Acta Botanica Sinica 2004, 46 (3): 253 258 http://www.chineseplantscience.com Ancestral Area Analysis of the Genus Caragara (Leguminosae) ZHANG Ming-Li * (Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China) Abstract: Caragana has a temperate Asian distribution. Based on the phylogeny and 13 distributional areas of this genus, its ancestral area was studied via the ancestral area analysis suggested by Bremer (1992), Ronquist (1994) and Hausdorf (1997). The results indicate that three areas, Far East-Northeast China, Altai-Sayan and North China-Qinling Mountains (Mts) are likely the ancestral areas. Linking to the viewpoints of the Holarctic origin for north temperate flora, Far East-Northeast China seems more likely to be the ancestral area. According to the three ancestral areas isolated geographically and the analysis in the present study, as well as former biogeographical analysis of this genus, it is suggested that Caragana speciation is mainly in the mode of vicariance rather than dispersal, and dispersed is often in short distance. Key words: Caragana ; ancestral area; distribution pattern; evolution Caragana, belonging to the Papilionoideae (Leguminosae) and comprising about 70 species (Polhill, 1981), has a temperate Asian distribution (Wu,1993), mainly located in the cold and drought area of northwestern Qinghai-Xizang Plateau of China. The species of this genus have distinctive morphological variation and ecological adaptation especially to drought and cold. Some species occurring in grassland, desert or alpine mountain meadow, could form dominant and constructed species in shrubs, sometimes even solely occupied the whole community (Wu,1980). Komarov (1908; 1945) studied the East Asian and Mongolian floristic geography by using five genera Caragana, Clematoclethra, Codonopsis, Epimedium and Nitraria among which Caragana appeared as the key genus. After Komarov s works, Caragana has been treated as a hot spot by the plant taxonomists in China, Russia, Mongolia and other countries (Pojarkova, 1945; Moore, 1962; 1968; Sanchir,1979; 1980; Liu,1993; Zhao,1993). In terms of the origin of the genus, Komarov (1908; 1945) pointed out that the genus was originated from the southeastern East Asia, and C. sinica was the primitive species with pinnate leaves containing two pairs of leaflets. From the southeastern East Asia, this species evolved northward and westward respectively into one group with pinnate leaves containing many pairs of leaflets and into another group with palmate leaves. Komarov (1908; 1945) considered that the flora of Mongolia and Central Asia were originated from East Asia. Moore (1968) discussed the origin of the genus and found C. sinica was a triploid species (2n = 24) from chromosome data, suggesting that it could not be a primitive species. Most species with pinnate leaves containing many pairs of leaflets and foliage rachis deciduous were diploid (2n = 16) and likely formed a primitive group. Moore (1968) inferred that the southern Balkash Lake was the place of origin in terms of the groups at different evolutionary stages in his phylogenetic tree, and dispersed eastward to the Asian Pacific shore and westward to the southern Europe. However, both Sanchir (1979) and Zhao (1993) regarded C. arborescens morphologically as a primitive species, and its distributional areas, Siberia, as the place of origin. Having summed up the species morphology, pollen morphology and chromosome data, I set up a phylogenetic tree using cladistics (Zhang, 1997a), and analyzed the area relationship with analytical biogeographical methods such as component analysis, minimum spanning tree, cluster analysis and parsimonious analysis of endemicity (Zhang, 1996; 1998). The results showed that C. arborescens and its related group with pinnate leaves containing many pairs of leaflets were primitive, and originated from the eastern Siberia. However, the analytical biogeographical methods usually focus on the area relationship. While the distribution pattern, especially ancestral area, has not been directly studied. Therefore, in this study attention was paid to locate the place of origin by using the ancestral area analysis. Bremer (1992) proposed a method to estimate the center of origin or ancestral area. Ronquist (1994; 1995) critiqued Bremer s method based on the Camin-Sokal s irreversible parsimony, and suggested his method on the basis of Fitch s Received 20 Oct. 2003 Accepted 12 Dec. 2003 Supported by the National Natural Science Foundation of China (49971006, 39893360) and the Knowledge Innovation Program of The Chinese Academy of Sciences (KSCX2-1-06B). * Author for correspondence. E-mail: <minglizhang@hotmail.com>.
reversible parsimony. Bremer (1995) gave an explanation of his method. After combining both Bremer s (1992) and Ronquist s (1994) methods, Hausdorf (1997) proposed a weighted ancestral area analysis. So far, there are three methods for quantitative estimation of the ancestral area. In the present investigation, the ancestral area and distribution pattern of Caragana were analyzed by using a combination of all three methods. 1 Materials and Methods 1.1 Phylogenetic tree I have constructed a phylogenetic tree or cladogram of 72 species of the genus by using 24 characters comprising 20 morphological, three pollen and one chromosomal characters (Zhang,1997a). The twenty morphological characters are all good characters in the genus. Based on this cladogram, two reduced cladograms are obtained by reducing some species, just like our previous component analysis (Zhang, 1998) (Figs.1,2). 1.2 Areas The distribution region of Caragana was divided into 13 areas (Zhang,1998) according not only to the floristic regionalization of China (Wu and Wu, 1996) and that of the world (Takhtajan, 1986) (Fig.3), but also to the distributional characteristics of Caragana, for instance, C. sinica appeared in both the eastern and southern China. These two regions (Wu and Wu,1996) were treated as an area, namely Subtropical East Asia area. Thirteen areas could be regarded as endemic area to Caragana because there are endemic species in each area, and there are obvious differentiation among the areas in terms of the flora (Wu and Wu, 1986) and vegetation (Wu,1980). 1.3 Ancestral area analysis It is necessary to label the species distribution area into the two reduced cladograms (Figs.1, 2). And then the indices of G, L and G/L of Bremer s (1992) method, of S and RP of Rounquist s (1994) method, of GSW, LSW and PI of Hausdorf s (1997) method were calculated. In principles, Bremer s method and Hausdorf s method follow the criteria that the areas are positionally plesiomorphic in the area cladogram being more likely as parts of ancestral area than the positionally apomorphic branches. Ronquist s method estimates the area as ancestral area by the number of necessary steps under the assumption that this area was the ancestral area. The most probable ancestral area is with the minimum number of the steps. Fig.1. A reduced cladogram from Zhang (1997a) including 12 areas. A, Far East-Northeast China; B, Altai-Sayan; C, Mongolia Plateau; D, North China-Qinling Mts; E, Hengduan Mts; F, Himalayas; G, Balut-Afghanica; H, Central Asia; I, Tianshan Mts; J, Pamir-Alai; K, Europe-West Sibirica; L, Turan; M, East Asia Subtropical. Fig.2. A reduced cladogram from Zhang (1997a) including 13 areas. A M are the same as in Fig.1.
ZHANG Ming-Li: Ancestral Area Analysis of the Genus Caragara (Leguminosae) Fig.3. Caragana distribution and 13 areas (A M), of which A, B and D were the ancestral areas in this paper. These three areas are just Caragana arborescens distribution. A M are the same as in Fig.1. In Bremer s, Ronquist s and Hausdorf s methods, G (gain) means number of necessary gains forward Camin- Sokal parsimony; L (loss) means number of necessary losses under reverse Camin-Sokal parsimony; S means number of necessary steps if the area was the ancestral area; RP means S values rescaled to a maximum value as the reciprocal of the S values multiplied by the smallest S value; GSW means number of weighted gain steps; LSW means number of weighted loss steps; PI=GSW/LSW. If the G/L, RP and PI values of the area are larger, the area will more likely be the ancestral area. 2 Results and Discussion 2.1 Ancestral area The calculated results for Caragana are shown in Table 1 and Table 2 corresponding to Figs.1, 2, respectively. Three areas, Far East-Northeast China, Altai-Sayan, and North China-Qinling Mts, were shown to be the ancestral areas as they have the highest G/L, RP and PI values. Additionally Balut-Afghanica has also large values of G/L and PI, G/L=0.50, PI=0.36. In Table 2, both G/L and PI have in common the first five largest values, which correspond to five areas, i.e., Far East-Northeast China, Altai-Sayan, North China-Qinling Mts, Hengduan Mts, and Balut-Afghanica. Therefore, these areas are indicated as ancestral areas. However, in Table 2 the larger values of RP were found only in North China-Qinling Mts, Hengduan Mts, and Balut- Afghanica indicating that these areas were ancestral areas. This result is different from that coming from G/L and PI. And in Table 2, North China-Qinling Mts has the largest values of G/L, RP and PI obtained from the three methods. In Table 1, RP and PI values indicate that North China- Qinling Mts has the highest values, but the highest G/L values were obtained in Far East- Northeast China and Altai-Sayan. Which area is the most likely ancestral area among Far East- Northeast China, Altai-Sayan, and North China-Qinling Mts? Due to some primitive species of Caragana occurring in Boreal Siberia, the origin of boreal temperate flora was located in the eastern and middle Siberia (Budantsev,1992). So, the balanced conclusion to the place of origin between Caragana and boreal temperate flora would be inferred as the eastern Siberia, namely Far East- Northeast China. Previous results of analytical biogeography, Zhang (1998) also showed that Far East- Northeast China was the ancestral area of Caragana. The 13 areas were divided into two clusters, East Asia and Tethys, by using some analytical biogeographical methods, such as component analysis, minimum spanning tree (MST), parsimony analysis of endemicity (PAE) and cluster analysis (Zhang,1996; 1998). East Asia cluster is composed of Far East-Northeast China, Mongolia Plateau, North China-Qinling Mts, Hengduan Mts, Himalayas and East Asia Subtropical. Other areas belong to Tethys cluster. Why Mongolia Plateau was included in the East Asia cluster? Since Mongolia Plateau especially Nei Mongol and Northeast China-North China are geographically linked, and both share same species, such as C. microphylla, therefore, it would be reasonable, referring to the Caragana distribution pattern and in the present cladogram, to put Mongolia Plateau in the East Asia cluster. Because some areas with larger values belong to either East Asia or Tethys, which of the two clusters is primitive in the Caragana distribution pattern? For ancestral comparison here the average values of G/L and PI of the two area clusters are calculated (Tables 1, 2). All the above values indicate that East Asia is more likely primitive, its related G/L and PI values are always larger than those of Tethys. Consequently Kamarov s view
Table 1 An ancestral area analysis of Caragana based on Fig.1 G L G/L S RP GSW LSW PI A 1 1 1.00 14 0.93 1.00 1.00 1.00 B 1 1 1.00 14 0.93 1.00 1.00 1.00 C 1 4 0.25 15 0.87 0.50 2.50 0.20 D 4 5 0.80 13 1.00 2.03 1.62 1.26 E 1 5 0.20 15 0.87 0.33 2.83 0.12 G 2 4 0.50 15 0.87 0.83 2.33 0.36 H 1 8 0.13 15 0.87 0.17 3.95 0.04 I 1 8 0.13 15 0.87 0.17 3.95 0.04 J 1 4 0.25 15 0.87 0.50 2.50 0.20 K 1 7 0.14 15 0.87 0.20 3.78 0.05 L 1 8 0.13 15 0.87 0.17 3.95 0.04 M 1 6 0.17 15 0.87 0.25 3.08 0.08 G (gain), number of necessary gains forward Camin-Sokal parsimony; L (loss), number of necessary losses under reverse Camin-Sokal parsimony; S, number of neccessary steps if the area was the ancestral area; RP, S values rescaled to a maximum value of 1 by inverting them and multiplying by the smallest S value; GSW, number of weighted gain steps; LSW, number of weighted loss steps; and PI = GSW/LSW (Bremer, 1999; Ronquist, 1994; Habisdorfs, 1997). East Asia average G/L = (1.00+0.25+0.80+0.20+0.17)/5 = 0.484; Tethys average G/ L = (1.00+0.50+0.13+0.13+0.25+0.14+0.13)/7 = 0.326; East Asia average PI = (1.00+0.2+1.26+0.12+0.08)/5 = 0.532; Tethys average PI = (1.00+0.36+0.04+0.04+0.20+0.05+0.04)/7 = 0.247. A M are the same as in Fig.1. Table 2 An ancestral area analysis of Caragana based on Fig. 2 G L G/L S RP GSW LSW PI A 1 2 0.50 19 0.84 1.00 2.00 0.50 B 1 2 0.50 19 0.84 1.00 2.00 0.50 C 1 3 0.33 19 0.84 0.50 2.50 0.20 D 4 7 0.57 16 1.00 1.98 1.93 1.03 E 3 7 0.43 18 0.89 0.75 3.03 0.25 F 1 5 0.20 20 0.80 0.25 3.58 0.07 G 2 4 0.50 18 0.89 0.83 2.33 0.36 H 2 9 0.22 19 0.84 0.29 3.71 0.08 I 1 9 0.11 20 0.80 0.13 3.72 0.03 J 1 3 0.33 19 0.84 0.50 2.50 0.20 K 1 8 0.13 20 0.80 0.15 3.59 0.04 L 1 9 0.11 20 0.80 0.13 3.72 0.03 M 1 7 0.14 19 0.84 0.17 3.45 0.05 East Asia average G/L = (0.50+0.33+0.57+0.43+0.20+0.14)/6 = 0.362; Tethys average G/L = (0.50+0.50+0.22+0.11+0.33+0.13+0.11)/7 = 0.271; East Asia average PI = (0.50+0.20+1.03+0.25+0.07+0.05)/6 = 0.35; Tethys average PI = (0.50+0.36+0.08+0.03+0.20+0.04+0.03)/ 7 = 0.177. Abbreviations are the same as in Table 1. point (Kamarov, 1908; 1945), that Caragana was originated from East Asia and then dispersed into Mongolia and Central Asia, is reasonable. 2.2 Distribution pattern The ancestral areas of Caragana are likely to be Far East-Northeast China, Altai-Sayan, and North China-Qinling Mts according to our results from the ancestral area analysis. These three areas are just the distribution region of Caragana arborescens which is the most primitive species in Caragana (Zhang,1997a) (Fig.3). Because these areas are far isolated geographically, the speciation and diversification mode in Caragana could be explained on the basis of vicariance. Dispersion can only be considered as subordinate and is in short distance (Zhang,1997b; 1998), for instance, the distribution pattern of Qinghai-Xizang (Tibetan) Plateau and Himalayas (Zhang,1997b). Concerning the time of origin, the Bering Land Bridge connected the East Asia and North America, broke-up in Pliocene (Hamilton,1983; McKenna,1983). If the time of origin of Caragana was before the Pliocene, it should appear in North America via the Bering Lund Bridge before Pliocene where the two regions were connected. However, Caragana species are naturally absent in North America, so, according to its restricted temperate Asian distribution pattern and its absence in North America, the time of origin and differentiation of Caragana seem quite late, and could be inferred to Pliocene or latter. 2.3 Method of ancestral area analysis Some methods of analytical biogeography, such as component analysis, minimum spanning tree, parsimonious
ZHANG Ming-Li: Ancestral Area Analysis of the Genus Caragara (Leguminosae) analysis of endemicity and cluster analysis (Myers and Giller,1988), focus on the area relationship rather than on the identification and originiation of the ancestral area, except for component analysis. As ancestral area analysis is emphasized on estimation of ancestral areas (Bremer,1992; 1995), it provides some numerical indices, therefore, it is a suitable method. According to the three method of ancestral area analysis as well as the results of combined use of these methods in the present study, Hausdorf s (1997) method as derived from Bremer s (1992) gives an ancestral area weighted estimation in which PI is more precise than Bremer s (1992) G/ L to ancestral area. Moreover, Bremer s (1992) and Hausdorf s (1997) methods are different from Ronquist s (1994) method (Table 2). Compared with these three methods, the Nothofagus analysis resulting from Swenson et al. (2000) had also shown the same conclusion. Acknowledgments: I deeply appreciate to K Bremer for his help during my visit in Uppsala University. Many thanks are also given to F. Ronquist and J. Wen for his/her help, to three anonymous reviewers for their valuable comments. References: Bremer K.1992. Ancestral areas: a cladistic reinterpretation of the center of origin concept. Syst Biol, 41:436 445. Bremer K.1995. Ancestral areas: optimization and probability. Syst Biol, 44:255 259. Budantsev L Y. 1992. Early stages of formation and dispersal of the temperate flora in the boreal region. Bot Rev, 58:1 48. Hamilton W. 1983. Cretaceous and Cenozoic history of the northern continents. Ann Miss Bot Gard, 70:440 458. Hausdorf B. 1997. Weighted ancestral area analysis and a solution of the redundant distribution problem. Syst Biol, 47:445 456. Komarov V L. 1908. Generis Caragana monographia. Acta Horti Petrop, 29:77 388. Komarov V L. 1945. V.L. Komarov Opera Selecta. Mosquae: Acad Sci Press, USSR. 159 342. Liu Y-X. 1993. Caragana. Flora Reipublicae Sinicae. Tomus 42 (1). Beijing: Science Press. 17 67. (in Chinese) McKenna M C. 1983. Holarctic landmass rearrangement, cosmic events, and cenozoic terrestrial organisms. Ann Miss Bot Gard, 70:459 489. Moore R J. 1962. On the origin Caragana sinica. J Arnold Arboretum, 43:203 214. Moore R J. 1968. Chromosome numbers and phylogeny in Caragana (Leguminosae). Can J Bot, 46:1513 1522. Myers A A, Giller P S. 1988. Analytical Biogeography. London: Academic Press. Pojarkova A I. 1945. Caragana. Komarov V L. Flora of USSR, Vol.. Moscow and Leningrad: Acad Sci Press, USRR. 327 368. Polhill R M. 1981. Galegeae. Polhill R M, Raven P H. Advances in Legume Systematics, Part 1. London: Royal Botanical Garden, Kew. 357 363. Ronquist F. 1994. Ancestral areas and parsimony. Syst Biol, 43: 267 274. Ronquist F. 1995. Ancestral areas and revisited. Syst Biol, 44: 572 575. Sanchir Cz. 1979. Genus Caragana Lam. (Systematics, geography, phylogeny and economic significance in study on flora and vegetation of P.R. Mongolia. Vol.1. UlanBotaor: Academic Press. Sanchir Cz. 1980. Outline of Caragana Lam. Species. Trans Inst Bot Acad P. R. Mongolia, 4:106 123. Swenson U, Hill R R, McLoughlin S. 2000. Ancestral area analysis of Nothofagus (Nothofogaceae) and its congruence with the fossil record. Aust Syst Bot, 13:469 478. Takhtajan A. 1986. Floristic regions of the world. Berkeley:University of California Press. Wu C-Y. 1993. The areal-types of Chinese genera of seed plants. Acta Bot Yunnan, 5(Suppl.):1 139. (in Chinese with English abstract) Wu Z-Y. 1980. China Vegetation. Beijing: Science Press. (in Chinese) Wu Z Y, Wu S G. 1996. A proposal for a new floristic kingdom (realm) the E. Asiantic Kingdom,its delineation and characteristics. Zhang A L, Wu S G. Floristic Characteristics and Diversity of East Asian Plants. Beijing and Berlin: China Higher Education Press and Springer-Verlag. 3 42. Zhang M-L. 1996. A numerical analysis of endemism for Caragana (Fabaceae). Zhang A L, Wu S G. Floristic Characteristics and Diversity of East Asian Plants. Beijing and Berlin:China Higher Education Press and Springer-Verlag. 223 227. Zhang M-L. 1997a. A reconstructing phylogeny in Caragana (Fabaceae). Acta Bot Yunnan,19:331 341. (in Chinese with English abstract) Zhang M-L. 1997b. The geographical distribution of the genus Caragana in Qinghai-Xizang Plateau and Himalayas. Acta Phytotax Sin, 35:136 147. (in Chinese with English abstract) Zhang M-L. 1998. A preliminery analytical biogeography in Caragana (Fabaceae). Acta Bot Yunnan, 21:1 11. (in Chinese with English abstract) Zhao Y-Z. 1993. Taxonomic study of the genus Caragana from China. Acta Sci Nat Univ Intramongolicae, 24:631 653. (in Chinese with English abstract) (Managing editor: HAN Ya-Qin)