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Home , Form (botany), Form (zoology), Race (biology), Subspecies, Subvariety

, SEMISPECIES, SUPERSPECIES

James Mallet University College London

I. A Brief History of Subspecific as separate , and ‘‘lumpers’’ who ignored II. The Subspecies Today geographic variation, and united local variants into a III. Further Reading single species. The problem was compounded by early systematists’ belief that species had an Aristotelian ‘‘essence,’’ each fundamentally different from similar essences underlying other species. To Linnaeus’ fol- DISTINCT POPULATIONS THAT REPLACE EACH lowers, it seemed important to decide which level of OTHER GEOGRAPHICALLY were recognized either variation was fundamental. The terms ‘‘’’ and as full species or as lower-level ‘‘varieties’’ or ‘‘forms’’ ‘‘species’’ both result from Aristotelian philosophy, and under the original . In , a although Linnaeus is usually credited with establishing practical resolution of this ambiguity took place the species as the basal taxonomic unit, he confused largely between about 1880 and 1920, with the matters, after recognizing that some plant species were recognition of a single additional , of origin, by suggesting that genera were a more the geographic subspecies (while in , many important taxonomic level (i.e., a separately created infraspecific ranks remain valid). Since the 1980s, the kind) than species. fashion has changed once more. Some systematists are Once evolution was accepted, it became clear that again recognizing geographical replacement forms as variation at all levels in the taxonomic hierarchy was full species, even when they blend together at their due to more or less similar causes; the only difference boundaries. between variation above the level of genus or species and below was one of degree. Darwin realized that species could evolve from intraspecific varieties. Darwin used the term ‘‘species’’ in a new and nonessentialist I. A BRIEF HISTORY OF SUBSPECIFIC sense: ‘‘... the complete absence, in a well-investigated TAXONOMY region, of varieties linking together two closely-allied forms, is probably the most important of all the crite- A. Variation Below the Level of Species rions of their specific distinctness ... Geographical dis- tribution is often brought into play unconsciously and Since the invention of binominal nomenclature by sometimes consciously; so that forms living in two Linnaeus, there has been a conflict between ‘‘splitters’’ widely separated areas, in which most of the other in- who named more or less well-defined local populations habitants are specifically distinct, are themselves usually

Encyclopedia of Biodiversity Copyright & 2007 Elsevier Inc. All rights of reproduction in any reserved. 1 2 ______SUBSPECIES, SEMISPECIES, SUPERSPECIES______looked at as distinct; but in truth this affords no aid in North America were Elliott Coues, who published a distinguishing geographical races from so-called good or catalog of American birds in 1872 incorporating an true species’’ (Darwin, 1874). Darwin showed convinc- early version of this trinominal nomenclature, in ingly that there was no essential difference between which subspecies were prefixed by ‘‘var.,’’ and Robert species and ‘‘varieties’’; species were simply varieties Ridgway, who finally dropped the ‘‘var.’’ in his own which had diverged more, and which could coexist 1881 summary of North American bird nomenclature. without intermediates being common. However, with The American Ornithologists’ Union soon adopted his term ‘‘varieties’’ Darwin did not clearly distinguish this policy, and the idea then spread to Europe, par- between polymorphic variants within populations ticularly England where Walter Rothschild began and the identifiable geographic populations normally amassing his vast collection of birds and butterflies, today considered as geographic ‘‘races’’ or ‘‘subspecies.’’ andhadhiredexcellentandproductivestaff,the To Darwin the distinction was unimportant, because ornithologist Ernst Hartert and the entomologist polymorphic variants, clinal variation, geographic races Karl Jordan, to curate and describe the new material. or subspecies, and ‘‘good’’ species formed a continuum. Jordan was particularly important in spreading the Darwin demonstrated that this continuum was excellent idea of trinominal nomenclature to entomologists, evidence for an evolutionary origin of the taxa we call and in promoting the abandonment of other subspe- species. cific nomenclature. He was regarded by the Rothschi- lds as the ‘‘clever’’ member of the staff, and published enormous systematic treatises as well as papers on the B. The Trinominal Revolution in Zoology theory of systematics, justifying trinominal nomen- clature and the recognition of the ‘‘subspecies’’ as a Many systematists wished to preserve the purity of the valid, identifiable in its own right. Both Jordan simple genus–species binominal nomenclature, but by and Hartert were Germans who contributed to and read the 1850s, there were enormous stresses. It began to German as well as English journals, and in Germany a be realized that many clearly identifiable geographic similar revolution was taking place. Thus, these sys- replacement forms were an important intermediate tematic ideas were able to spread to the rest of Europe stage between insignificant local variants and ‘‘good’’ in a time when science was often highly parochial. The species. Some lumped these replacement forms as standard trinominal nomenclature for subspecies, and varieties within species, while others continued des- the abandonment of other named ranks, such as semi- cribing these replacement forms as separate species: species and superspecies, soon became established in practices varied widely, leading to considerable con- the International Code of Zoological Nomenclature, fusion. Although some Europeans had long advocated and has remained there ever since. naming geographic forms as subspecies, the accumu- Meanwhile, botany, Linnaeus’ major expertise, lation of major North American museum collections remained much less prescriptive. Many infraspecific during the great push of colonization and railway ranks are still considered valid taxa under the Inter- construction westwards was probably the most im- national Code of . For in- portant catalyst of a revolutionary new systematics. stance, Saxifraga aizoon var. aizoon subvar. brevifolia In this new approach, nomenclature consisted of a f. multicaulis subf. surculosa is a valid scientific name trinominal: genus–species–subspecies, which is still in botany, with names for , , form, the dominant taxonomic practice today. The maxim and subform, as well as genus and species ranks. was: ‘‘ [at the boundary between two Cultivated strains, hybrids, subspecies, are also valid geographic replacement forms] is the touchstone of in botany, and subspecies do not necessarily refer trinominalism.’’ Examples from commonly observed specifically to geographic populations, as in zoology. birds which intergrade are, in North America, the The remainder of this article is concerned largely eastern rufous-sided towhee (Pipilo erythrophthalmus with zoological terminology. It is important to realize, erythrophthalmus) replaced in the west by the spotted however, that both the botanical and the zoological towhee (Pipilo erythrophthalmus maculatus), and in codes avoid controversy by not specifying how to Europe the carrion crow (Corvus corone corone) found decide whether a particular group of specimens is a in the south and west, replaced by the hooded crow species or infraspecific taxon. The goal of these codes (Corvus corone cornix) in the north and east. Among is to merely regulate nomenclature once a decision of the ornithologists responsible for this revolution in rank has been reached. ______SUBSPECIES, SEMISPECIES, SUPERSPECIES______3

C. Theories of Divergence: Superspecies, Rassenkreise were again considered to be equivalent to species, composed of races or subspecies. However, Semispecies, and Subspecies now there was an additional layer in the taxonomy, of It is hard to imagine the diversity of ideas by which the groups of Rassenkreise that replaced one another systematists of 100 years ago explained geographic geographically, the Artenkreise. Thus an Artenkreis could variation. At that time, evolution by natural selection consist of multiple Rassenkreise. Rensch and many was far from generally accepted, in fact many believed others believed that the subspecies was an incipient that it had been disproved. One of the most influential species, of which the geographic replacement species, ornithologists of the time was Otto Kleinschmidt, who Artenkreise were a further development, until finally believed that all species suddenly came into being long divergence was sufficient to allow complete geographic ago, and since then had remained completely separate. overlap, whereupon new Rassenkreise could again be Replacement forms or subspecies developed via nat- formed. ural selection from the main species but, in Kleinsch- These terms did not catch on, and most scientists midt’s view, subspecies could never evolve into new came to the conclusion that the Rassenkreise were species as the Darwinians supposed. To distinguish his equivalent to the species taxa used by Linnaeus and new species concept from the older one in which Darwin. Probably a major reason that we do not use geographical replacements might be named as separate these multiple taxonomic terms is due to the prolific species, Kleinschmidt called his theory of variation the work published in English by another German, Ernst Formenkreis (ring of forms) theory. The Formenkreis Mayr. Mayr had worked for Walter Rothschild, and theory fitted neatly with, and indeed promoted the knew Hartert. After Walter Rothschild was black- new practices of naming subspecies and trinominal mailed by a lover, his enormous bird collection of nomenclature. 280,000 skins was sold in 1932 to the American In those times many somewhat peculiar explanations Museum of Natural History, where Mayr happened to competed to explain geographic variation and speciat- have been hired as a curator. Mayr’s experience of ion, including Kleinschmidt’s ‘‘nonspeciation’’ theory, ornithology, contact with the European literature, and J. P. Lotsy’s hybridization theory, mutationism, inherit- burgeoning friendship with the geneticist Theodosius ance of acquired characters, as well as natural selection. Dobzhansky (who convinced him of the lack of evid- In Britain, Jordan and Rothschild argued eloquently and ence for inheritance of acquired characters), lent a influentially against any new terminology (including unique opportunity to influence the course of system- Formenkreis) that had theoretical implications, and pro- atics and evolutionary biology. Mayr did not waste this posed incorporating as little evolutionary theory into opportunity. Mayr used ideas underlying Rensch’s taxonomy as possible, in view of the lack of agreement terms, but renamed them in English. The Rassenkreis among scientists at the time. Rothschild and Jordan became simply the species or ‘‘polytypic’’ species, (e.g., 1895, 1903), supported by Hartert, agreed both with its geographic races being subspecies, while the with the nomenclatural practice of naming subspecies, Artenkreis became the ‘‘superspecies,’’ and its compo- and also that subspecies were valid real taxa that could nent parts ‘‘semispecies,’’ that is, not very divergent evolve into full species. They argued that the Linnaean geographic replacement species, which may hybridize term ‘‘species’’ should be retained for the whole group occasionally but not frequently where they overlap. of races, and that the geographic races were not true Mayr successfully blended the local species concept of species, they were simply ‘‘subspecies’’ or incipient Poulton and Dobzhansky based on interbreeding with species. the geographic Rassenkreis idea of species, incorpora- Others felt that the term species was too emotive to ting Jordan and Rothschild’s ideas about subspecies. be used in the new, multiple-subspecies sense. Some He renamed this combination of ideas ‘‘the biological scientists continued following the Formenkreis doctrine, species concept,’’ a term which has since remained and had begun to name quite distinct taxa, which did strongly associated with Mayr’s name. His many influ- not intergrade at their boundaries, as subspecies. This ential articles and books promoted a new program situation led in the 1920s and 1930s to the neo- of species study, a science of the species that is still Darwinian ornithologist Bernhard Rensch scrapping the with us today. Central to Mayr’s system was the belief term Formenkreis because of its theoretical limitations, that discrete taxa such as species or subspecies would and instead substituting two new terms, Rassenkreis normally diverge in ‘‘allopatry,’’ that is, in complete (circle of races) and Artenkreis (circle of species). geographic isolation. 4 ______SUBSPECIES, SEMISPECIES, SUPERSPECIES______

II. THE SUBSPECIES TODAY in separate species in spite of the fact they have not truly ‘‘speciated.’’ The two taxa differ strongly in call, morpho- A. Modern Views of Subspecies and logy, skin thickness, the sizes of water bodies used for breeding, and egg size, as well as in mitochondrial Semispecies deoxyribonucleic acid (DNA) and protein sequence. The The views of Darwin, Wallace, Rensch, and Mayr that levels of differentiation suggest that the Bombina taxa geographic replacement forms, subspecies and semi- have evolved separately for many millions of years. This species, are in fact incipient species, has few critics situation of multiple character changes has now been today. Most geographic replacement species (i.e., shown to be true across many examples of subspecies as ‘‘semispecies,’’ which intergrade only rarely when they well as species separated by hybrid zones. Gene flow can meet) must indeed have evolved from previously be shown to be almost completely blocked by hybrid interbreeding subspecies. Modern genetic data have zones such as these, even if hybridization is frequent done nothing to cast doubt on this idea. Meanwhile, (Barton and Hewitt, 1985). Thus, while some named superspecies became a term reserved for groups of subspecies undoubtedly merited Wilson and Brown’s semispecies that intergraded little at their boundaries. scorn, genetic evidence shows that there are plenty of However, under the trinominal approach, taxono- local replacement forms which hybridize at their bound- mists were now required to describe subspecies, which aries but which do form ‘‘real’’ identifiable taxa that has never been seen as a particularly noble activity in are not reproductively isolated, and are therefore valid comparison to the description of species, especially subspecies under the Wilson and Brown criteria. recently. A strong attack on the zoological subspecies was mounted by Wilson and Brown (1953). Both were systematists working on ants, a group particularly B. Subspecies, Species, and Conservation riddled with poorly conceived trinominals and other named varieties at the time. Wilson and Brown argued This opposition among modern taxonomists to sub- that subspecies rarely, if ever, could be justified on the species taxa can be traced as one catalyst of the recent basis of multiple characters, and that therefore they ‘‘diagnostic’’ version of the phylogenetic species con- were not ‘‘real taxa.’’ The only ‘‘real taxa’’ were species, cept. The adherents of this view of species, led by which in a sense were self-defining because inter- the ornithologist Cracraft (1989), proposed a radical breeding prevented divergent genes from flowing from species concept so that even a single fixed character one species to another. Subspecies that interbred at difference may define a geographic form as a separate their boundaries, on the other hand, were not so species. Multiple character justification is not con- endowed, so that genes and morphological characters sidered necessary, even at the species level. The prac- could flow between them. Good examples of subspe- tical result of this new concept is that many local forms, cies were put forward which undoubtedly would be having been downgraded to subspecies in polytypic hard to justify on multiple character grounds. This species, are again being recognized as species, leading single paper was enormously influential on systematics to taxonomic inflation. In birds and butterflies, which in the United States, and generations of insect system- often have many morphologically or genetically distinct atists trained at Harvard and Cornell, where Wilson subspecies, this could easily result in a (2–10)-fold and Brown worked, and their own many intellectual increase in the number of species. descendants, and their students’ students in turn, have It is probable that the revision of geographic forms eschewed the practice of naming subspecies. upward to the level of species is being driven not only However, recent work shows that many subspecies by theoretical considerations, but also by existing separated by hybrid zones do in fact differ at multiple legislation, which proposes that ‘‘endangered species’’ morphological, behavioral, and genetic characters (Bar- are the valuable units to be conserved. If a reserve ton and Hewitt, 1985). For instance, the toad Bombina contains a taxon recognized as a species rather than bombina meets its relative Bombina variegata across a just as a local , it may be seen as more valuable for broad front in Europe. The two forms hybridize freely conservation purposes. The potential consequences for in the contact zone—although the hybrids can be biodiversity and conservation of the continued insta- shown to suffer some inviability—and so should really bility of the term ‘‘species’’ are detailed in the article be classified as members of the same species under Species, Concepts Of. Today’s conservationists are red- polytypic or biological species concepts. However, it has ucing emphasis on species conservation, and are beco- always seemed natural to place such well-defined forms ming increasingly aware of biodiversity at all the levels ______SUBSPECIES, SEMISPECIES, SUPERSPECIES______5 of the hierarchy of , including well-marked subspe- Cracraft, J. (1989). Speciation and its ontology: The empirical con- cies. Thus, the legislative need for differentiating local sequences of alternative species concepts for understanding pat- races as species may ultimately become less important and processes of differentiation. In Speciation and its Consequences (D. Otte and J. A. Endler, Eds.), pp. 28–59. Sinauer provided that future legislation falls more into line with Associates, Sunderland, MA. the prevailing biological thought. Darwin, C. (1874). The Descent of Man and Selection in Relation to Sex, 2nd ed. John Murray, London. Johnson, K. R. (2003). Karl Jordan: A life in systematics. PhD dis- III. FURTHER READING sertation, Oregon State University, Corvallis. Mallet, J. (2004a). Poulton, Wallace and Jordan: How discoveries in Papilio butterflies initiated a new species concept 100 years ago. Much of the historical overview in this article is Syst. Biodiv. 1, 441–452. covered by the excellent reviews of Stresemann (1936, Mallet, J. (2004b). Species problem solved 100 years ago. Nature 1975), Mayr (1982), Rothschild (1983), as well as by 430, 503. other sources already cited. A recent biography of Karl Mayr, E. (1982). The Growth of Biological Thought. Diversity, Evolut- Jordan (Johnson, 2003) and work on the connections ion, and Inheritance. Belknap, Cambridge, MA. Rothschild, M. (1983). Dear Lord Rothschild. Birds, Butterflies and between the species concepts of A. R. Wallace, E. B. History. Hutchinson, London. Poulton, Karl Jordan, and (Mallet, 2004a, Rothschild, W., and Jordan, K. (1895). A revision of the Papilios of b) may also be of interest. the eastern hemisphere, exclusive of Africa. Novitat. Zool. 2, 167– 463. Rothschild, W., and Jordan, K. (1903). A revision of the lepidop- See Also the Following Articles terous Sphingidae. Novitat. Zool. 9(Suppl.), I–cxxv, 1–813. Stresemann, E. (1936). The Formenkreis theory. Auk 53, 150–158. SPECIATION, PROCESS OF  SPECIES, CONCEPTS OF Stresemann, E. (1975). Ornithology. From Aristotle to the Present. Harvard University Press, Cambridge, MA. Reprinted edition of Stresemann’s 1951 ‘‘Entwicklung der Ornithologie.’’ Translated Bibliography by H. J. Epstein and C. Epstein; G. W. Cottrell Ed.; foreword and epilogue by E. Mayr. Barton, N. H., and Hewitt, G. M. (1985). Analysis of hybrid zones. Wilson, E. O., and Brown, W. L. (1953). The subspecies concept and Annu. Rev. Ecol. Syst. 16, 113–148. its taxonomic application. Syst. Zool. 2, 97–111.