypic species. He also discussed numerous borderline cases between subspecies and species which document that in the majority of cases, species originate from geographically isolated populations. Conspicuous phenomena of geographical variation are described in Bergmann's, Allen's, and Gloger's Rules. At that time, he interpreted these rules by a direct influence of the environment. His book was the first manifesto of "the new systematics" and Rensch the first "new systematist." In further publications he explained the geographic principle, the geographical replacement of conspecific taxa, individual and geographical variation, superspecies, and speciation in what he called Instructions for zoological-systematic Studies (1934). He also demonstrated the adaptive nature of some subspecific differences in birds. No equivalent title for Rensch's booklet of 1934 existed in the English literature until Mayr (1942e) published his volume which, in the first chapters, includes an introduction to tax-onomic procedures. On June 6,1941 Mayr wrote to Stresemann: "I am presently busy preparing mybook manuscript on Systematics and the Origin of Species. One cannot deal with this topic without noticing all the time, how much the solution or at least the clear exposition of these problems owes to our friend Rensch."

8 "My real interests have shifted [from taxonomy and zoogeography] to very different fields, in particular functional anatomy and physiology" (letter to Mayr dated 14 October 1929

In fact, Mayr (1942e) cited the publications of Rensch more frequently than those of Stresemann and wrote in retrospect: "My own work [on geographic variation and speciation] was a continuation of the work of Rensch" (Mayr 1976m: 119) and "he probably had more influence on my thinking than anyone else; I greatly admired his 1929 book" (Mayr 1980n: 416).

Until the early 1950s, systematists used the term "species" without distinction between (1) a theoretical concept, (2) a category in the taxonomic hierarchy, and (3) a particular species taxon, including Mayr, as he himself has said repeatedly.9 Modern definitions read (Mayr 1969b: 4,5,26):

(1) The theoretical species concept of general biology (the "nondimensional" biological species concept): "Species are groups of interbreeding natural populations that are reproductively isolated from other such groups."

(2) "The species category in the taxonomic hierarchy is a class the members of which are the species taxa."

(3) The species taxon is a taxonomic group that is considered to constitute a particular species, e.g., the Robin (Turdus migratorius). Under the same biological species concept authors may delimit species taxa more broadly ("lumpers") or more narrowly ("splitters") and systematists delimiting species taxa similarly, may adhere to different theoretical species concepts, i.e., no relationship exists between the species concept adopted by a particular systematist and the recognition of narrowly or more broadly delimited species taxa (Haffer 1992, p. 118, Table 2).

In Mayr's early publications on species and speciation these different meanings are usually, but not always, obvious from the context in which he used the term "species." Terminological confusion concerned mainly the theoretical species concept and the species taxon, such as Mayr's use of the non-dimensional species concept (the actual concept) and the multi-dimensional species concept (which is actually the species taxon; see below). "There is an undeniable tension between these two aspects of the word species and from 1942 until the present time, I have never ceased to struggle with this problem" (Mayr 1992i: 9). Mayr also failed to distinguish completely the species concept and the species category in taxonomy, as he used the definition for the species concept also for the category (Bock 1995b).

In his first theoretical paper Mayr (1940c) approached "Speciation phenomena in birds" as a taxonomist. Considering numerous species taxa of the Australasian bird fauna and how new species probably originated he singled out for "species in the making" strongly differentiated peripherally isolated populations with ranges detached from the main species range on an island, on a mountain or beyond some other geographical or ecological barrier. Such forms are geographical representatives of their near relatives and show the common origin still very clearly. They are

9 The word taxon "recently coined" by botanists was already mentioned by Mayr et al. (1953a: 36, 323).

differentiated at the level of subspecies or species, in some cases even as mono-typic genera. His examples are sufficient to show that geographical variation and isolation of populations lead to the formation of new species taxa (geographical or allopatric speciation). In view of his taxonomic approach the species definition he proposed was that of a polytypic species taxon:

"A species consists of a group of populations which replace each other geographically or ecologically and of which the neighboring ones intergrade or hybridize wherever they are in contact or which are potentially capable of doing so (with one or more of the populations) in those cases where contact is prevented by geographical or ecological barriers" (1940c: 256).

Hence, interpretation was required of all the factual information to decide whether allopatric populations are "potentially capable" of interbreeding, that is, whether to name them subspecies or species. The differences among representative island populations were not only quantitative and continuous but often qualitative and discrete as observed among congeneric species. For this reason he replaced the typological concept by a concept of species taxa as aggregates of geographically variable populations. In this article he did not (yet) discuss the general species concept based on reproductive isolation between populations but he did so during the following year.

The central topics of Mayr's Jesup lectures in March 1941 were the biological species concept and the origin of new species taxa. Only four months later, on 31 July 1941, he spoke at the Marine Biological Laboratory (Woods Hole, Cape Cod, Massachusetts), on his main research topic, "The origin of gaps between species" (Mayr 1941i): Evolution is a continuous process, he stated, but the units produced by evolution are discontinuous, a problem that the geneticists had left open. Two different classes of gaps between species need to be distinguished:

(a) Absolute "bridgeless" gaps between sympatric species at a particular locality. The main phenomenon is reproductive isolation between species. These have objective reality, e.g., the five similar species of thrushes of the genus Hylocichla of which up to three inhabit the same woods in northeastern North America without the slightest intergradation, and

(b) Relative (gradational) gaps between allopatric representatives. In widespread species taxa geographically differentiated continuous populations interbreed and merge into each other. Toward the periphery of the species range there are often representative forms which are geographically separated by a barrier. In such situations the taxonomist must use his judgment to infer the taxonomic status of these latter forms. Obviously, such species taxa cannot be delimited in an objective way. Geographical variation coupled with geographical separation completely blurs the borderline.

Geographically separated populations are of the greatest importance for speciation. Mutation, difference of selective factors and differences of random gene loss will, through time, produce an increasing divergence. Eventually, isolated populations will become distinct species and may come into contact with one another without interbreeding, provided reproductive (genetic) isolation is complete (al-lopatric speciation). Occasionally it happens that a geographical barrier breaks down before that is the case. The result is extensive hybridization in the zone of contact. Sympatric speciation "is of common occurrence in certain animal groups with very specific ecological requirements, but almost completely absent in all other animal groups" (Mayr 1941i: 142; see below, p. 223).

Summarizing, Mayr (1941i) distinguished clearly reproductively isolated populations of different species taxa at a particular locality and geographically representative interbreeding populations belonging to the same species taxon. From these considerations he derived in this article his definition of a polytypic species taxon (1940c). The theoretical species concept with respect to the absolute gap between sympatric species taxa was presented in his book, Systematics and the origin of species (1942e: 120) based on his Jesup lectures and his lecture at the Marine Biological Laboratory in 1941. Here he gave definitions for both the theoretical species concept ("Species are groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups") and for the polytypic species taxon (Mayr 1940c, 1941i and quoted above). "The gaps between sympatric species are absolute, otherwise they would not be good species; the gaps between allopatric species are often gradual and relative, as they should be, on the basis of the principle of geographic speciation" (1942e: 149). Criteria to infer the subspecies or species status of allopatric populations are here suggested as follows: "We must study other polytypic species of the same genus or of related genera and find out how different the subspecies can be that are connected by intermediates, and, vice versa, how similar good sympatric species can be. This scale of differences is then used as a yardstick in the doubtful situations" (1942e: 166-167).

Mayr (1942e: 148; 1943e, 1946l, 1955e, 1963b) continued to illustrate the absolute gaps between sympatric species by the five thrushes of the genus Hylocichla in northeastern North America several of which may occur at the same locality.10 They are very similar, but completely separated from one another by biological discontinuities. However, he emphasized that reproductive isolation in nature does not necessarily mean sterility. Ability to cross in captivity is not a decisive test.

Mayr introduced the term "sibling species" for morphologically very similar populations that were nevertheless reproductively isolated and discussed this phenomenon repeatedly. The striking discontinuity between local populations of animals and plants, the "nondimensional" species (Mayr 1946l: 273), had already impressed J. Ray and C. Linnaeus during the 17th and 18th centuries, respectively, and instigated the development of the biological species concept. Also some native people recognize as such the same natural units that are called species by the biologist:

"Some 25 years ago, when I was in the mountains of New Guinea I was all alone with a tribe of very primitive Papuans, who were excellent hunters. I sent them

10 Four of these spotted thrushes are currently included in the neotropical genus Catharus and only the Wood Thrush (Hylocichla mustelina) remains in this genus.

out every morning with their guns, and for every specimen that they brought back I asked, 'What do you call this one?' I recorded the scientific name in one column and the native name in another. Finally, when I had everything in the area, and when I compared the list of scientific names and the list of native names, there were 137 native names for 138 species. There were just two little greenish bush warblers for which they had only a single name. At the time, I took this for granted because as a naturalist I always believed in species, but whenever I read statements by armchair biologists who deny the existence of species, I always marvel at the remarkable coincidence that the scientist and the native in New Guinea should by pure accident have an imagination that is so closely similar that they assign the mountain birds of New Guinea to the same number of species" (Mayr 1956g: 5; see also here p. 58, Mayr 1943e, 1949m, 1963b: 17, and Diamond 1966).

In later publications Mayr usually quoted the definition of the theoretical biological species concept (the "nondimensional species"), sometimes without the qualifying "actually or potentially" in front of "interbreeding," because it is irrelevant for species status whether the isolating mechanisms are challenged at a given moment (e.g., Mayr 1949j, 1953b, 1969b, 1982d: 273).

Mayr (1949f: 290) considered an emended species definition: In case speciation occurs without a complete separation of the populations an extended definition may become advisable: "Species are groups of actually or potentially interbreeding natural populations that are either completely reproductively isolated from other such groups or whose genetic differentiation (owing to mutation, selection, etc.) outweighs an actual or potential gene interchange with other such groups." He added "But there are also some serious objections to such an emendation." After ecological factors had been emphasized by various workers Mayr (1951l: 92) defined the species as "an aggregate of interbreeding natural populations which are not only reproductively isolated from other such aggregates but also ecologically specialized sufficiently so as not to compete with other such species" or more formally: "A species is a reproductive community of populations (reproductively isolated from others) that occupies a specific niche in nature" (1982d: 273). The reason why he added the qualifying clause "that occupies a specific niche in nature" was that "it seemed to me that no population has completed the process of speciation until it is able to coexist with its nearest relatives. [...] Time will show whether this additional qualification is useful or confusing" (1987e, p. 214).

If the ecological factor would be raised to a criterion for species status, such a definition would reduce to subspecies status most closely related paraspecies which are reproductively isolated but exclude each other because of ecological competition. For this reason such a definition (with the above qualifying clause) never caught on and Mayr (1992a: 222) himself returned to this simple wording: "A species is an interbreeding community of populations that is reproductively isolated from other such communities." Local representative populations of species have particular niches, but not a species as a whole.

In Mayr's early publications of the 1940s and 1950s, there is no terminological distinction between the species concept and the species taxon. In a lecture on "The species as a systematic and as a biological problem" Mayr (1956g: 7) introduced for the polytypic species a new "multidimensional species concept" (see also Mayr 1957f: 16,1963b: 19). When he had clarified for himself the distinction between the theoretical species concept and the species taxon during the early 1960s, "it became evident that the polytypic species is merely a special kind of species taxon but does not require any change in the concept of the biological species category" (Mayr 1982d: 290). Therefore in his writings of the late 1960s and following decades he no longer mentioned a "multidimensional species concept" but stated: "The species concept is meaningful only in the nondimensional situation: multidimensional considerations are important in the delimitation of species taxa but not in the development of the conceptual yardstick" (1982d: 272; see also Hey (2006:448) for a summary of Mayr's changing categorization of species concepts).

Beurton (2002) presented a detailed historical review of Mayr's struggle with the biological species concept during more than 50 years. It would have been easier for the reader to follow Beurton's arguments if he had clarified from the start the early terminological confusion regarding (a) the biological species concept per se and (b) the polytypic species taxon and if he had applied Mayr's later clarification to his early writings (rather than presenting the early confusion again in detail without applying Mayr's later clarification). Mayr (1940c) discussed species taxa and that is what his definition referred to (see above). In his Jesup lectures he talked about the general "species problem" referring both to the absolute gaps between sympatric species and to the relative gaps between allopatric taxa, as is obvious from Mayr (1941i), an article Beurton (l.c.) did not consult. Mayr (2002a: 100) himself commented: "It is a basic weakness of Beurton's account that the confusion between species concept and species taxon is not clarified. [...] Those authors who fail to make the distinction, provide a confused and misleading analysis." Mayr (1942e) then presented the distinction between the biological species concept (absolute gaps) and the polytypic species taxon (relative gaps), as in 1941.

The theoretical concept and definition of biological species (Mayr 1942e and later) found entrance into all textbooks of biology. Bock (1986,1992a, 1994,1995b, 2004b) emphasized that genetic isolation was meant when Dobzhansky (1937) and Mayr (1942e) spoke of the "common gene pool" and the "harmonious genotype of a species." Mayr (1968i: 164) stated: "Possession of a shared genetic program is the common tie uniting individuals derived from the gene pool of a given species." Therefore Bock (l.c.) emended the definition of biological species to read: "A species is a group of actually or potentially interbreeding populations of organisms which are genetically isolated in nature from other such groups." Bock's emendation appears useful also in view of the discovery in recent years that several geographically representative taxa, especially of insects, hybridize freely along the contact zone for lack of premating isolating mechanisms, but such hybrids are infertile due to fully developed postmating isolating mechanisms. In addition, Bock (l.c.) made a distinction between the sets of isolating mechanisms for genetic isolation and reproductive isolation which Mayr failed to do. Some bird species which meet along "zones of overlap and hybridization" (Short 1969) may also represent taxa which are genetically isolated but not fully isolated repro-ductively. These biospecies would be considered conspecific taxa under Paterson's

(1985) "recognition concept" of species. Evolutionists need to distinguish between genetic isolation, reproductive isolation, and ecological isolation of species (Bock 1979,1986,2004d). Genetic isolation mustbe complete before the neospecies establish secondary contact in order not to hybridize, but reproductive and ecological isolation may be perfected in sympatry through natural selection and mutual selective demands.

The "horizontal" biological species concept refers to genetically separated groups of populations which live during a particular time plane like the Present or any time plane of the geological past (Fig. 5.3). Under this concept, species have, strictly speaking, no origin, age or duration. They represent horizontal "cross sections" ofvertical phyletic species lineages in the time dimension (Bock 1979,1986, 1992a; Szalay and Bock 1991). A phyletic lineage is the continuum of a species in time and documents its history; it does not participate in the development of species (populations do). The "phyletic lineage" and the "species" should be kept separate conceptually.

Mayr's (1931b, 1942e) consistent application of the superspecies concept in his systematic work was of general significance because it permitted the combination of several closely related geographical representatives under one superspe-cific name without reducing these allo- or paraspecies to subspecies status. Such 'superlumping' had been advocated by several workers (e.g., Kleinschmidt and

Fig. 5.3. Several imaginary phyletic lineages illustrate "species" limits under the cladistic concept (clad.) and the paleontological concept (pal.). Schematic representation. Groups of populations representing the various lineages at particular time levels (t1-t4) are different biological species (oval circles). Vertical scale-geological time; horizontal scale-morphological and other biological changes. A-L represent paleontological "species," except C-F, which together are one paleontological "species" but represent 2 cladistic "species." The current time level is t4

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