Units in Biogeography

648 SYSTEMATIC BIOLOGY VOL. 51 Syst. Biol. 51(4):648 652, 2002 DOI: 10.1080/10635150290102320 Units in Biogeography BERNHARD HAUSDORF Zoologisches Institut und Zoologisches Museum der Universität Hamburg, Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany; E-mail: hausdorf @zoologie.uni-hamburg.de In the past two decades, vicariance biogeography has become a major subdiscipline of biogeography. The subject of vicariance biogeography is the study of area relationships (e.g., Nelson and Platnick, 1981; Morrone and Crisci, 1995; Humphries and Parenti, 1999). An important step in the investigation of area relationships is the transformation of a taxon cladogram into an area cladogram. Different delimitations of unit areas can result in different outcomes concerning area relationships (Henderson, 1991). Therefore, area delimitation is a crucial issue. Most authors agree that areas of endemism should be treated as units. However, the de nition and the delimitation of areas of endemism are controversial. Whereas most authors considered an extensive sympatry of at least two species as a fundamental requirement (Nelson and Platnick, 1981; Platnick, 1991; Morrone, 1994; Linder, 2001), Harold and Mooi (1994) did not require sympatry but rather used congruence among area cladograms as a recognition criterion. AREAS OF ENDEMISM: DEFINITION Although there is general agreement that areas of endemism are the units in biogeography, hardly any clear de nition of that term can be found in the literature (Henderson, 1991; but see Harold and Mooi, 1994; Linder, 2001). Before recognition criteria and the delimitation of areas of endemism can be discussed, the term area of endemism should be de ned clearly. A de nition of areas of endemism can be derived from the vicariance model, because the term has been used mainly within the vicariance biogeography framework. According to the vicariance model, an ancestral biota was fragmented by the appearance of a barrier. The barrier limited or obviated the gene ow between populations separated by the barrier. This vicariance event resulted in allopatric speciation of many of the species formerly constituting the ancestral biota. In this way, two new biotas emerged, which are separated by the barrier. The causal link between the appearance of the barrier and the formation of new biotas is essential in the vicariance model. By repetitions of this process, small areas with distinct biotas, that is, with many species restricted to individual areas, emerge. These are areas of endemism. Thus, areas of endemism can be de ned as areas delimited by barriers, the appearance of which entails the formation of species restricted by these barriers. Usually, vicarance cannot be observed directly because this process generally takes geologic time periods. Therefore, it is important to derive predictions about observable patterns from the model. One prediction that can be derived from the vicariance model concerns the spatial similarities of distribution areas originating by vicariance. After a vicariance event, there should be a group of species restricted to one side of a barrier and a group restricted to the other side of the barrier. On average, the range of a species will be more similar to the ranges of other species living on the same side of the barrier, that is, in the same area of endemism, than to the ranges of species living on the other side of the barrier. Thus, two groups of taxa, each with similar ranges, originate from a vicariance event. Such groups of taxa have been called faunal or oristic elements. The ranges of two species living on the same side of the barrier may not necessarily overlap, especially when these species differ ecologically and thus are restricted to different portions within the area of endemism. The de nition of area of endemism in the sense of Nelson and Platnick (1981:468), Platnick (1991), Morrone (1994), and Linder (2001) is based on spatial similarities of distribution areas, that is, relatively extensive sympatry of at least two species (Platnick, 1991).

2002 POINTS OF VIEW 649 FIGURE 1. Hypothetical distributions for the discussion of the de nition of area of endemism. (a) Two groups of two species each with relatively extensive sympatry describe two areas of endemism. (b) The distribution area of one of three groups of two species each with relatively extensive sympatry overlaps the distribution area of the other groups. Thus, these three groups of species cannot describe three areas of endemism. Linder (2001:893) presented an explicite definition of area of endemism according to which areas of endemism are areas delimited by the congruent distribution of at least two species of restricted range. I call this the standard de nition of area of endemism. The hypothetical example depicted in Figure 1a demonstrates the principle. The ranges of four species are shown. The distributions of species 1 and 2, and 3 and 4, respectively, are more or less coincident. Thus, they de- ne two areas of endemism. However, the example depicted in Figure 1b shows that the standard de nition is insuf cient to decide which areas should be considered areas of endemism. There are three groups of two species with largely congruent ranges. The ranges of species 5 and 6 overlap with those of all other species. According to the de nition above, there would be three partly overlapping areas of endemism. This interpretation is not compatible with the vicariance model, which states that areas of endemism are nonoverlapping. A second pattern that can be predicted based on the vicariance model concerns the phylogenetic relationships within the taxa inhabiting the areas of endemism. Because of the causal link between the appearance of barriers and the origin of new species, area cladograms based on taxonomic cladograms of individual taxa should be congruent and should re ect the unique history of the areas (with the exception of some species not responding to some of the vicariance events; see Platnick and Nelson, 1978; Nelson and Platnick, 1981). This pattern is the basis of the de nition given by Harold and Mooi (1994:262): an area of endemism is a geographic region comprising the distribution of two or more taxa that exhibit a phylogenetic and distributional congruence and having their respective relatives occurring in other such-de ned regions. Contrary to the suggestions of Nelson and Platnick (1981), Platnick (1991), Morrone (1994), and Linder (2001), this de nition does not require that all species occur in a large portion of the area of endemism; the ranges of some species may not overlap within an area of endemism (e.g., because they are restricted to different habitats). Whereas Harold and Mooi s (1994) de nition and my de nition of areas of endemism do not necessarily require the relative extensive sympatry demanded by Platnick (1991), the requirement that the areas of endemism be delimited by barriers, the appearance of which entailed the formation of species restricted by the barriers, is more stringent than Platnick s (1991) requirement of congruent distributional limits of two or more species. That areas are delimited by barriers, the appearance of which entailed the formation of species restricted by the barriers, is a hypothesis that must be tested. Harold and Mooi (1994) proposed to test the prediction that the area cladograms of different taxa are congruent. The problem with this approach is that the units of the biogeographic analysis must be de ned before the taxon cladograms can be converted into area cladograms. The proposed test can be used to determine whether the prede ned unit areas are areas of endemism. Obviously, the units must be de- ned before areas of endemism can be recognized. Thus, areas of endemism as de ned here or by Harold and Mooi (1994) cannot be the units of biogeographic analyses. Areas of endemism are not used as basic units in the procedure proposed by Harold and Mooi (1994). In their procedure, areas of occurrence are the basic units. Axelius (1991) showed that the use of distribution areas as basic units for the construction of area cladograms can result in paradoxical conclusions

650 SYSTEMATIC BIOLOGY VOL. 51 (e.g., an area is more related to a different area than to some part of itself) when distribution areas overlap. Harold and Mooi (1994) avoided this problem by combining all (partly) overlapping areas. Thus, they were unable to recognize areas of endemism when dispersal had occurred. AREAS OF ENDEMISM: DELIMITATION Although the standard de nition of area of endemism is based on distribution patterns of species (more or less congruent distributional boundaries of at least two species), geomorphological or palaeogeographical units (e.g., islands, continents, mountain ranges) are considered areas of endemism in most empirical studies without an explicit analysis of distribution patterns. This assumption is probably made because of problems in delimiting areas of endemism. The delimitation of areas of endemism is not problematic when species originate by vicariance and there is no dispersal. Under these conditions, there are groups of species having separate ranges (as in Fig. 1a). However, the delimitation of areas of endemism becomes problematic when dispersal occurs. The occurrence of dispersal has never been doubted by vicariance biogeographers (Platnick and Nelson, 1978). Without dispersal, there would be continuity within and discontinuity between areas of endemism. This condition has been cited as a recognition criterion of biotic provinces (Peters, 1955). However, changes in species composition are gradual shifts over large zones rather than sharp breaks between neighboring homogeneous areas (Peters, 1955; Kaiser et al., 1972). Consider the distribution areas of the 10 species depicted in Figure 2. Assume that the situation is the result of a vicariance event separating eastern and western species and subsequent dispersal. How large were the areas of endemism? Were they as large as the distribution areas of species 3 and 9 or 2 and 7, or were they even smaller than the distribution areas of species 5 and 6? The biogeographical data alone are insuf cient for delimiting the areas of endemism. Dispersal decouples the history of species from the history of areas. The best-known real example of the general problem depicted in Figure 2 is the delimitation of the Oriental and the Australian regions. Although many authors have addressed this subject, it is not possible FIGURE 2. Hypothetical distributions of 10 species demonstrating the dif culty involved in delimiting areas of endemism based on biogeographical data alone when dispersal has occurred. to determine the limits of these two regions on the basis of biogeographical data (Mayr, 1944; Holloway and Jardine, 1968; Simpson, 1977; Vane-Wright, 1991). Mayr (1944) proposed drawing the borderline between the two zoogeographic regions in the area where the faunal elements of the two regions intermingle such that the faunal element of one region prevails on one side of the borderline and the faunal element of the other region prevails on the other side. However, Mayr admitted that this line would be an arbitrary separation of a continuous series of values at the halfway point between the extremes and that the line could be different for different taxa. If it is not possible to establish the border between two regions separated by several hundred kilometers of ocean on the basis of biogeographical data, it will hardly be possible to delimit areas of endemism separated only temporarily by climatic barriers on a continent, for example. In situations such as that in Figure 2, the operational methods proposed for identifying and delimiting areas of endemism by Morrone (1994) and Linder (2001; see also Linder and Mann, 1998) cannot be used to nd the limits of areas of endemism. Moreover, the reasons for using parsimony algorithms designed to reconstruct a dichotomous split sequence to delimit areas of endemism are unclear, because the distribution of taxa in grid quadrats is not the result of such a split sequence between the quadrats. Existing methods also do not test whether a distribution pattern is nonrandom. Hovenkamp (1997) tried to evade the problem of delimiting areas of endemism by focusing on supposed vicariance events instead of areas of endemism. However, in

2002 POINTS OF VIEW 651 situations such as that shown in Figure 2, this approach is no solution because the position of the barrier causing the vicariance event cannot be located because of subsequent dispersal (at least not with biogeographical data). BIOTIC ELEMENTS AS BIOGEOGRAPHIC UNITS Reconsider the situation depicted in Figure 2. It is not possible to determine by an analysis of distribution areas which species dispersed how far or to delimit the areas of endemism with the available information. However, by comparing the distribution areas of the various species, two groups of species with similar ranges can easily be recognized. Such groups have been called faunal or oristic elements or groups (e.g., Rebel, 1931; de Lattin, 1957; Mayr, 1965; Holloway and Jardine, 1968; Udvardy, 1969; Jardine, 1972; Birks, 1987; Frey, 1992; Dennis et al., 1998). I de ne biotic element as a group of taxa whose ranges are signi cantly more similar to each other than to those of taxa of other such groups. A computational method for the analysis of biotic elements was described by Hausdorf and Hennig (unpubl.). The existence of biotic elements is predicted by the vicariance model (see above), and in contrast to areas of endemism, biotic elements can be determined by using distribution data alone. Hence, biotic elements are suitable for use as biogeographic units. Areas of endemism are suitable for use as biogeographic units only when species originate by vicariance and there is no dispersal. However, these presuppositions are not tested in vicariance biogeographic studies. Vicariance biogeography regards dispersal as a secondary process that creates noise in the data. However, biotic elements do not presuppose a speci c speciation mode and are suitable units, even when extensive range expansions or range shifts have occurred, such as in response to climatic changes (Frey, 1992). The concept of biotic elements tries to summarize all generalities of the geographical distributions of organisms. The delimitation of biotic elements is only the rst step in a biogeographic analysis. Whether (parts of) biotic elements are historical units and how far they are in uenced by ecological factors must be investigated by further analyses. If biotas evolve according to the vicariance model without dispersal, each biota would consist of a single biotic element and the biotic elements would not overlap. Just as sympatry of sister groups, sympatry of biotic elements is evidence for dispersal. If a biota consists of a single biotic element, there is no evidence for vicariance events within that biota. Only when different biotic elements can be distinguished is it meaningful to investigate how they have been in uenced by vicariance and dispersal. Biotic elements are not necessarily generated by vicariance events. Biotic elements can also originate when an area is colonized from different source areas across preexisting barriers by chance dispersal and when the populations in the area under consideration evolve into new species. Another possible scenario is that species that originated in separate areas colonize the same larger region, either after the removal of barriers or by chance dispersal. In such cases, biotic elements are geographical but not historical units. Whether biotic elements (or parts of them) are historical units can be tested, such as by a comparison of the cladograms of the respective groups. The taxon cladograms can be converted into element cladograms by replacing the taxon names with the respective biotic element (analogous to the area cladogram approach). The element cladograms of those groups that form historical units should match. The parts of the biotic elements that form historical units can be termed vicariance elements. Some problems with the area cladogram approach can be solved by using biotic elements as units with the element cladogram approach. One important issue concerns groups with different histories in the same area. For example, the terrestrial mollusc fauna of northeastern Africa is dominated by Palearctic groups, whereas the freshwater mollusc fauna is dominated by Ethiopian groups that colonized northeastern Africa through the Nile (Pallary, 1909). Area cladograms based on terrestrial snails imply that northeastern Africa is related to other Mediterranean countries, whereas area cladograms based on freshwater molluscs indicate that northeastern Africa is related to parts of subsaharan Africa. A consensus tree of such cladograms would be unresolved. The area cladogram approach does not reveal

652 SYSTEMATIC BIOLOGY VOL. 51 information on the history of northeastern Africa because the fauna is composed of different elements with different histories that cannot be shown in a single area cladogram. An analysis of the biotic elements is a more appropriate rst step toward understanding the genesis of composite biotas. REFERENCES AXELIUS, B. 1991. Areas of distribution and areas of endemism. Cladistics 7:197 199. BIRKS, H. J. B. 1987. Recent methodological developments in quantitative descriptive biogeography. Ann. Zool. Fenn. 24:165 177. DE LATTIN, G. 1957. Die Ausbreitungszentren der holarktischen Landtierwelt. Zool. Anz. Suppl. 20: 380 410. DENNIS, R. L. H., W. R. WILLIAMS, AND T. G. SHREEVE. 1998. Faunal structures among European butter ies: Evolutionary implications of bias for geography, endemism and taxonomic af lation. Ecography 21: 181 203. FREY, J. K. 1992. Response of a mammalian faunal element to climatic changes. J. Mammal. 73:43 50. HAROLD, A. S., AND R. D. MOOI. 1994. Areas of endemism: De nition and recognition criteria. Syst. Biol. 43:261 266. HENDERSON, I. M. 1991. Biogeography without area? Aust. Syst. Bot. 4:59 71. HOLLOWAY, J. D., AND N. JARDINE. 1968. Two approaches to zoogeography: A study based on the distributions of butter ies, birds and bats in the Indo- Australian area. Proc. Linn. Soc. Lond. 179:153 188. HOVENKAMP, P. 1997. Vicariance events, not areas, should be used in biogeographical analysis. Cladistics 13:67 79. HUMPHRIES, C. J., AND L. R. PARENTI. 1999. Cladistic biogeography. Oxford Univ. Press, Oxford, U.K. JARDINE, N. 1972. Computational methods in the study of plant distributions. Pages 381 393 in Taxonomy, phytogeography and evolution (D. H. Valentine, ed.). Academic Press, London. KAISER, G. W., L. P. LEFKOVITCH, AND H. F. HOWDEN. 1972. Faunal provinces in Canada as exempli ed by mammals and birds: A mathematical consideration. Can. J. Zool. 50:1087 1104. LINDER, H. P. 2001. On areas of endemism, with an example from the African Restionaceae. Syst. Biol. 50:892 912. LINDER, H. P., AND D. M. MANN. 1998. The phylogeny and biogeography of Thamnochortus (Restionaceae). Bot. J. Linn. Soc. 128:319 357. MAYR, E. 1944. Wallace s line in the light of recent zoogeographic studies. Q. Rev. Biol. 19:1 14. MAYR, E. 1965. What is a fauna? Zool. Jahrb. Syst. 92:473 486. MORRONE, J. J. 1994. On the identi cation of areas of endemism. Syst. Biol. 43:438 441. MORRONE, J. J., AND J. V. CRISCI. 1995. Historical Biogeography: Introduction to methods. Annu. Rev. Ecol. Syst. 26:373 401. NELSON, G., AND N. PLATNICK. 1981. Systematics and biogeography: Cladistics and vicariance. Columbia Univ. Press, New York. PALLARY, P. 1909. Catalogue de la faune malacologique de l Égypte. Mem. Inst. Égyptian 6:1 92. PETERS, J. A. 1955. Use and misuse of the biotic province concept. Am. Nat. 89:21 28. PLATNICK, N. I. 1991. On areas of endemism. Aust. Syst. Bot. 4:xi xii. PLATNICK, N. I., AND G. NELSON. 1978. A method of analysis for historical biogeography. Syst. Zool. 27: 1 16. REBEL, H. 1931. Zur Frage der europäischen Faunenelemente. Ann. Naturhist. Mus. Wien 46:49 55. SIMPSON, G. G. 1977. Too many lines; the limits of the Oriental and Australian zoogeographic regions. Proc. Am. Philos. Soc. 121:107 120. UDVARDY, M. D. F. 1969. Dynamic zoogeography. Van Nostrand Reinhold, New York. VANE-WRIGHT, R. I. 1991. Transcending the Wallace line: Do the western edges of the Australian region and the Australian plate coincide? Aust. Syst. Bot. 4:183 197. First submitted 9 May 2001; reviews returned 22 March 2002; nal acceptance 2 May 2002 Associate Editor: Peter Linder Syst. Biol. 51(4):652 664, 2002 DOI: 10.1080/10635150290102311 Resolution of a Supertree/Supermatrix Paradox JOHN GATESY, 1 CONRAD MATTHEE, 2 ROB DES ALLE, 3 AND CHERYL HAYASHI 1 1 Department of Biology, University of California, Riverside, California 92521, USA 2 Department of Zoology, University of Stellenbosch, Stellenbosch 7602, South Africa 3 Department of Invertebrates, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA In the total evidence approach to systematics, all characters and taxa are merged in a single supermatrix, and the data are analyzed simultaneously (Miyamoto, 1985; Kluge, 1989; Nixon and Carpenter, 1996). Recently, however, a plea has been made for the use of supertrees in systematics (Sanderson et al., 1998). In this framework, individual characters are not interpreted as phylogenetic evidence. Instead, topologies supported by different published studies, that is, source trees, are encoded into