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2Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing 100093, People's Republic of China; and 4Department of Natural Sciences, Florida Museum of Natural History, Gainesville, Florida 32611
Received for publication June 26, 1998. Accepted for publication January 11, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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Key Words: Betulaceae • ecological adaptation • ITS sequences • paleobotany • phylogeny • rbcL sequences
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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130 modern species (Chen, 1994
). Most species of the family are distributed in temperate regions of the Northern Hemisphere. Some species occupy subtropical highlands and extend up to 4100 m in elevation (e.g., Betula platyphylla Suk.). Only one species, Alnus glutinosa (L.) Gaertn., occurs in Africa. Another, Alnus accuminata HBK, extends from central America southward to northern Argentina. Except for Ostryopsis, which is endemic to China, the other five genera show similar patterns of distribution among the northern continents.
Ever since the genus Ostryopsis Decne. was established in 1873, the Betulaceae sensu lato have been considered to include six extant genera. Most authors have supported the division of the family into two main clades, treated either as two tribes (Prantl, 1894
; Winkler, 1904
) or subfamilies (Rendle, 1925
; Jury, 1978
; Takhtajan, 1980
; Thorne, 1983
; Furlow, 1990
). Some authors ranked these two clades as families—Betulaceae sensu stricto (Alnus and Betula) and Corylaceae (Corylus, Ostryopsis, Carpinus, and Ostrya) (e.g., Hutchinson, 1967
; Dahlgren, 1983
). However, the Betulaceae sensu lato are a monophyletic family of woody plants defined by several synapomorphies, such as male and female compound catkins composed of cymules each with two or three flowers (Abbe, 1935
, 1938
, 1974
), the slightly rugulate, microspinulate sculpture of pollen exine seen with scanning electron microscopy, and the relative thick tectum with microchannels (Chen, 1991
). The monophyly of the family is also supported by numerous similarities in growth habitat (Kikuzawa, 1982
), morphology (Metcalfe and Chalk, 1950
), wood anatomy (Hall, 1952
), S-type sieve-tube plastids (Behnke, 1973
), embryology (Chen, Lu, and Pan, 1990
; Zhang and Chen, 1994
; Xing, Chen, and Lu, 1998
), and serology (Brunner and Fairbrothers, 1979
). With respect to the phylogenetic relationships of the Betulaceae, although extensive research has been conducted by many authors (e.g., Abbe, 1938
; Hjelmqvist, 1948
; Hall, 1952
; Kuprianova, 1965
; Hardin and Bell, 1986
; Chen, Lu, and Pan, 1990
; Furlow, 1990
; Chen, 1991
; Chen and Zhang, 1991
), nearly all arrangements of the six genera can be found in the literature.
Cladistic analyses were carried out by Crane (1989)
using 14 reproductive characters and by Bousquet, Strauss, and Li (1992)
using 35 morphological characters. They arrived at the same cladograms of the generic relationships of the Betulaceae. Crane (1989)
also discussed the evolution of the family based on abundant fossil records and considered that the fossil history of the Betulaceae conforms well to the phylogenies obtained. Bousquet, Strauss, and Li (1992)
compared the trees resulting from morphology and chloroplast DNA (cpDNA) rbcL nucleotide sequences. They concluded that there is complete congruence between morphological and rbcL-based molecular phylogenies, although Ostryopsis was excluded from their study, and the rbcL sequences from their study provided only 12 informative sites within the family. Savard, Michaud, and Bousquet (1993)
studied phylogenetic relationships between Alnus and Betula using the internal transcribed spacer (ITS) region of 18S–26S nuclear ribosomal DNA (nrDNA) and found that the ITS sequences have more informative sites that provide higher resolution for assessing the generic relationships than rbcL sequences.
This paper addresses the relationships of the six extant genera of the Betulaceae using ITS sequences of the nrDNA to provide increased phylogenetic resolution. In addition, the rbcL gene of Ostryopsis was sequenced to supplement the data of Bousquet, Strauss, and Li (1992)
and provide an rbcL data matrix for all the betulaceous genera. We compare the results of independent rbcL, ITS, and morphologically based phylogenetic analyses. We then combine the three data sets to evaluate the phylogeny using the greatest number of characters and reassess the morphological character evolution within the family. The resulting phylogeny is compared with trends inferred from the ecology and geographic distribution of extant taxa and evaluated in relation to data from the paleobotanical record.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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to include all extant genera of the family by sequencing the rbcL gene of Ostryopsis davidiana. The same accession of total DNA was used as that for sequencing ITS (see below). The molecular techniques were as described in Chen et al. (1998).
In order to better understand the outgroup relationships with other hamamelid families, we also established a data matrix including 26 rbcL sequences from the Betulaceae, Casuarinaceae, Myricaceae, Juglandaceae, Rhoipteleaceae, Fagaceae, Nothofagaceae, Moraceae, Ulmaceae, Urticaceae, Cercidiphyllaceae, Hamamelidaceae, and Cunoniaceae (Table 1). The data were employed in two separate analyses: (1) using Cunoniaceae of the Rosidae as an outgroup; and (2) using Cercidiphyllaceae and Hamamelidaceae of the "lower" Hamamelidae as outgroups. The shortest trees were sought with Phylogenetic Analysis Using Parsimony (PAUP) version 3.1.1 (Swofford, 1993
) with tree bisection and reconnection (TBR) branch swapping of the heuristic method. Relative support for clades was assessed with 500 replicates of bootstrap analysis.
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with a minor modification for extracting large amounts of total DNA. The universal primers "ITS3" and "ITS4" of White et al. (1990)
and P1 and P2 were used for amplification and sequencing. P1 and P2 were designed according to the rRNA gene sequence of Oryza sativa (Takaiwa, Oono, and Sugiura, 1985
). P1 is located 48-23 bp upstream from the 3' end of the 18s rRNA gene (5'-AGA AGT CGT AAC AAG GTT TCC GTA GG-3'). P2 is 15–39 bp downstream from the 5' end of the 5.8s rRNA gene (5'-GAT GCG AGA GCC GAG ATA TCC GTT G-3') (Wang and Li, 1998
). Polymerase Chain Reaction (PCR) was conducted in a thermocycler (Perkin Elmer 9600, Norwalk, CT). A double-stranded DNA including complete sequences of ITS-1 and ITS-2 was generated by primer pair P1 and "ITS4." The PCR products were purified by Wizard® PCR preps DNA purification system (Promega, Madison, WI), and then sequenced directly on an LKB DNA Sequencing Station (Pharmacia) using the Silver SequenceTM DNA sequencing system (Promega). Both ITS-1 and ITS-2 DNA strands were sequenced (Appendix 1), and at least 80% of the sequences were overlapped for verification. In order to ensure the quality of the DNA sequences, the purified PCR products for seven species were sequenced automatically to verify the manually generated sequences, using an ABI 377 DNA Sequencer. "ITS4" was used as the sequencing primer and at least 600 bp of DNA sequences, including ITS-1, ITS-2, and 5.8s, were obtained for each sample.
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. All ITS sequences were aligned manually. The gaps were treated as missing or as the fifth character state. For each analysis, 100 replications of random addition were conducted using heuristic searches with TBR branch swapping and MULPARS to save all equally most parsimonious trees. Bootstrap analyses consisted of 500 replications using heuristic searches with TBR branch swapping and simple addition.
Morphological and combined data analysis
Based on extensive specimen studies and the literature (inflorescences, cymules, and flowers—Abbe, 1935
, 1938
, 1974
; wood anatomy—Tippo, 1938
; Hall, 1952
; leaf morphology—Hardin and Bell, 1986
; Chen and Zhang, 1991
; pollen morphology—Wodehouse, 1935
; Kuprianova, 1963
, 1965
; Chen, 1991
), we selected 22 more stable morphological characters (Appendix 2). Nothofagus was designated as the outgroup. In the morphological character matrix (Appendix 3), 18 characters were treated as binary and four were coded as multistate. Parsimony analysis was conducted using the branch-and-bound algorithm of PAUP 3.1.1 with multistate characters treated as unordered (except character 8, which was treated as ordered). The distribution of nonhomoplasious and homoplasious characters was shown on the most parsimonious tree. Subsequently, two additional parsimony analyses were conducted treating all multistate characters as unordered and as ordered, respectively, to examing changes of topology and bootstrap support for each clade.
In the combined data matrix, the ITS sequences of Ostrya rehderiana Chun, Carpinus turczaninowii Hance, Ostryopsis davidiana Decne., Corylus heterophylla Fisch. ex Trautv., Betula alleghaniensis Britton, and Alnus glutinosa (L.) Gaertn. were used to represent each genus. The data from rbcL, ITS, and morphology were combined without weighting. Data were analyzed with PAUP 3.1.1 using the heuristic search options with gaps treated alternately as missing data or as the fifth character state. Bootstrap analyses were used to assess the robustness of the estimated phylogenetic trees. Each of these analyses was based on 500 replications.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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For the Betulaceae, only one topology is shown in all the most parsimonious and strict consensus trees. They have two major lineages, in agreement with the traditional division of the family. Alnus and Betula form the Betuloideae clade, and the other four genera comprise the Coryloideae clade. In the latter, Corylus is the sister group of Ostryopsis–Carpinus–Ostrya, and Ostryopsis is the sister group to Carpinus–Ostrya. The 50% majority rule consensus tree (CI = 0.617) with Bauera as an outgroup is shown with bootstrap values for each clade in Fig. 1. In this tree, the other hamamelid families, with the exception of Fagaceae, are monophyletic. The Betulaceae are first united with the Casuarinaceae and situated in a polytomy with Fagaceae, Myricaceae, and Rhoipteleaceae–Juglandaceae. The above clade is supported by a bootstrap value of 67%, and Nothofagus is the sister group of the clade. Rhoiptelea is closely related to the sampled genera of the Juglandaceae. They form a well-supported clade with a bootstrap value of 100%. The arrangement of genera within the Betulaceae is the same as in the above most parsimonious and strict consensus trees. The large clade including Corylus, Carpinus, Ostryopsis, and Ostrya is well supported with a bootstrap value of 99%, confirming the natural grouping of subfamily Coryloideae. Alnus and Betula form a single clade with a bootstrap value of 54%.
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). The length of ITS-1 varied from 214 to 223 bp, whereas that of ITS-2 varied from 228 to 232 bp. Within the Betulaceae, 79 sites for ITS-1 and 102 for ITS-2 are variable. Forty of 246 aligned sites (16.3%) within ITS-1 and 56 of 245 aligned sites (22.7%) within ITS-2 were phylogenetically informative (Appendix 1). The percentage of phylogenetically informative sites was 19.6% for ITS-1 and ITS-2 combined—more than 20 times as many as in the rbcL region. For the entire sequence, values of pairwise percentage sequence divergence ranged from 0.7 to 21.9% among the sampled betulaceous species and from 23.6 to 30.6% among the outgroup, Nothofagus, and the species in the Betulaceae (Table 4). Thus sequence divergence was much higher than that in rbcL (Table 3).
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). In the ITS tree Ostrya and Sect. Carpinus are united in a clade supported by a bootstrap value of 82%, with Sect. Distegocarpus as its sister group. The close relationship between Ostrya and Carpinus is also supported by morphological characters, such as vessels with simple perforations and tyloses (Hall, 1952
). However, these two genera are readily distinguished by their fruit morphology. Ostrya has inflated bladder-like, radially symmetrical involucres unlike the flat, open involucres of Carpinus. The extinct genus Asterocarpinus Manchester and Crane (1987)
is intermediate in having a radially symmetrical involucre that is open with four to seven lobes and occurs in the lower Oligocene at the same time as the first known Ostrya fruits. This result, if corroborated by other data sets, would suggest that Ostrya and Asterocarpinus should not be treated as distinct genera from Carpinus. When the gaps were treated as the fifth state, a single most parsimonious tree with 488 steps and CI = 0.793 resulted. The topology of the tree is the same as that generated when gaps were treated as missing. The bootstrap values for some clades differ slightly.
Morphological data
The four multistate characters (Appendix 2) were treated as unordered except for character 8 (anther sac separation), which we assumed to be ordered. The phylogenetic analysis of the Betulaceae using Nothofagus as the outgroup yielded a single most parsimonious tree of 37 steps with a consistency index of 0.703 (Fig. 3). The tree shows two major lineages, in agreement with those of the rbcL and ITS trees (Figs. 1, 2). The Coryloideae clade is well supported by eight characters, including four synapomorphies, and a bootstrap value of 86%. Corylus is the sister group of Ostryopsis–Carpinus–Ostrya. The later clade is supported by four nonhomoplasious characters and a bootstrap value of 63%. Ostryopsis is the sister group to Carpinus–Ostrya, and the latter two genera are linked by three nonhomoplasious characters and a high bootstrap value (94%). Alnus and Betula are united by one homoplasious and one nonhomoplasious character and supported by a bootstrap value of 63%.
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Combined data
An analysis based on the combined data sets from rbcL, ITS, and morphology, with gaps treated as missing data, generated a single most parsimonious tree of 366 steps (CI = 0.877). This tree (Fig. 4) resembles the ITS tree (Fig. 2) in having two major lineages. The Coryloideae clade, and the sister-group relationship between Carpinus and Ostrya, are reinforced with a bootstrap value of 100%. The Ostryopsis–Carpinus–Ostrya clade receives support with a bootstrap value of 82%, higher than that in the ITS and morphological trees. It is noteworthy that the Betuloideae clade is more strongly supported by combined analysis than in any of the separate analyses. The bootstrap value is as high as 88%, in contrast to 74%, the highest value obtained from a separate analysis (ITS). When gaps were treated as a fifth state, the analysis yielded a single most parsimonious tree (CI = 0.880) of 441 steps with bootstrap support levels similar to that in the above tree.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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These results support the continued recognition of two subfamilies in the Betulaceae: Betuloideae and Coryloideae, as suggested previously (Rendle, 1925
; Jury, 1978
; Furlow, 1990
). Relationships among genera within the Coryloideae have been debated, particularly the position of Ostryopsis. Abbe (1938)
placed Ostryopsis and Corylus together in the same tribe (Coryleae), contrasted with the tribe Carpineae, in which he placed Carpinus and Ostrya. Based on pollen and other morphological characters, Chen (1991
, 1994)
concluded that Ostryopsis should be placed with Carpinus and Ostrya in the Carpineae, leaving Corylus as a monogeneric tribe. The results of our current analyses strongly support the position of Ostryopsis as a sister group to Carpinus + Ostrya and that these three genera form a sister group to Corylus. Thus, Ostryopsis + Corylus would be a paraphyletic group, whereas Ostryopsis + Carpinus + Ostrya are a monophyletic group. Accordingly, we support the division of extant genera of the Coryloideae into two tribes: Coryleae (Corylus) and Carpineae (Ostryopsis, Carpinus, Ostrya). Among the extinct fruit genera known from the fossil record, Asterocarpinus (which appeared at about the same time as Ostrya) clearly falls within the Carpineae, but Palaeocarpinus (which predates the appearance of extant coryloid genera) has a combination of characters that seem to indicate an intermediate position between Corylus and Carpinus.
Congruence between phylogeny and ecological evolution
Ecologically informative characters can be compared with the phylogenetic tree to consider the possible influences of climate on the diversification of the Betulaceae (Fig. 5). Kikuzawa (1982)
conducted a cultivation experiment on 12 betulaceous species and observed the characteristics of leaf growth and winter buds. He found that new leaves are produced continuously from April to August each year in Alnus and Betula. By contrast, the period of new leaf appearance is very short in Carpinus and Ostrya and intermediate in Corylus. Another interesting climatic adaptation is the variation in number of scales in the winter buds. Winter buds of most Alnus species have only two scales. The number of bud scales increases successively from Betula to Carpinus. Betula, Corylus, and Ostryopsis have two to six scales, Ostrya and Carpinus up to 24.
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Except for Sect. Alnobetula, which is distributed at relatively higher latitudes, the alders have winter buds that are pedicellate, with only two scales, and have initiation and flowering of inflorescences during the same season, a long period of new leaf initiation, and the phenomenon of heavy leaf fall during the summer—characters that are apparently adaptive to climatic conditions of warmth throughout the year, precipitation in the spring, and drought in the summer. If Alnus represents the extant descendant of the most primitive betulaceous plants, then the family might have originated in an area with some Mediterranean climate features, and a number of derived groups of the family might have differentiated in more temperate climate. Indicators of more temperate climatic adaptation (colder winters, drier springs) include more protected winter buds, much shorter period of leaf appearance, the lack of excessive leaf fall during the summer, and the first-year appearance of catkins but flowering during the spring of the following year. These features occur in the derived groups of the Betulaceae and are particularly well represented by Carpinus and Ostrya.
Eastern Asia has the highest diversity and greatest level of endemism for the family. In addition to the genus Ostryopsis, several sections are restricted to this region today, including Betula sections Betulaster and Chinenses, Alnus sect. Cremastogyne, Corylus sect. Acanthochlamys, and Carpinus sect. Distegocarpus. Based on a statistical evaluation of the geographic distribution of species, sections and genera in the Betulaceae (Chen, 1994
), Sichuan Province and its adjacent provinces or regions of China (so-called Central China) are the distribution center of the extant members of Betulaceae. All six genera and 52 species, constituting 70.3% of the family, are native to this region today.
Paleogeographic and paleoclimatic evidence indicates that the Eurasian continent was more fragmented in the Late Cretaceous and Tertiary than at present, with many islands of different sizes south of the continent (Sun, 1979
). The Tethys Sea extended as far east as Tibet and Xinjiang, China, until the Early Tertiary. The climate of Central China was greatly influenced by the Tethys Sea, and the southeastern and the southwestern oceanic monsoons were weak compared with the present day (Guo, 1983
). Therefore, the climate of Central China in the Late Cretaceous and Early Tertiary was probably like that of the modern Mediterranean region with warm, wet springs and hot, recurrently dry summers. Such a climate is similar to that inferred for the early betulaceous plants based on phylogenetic relationships (Fig. 6). Thus, Central China might have been the center of origin and early evolution of the Betulaceae during the latest Mesozoic time. It is also true that this part of China acted as a refugium, preserving many taxa that became extinct in other parts of the Northern Hemisphere, because of the less severe impact of climatic cooling during the late Tertiary and Pleistocene (Ying, Zhang, and Boufford, 1993
; Manchester, 1999
). Ultimately, we must look to the fossil record of this part of China to assess the antiquity of the Betulaceae here in relation to other parts of the Northern Hemisphere.
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The oldest known Alnus infructescences occur in the middle Eocene of Oregon, USA, where they co-occur with staminate catkins and leaves (Crane, 1989
), but the pollen record suggests an earlier history for the genus, or perhaps related extinct genera. Stephanoporate pollen assigned to Alnipollenites R. Potonie with arci and vestibula diagnostic of Alnus is found in the Late Cretaceous (Santonian) of Japan (Miki, 1977
) and becomes very common in Eurasia and North America by the latest Cretaceous (Bratzeva, 1967
; Kedves and Uri-Kiss, 1968
; Sun, Zhang, and Hou, 1979
; Muller, 1981
). Alnipollenites is also reported from the Oligocene of Kalimantan (Sun et al., 1981
), the Miocene of Assam (Banerjee, Misra, and Koshal, 1971
) and Central America (Martin and Harrell, 1957
), and the Pleistocene of Taiwan islands (Chung and Huang, 1972
) and the northern Andes (van der Hammen, 1989
). It is likely that many of these later records actually represent the extant genus Alnus.
Paraalnipollenites L. S. Hills et S. Wallace, with weakly defined arci and vestibulate pores, is another pollen genus similar to Alnus, but its grains are triporate in contrast to the usually 4- and 5-porate pollen of Alnipollenites and Alnus, and might be considered morphologically intermediate between Alnus and Betula. Paraalnipollenites is recorded from the Maestrichtian of Inner Mongolia, China (Sun, Zhang, and Hou, 1979
) and Montana, USA (Oltz, 1969
). Thus, the pollen evidence suggests more diversity in the Alnus complex during the Late Cretaceous than at present, but the plants that produced Alnipollenites and Paraalnipollenites remain unknown from inflorescences, fruits, or leaves.
Reliable macrofossils of Betula first appear in the middle Eocene of North America (Crane and Stockey, 1987
). Reports of the genus from earlier strata of the Paleocene (such as, Seward and Holltum, 1924
—Europe; Hickey, 1977
—USA; Tao and Xiong, 1986
—China), based on fossil leaves and woods, remain unsubstantiated by the diagnostic inflorescence bracts. Fossil pollen resembling that of Betula has been assigned to two fossil pollen genera, Betulaepollenites R. Potonie and Betulaceoipollenites R. Potonie. Betulaepollenites grains have three pores with evident arci and vestibula. They first appear in the Late Cretaceous (Campanian) of Japan (Miki, 1977
) and subsequently occur in the Paleogene of China (Sun, Zhang, and Hou, 1979
) and North America (Frederiksen, 1989
). Grains of the other genus, Betulaceoipollenites, lack arci, but sometimes have an apparent vestibulum. They have been recorded from the Late Cretaceous (Maestrichtian) of Inner Mongolia, China (Sun, Zhang, and Hou, 1979
) and from the Paleocene of Far Eastern Russia (Bratzeva, 1967
) and Europe and North America (Williams and Brideaux, 1975
).
Arci and vestibula are important pollen characteristics of the early Betulaceae. Among fossil pollen grains with arci and vestibula, tetra- and pentaporate types occurred earlier than triporate ones. Triporate pollen grains with arci and vestibula appear earlier than those without arci and vestibula. With a few exceptions (e.g., A. rubra), the pollen of extant Alnus species has arci and vestibula. Although usually absent from the extant genus Betula, some species (e.g., Betula pubescens) may have weak arci. Both extant and extinct Coryloideae pollen lack arci and vestibula. The earliest fossil pollen grains considered to represent coryloid plants are Paleocene. All the Betulaepollenites pollen grains with arci might demonstrate that Alnus is indeed closely related to Betula. Betulaceoipollenites grains without arci are more similar to that of modern Betula than is Betulaepollenites. Therefore, Betulaceoipollenites may be considered more derived than Betulaepollenites. A genuine understanding of the systematic relationships of the plants that produced these kinds of pollen during the late Cretaceous must await recovery of megafossil specimens, especially flowers containing the pollen and the corresponding fruits. Such material would help to show whether these pollen were produced by true members of the Betulaceae or perhaps by parallel or convergent extinct taxa of the Normapolles complex. If we accept the pollen record at face value, it suggests that the Betuloideae predate the Coryloideae, which is congruent with our phylogenetic analyses of the extant genera. On the other hand, the earliest confirmed fruits of the family belong to the Coryloideae. The Coryloideae are represented by fruits of Palaeocarpinus and Cranea in the Paleocene, 58 million years ago, whereas Alnus and Betula fruiting material is not known until the middle Eocene, 48 million years ago.
The fossil genus Palaeocarpinus Crane conforms morphologically to the Coryloideae and may represent an ancestral stock within that subfamily. As in modern Coryloideae, the female catkins of Palaeocarpinus are composed of many two-flowered cymules. The paired, equal-sized, spiny to entire-margined bracts are similar to those of Corylus, but the small, longitudinally ribbed nuts are similar to those of Carpinus. In situ pollen grains from associated staminate catkins lack arci and are similar to those of Corylus, Carpinus, Ostryopsis, and Ostrya (Manchester and Chen, 1996
). Since Palaeocarpinus was established by Crane in 1981, about five species have been found from Paleocene deposits in England, northwestern China, and several localities in North America (Crane, 1981
; Crane, Manchester, and Dilcher, 1990
; Sun and Stockey, 1992
; Manchester and Chen, 1996
; Manchester and Guo, 1996
). This distribution pattern, involving all three northern continents, is also seen in extant Corylus, Carpinus, and Ostrya. It indicates that, as early as the Paleocene, coryloid plants were extensively distributed in the Northern Hemisphere, although the reliable fossil records of extant Corylus, Carpinus, and Ostrya (fossil bracts and nuts) occurred only later, in the middle Eocene to Early Oligocene (Tanai, 1972
; Manchester and Crane, 1987
; Wolfe and Wehr, 1987
).
Manchester and Chen (1998)
recently reported another Paleocene fossil genus—-Cranea from Wyoming, USA, based on leaves, involucres, fruits, and associated staminate catkins with in situ pollen. Most interestingly, the involucre of Cranea is almost the same as that of the extant Ostryopsis, but the latter is endemic to China. The associated catkins have pollen grains of the Carpinus type (Chen, 1991
), similar to those of Ostryopsis, Carpinus, and Ostrya. Cranea might be considered a link between primitive coryloid plants and the Ostryopsis–Carpinus–Ostrya clade. However, insufficient characters are known to include it in the phylogenetic analysis.
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PHYLOGENETIC IMPLICATIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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The sister-group relationship of Alnus and Betula is moderately well supported by ITS and rbcL sequence data. These genera are similar in the formation of paired wings that develop on the lateral margins of the ovary wall, but this may be a plesiomorphic character because it is shared with Nothofagus. It may be that Alnus was the earliest to diverge from the ancestor of the Betulaceae because it retains some primitive and distinct characters of the family, such as bisexual inflorescences, three-flowered cymules with more bracts, staminate flowers with perianth, and the cyclocytic stomatal apparatus. The Betulaceae have been considered likely to have evolved from Cretaceous groups with Normapolles pollen (Doyle, 1969
), having complex apertures. The pollen of Alnus, with arci, vestibulate apertures, and endexine thickening at apertural region is more similar than any other extant genera of the Betulaceae to pollen of the Normapolles complex.
Betula appears in some respects to be transitional between the Betuloideae and Coryloideae. Most features of the inflorescence, cymule, fruit, and wood are the same as or similar to those in Alnus, whereas the bifurcate stamen filament of Betula corresponds to that in the Coryloideae. The pollen of Betula exhibits characters intermediate between Alnus and Coryloideae, such as mostly triporate grains, arci lacking in most species, and vestibula absent in some species.
The Coryloideae clade is well supported in all trees generated by morphological, molecular, and combined analyses. Within this large clade, Corylus is the sister group of the other three genera in most trees. On the one hand, Corylus has some primitive characters shared with Alnus and Betula, such as bisexual inflorescences, staminate flowers with perianth, pollen apertures nonoperculate, endexine thickening at apertural region, and a haploid chromosome number of 14. On the other hand, it displays characters in common with Ostryopsis, Carpinus, and Ostrya, such as two-floret cymules with fewer bracts, tracheids absent, vessels without spiral thickening, and pollen without arci and vestibulum. Additionally, the occurrence of more autapomorphies on the Corylus branch relative to the other genera of Coryloideae indicates that Corylus might have a long evolutionary history since divergence from its ancestral group. These characters include filaments completely divided longitudinally and large, animal-dispersed fruits with hypogeal germination.
The relationship between Ostryopsis and the Carpinus–Ostrya clade is demonstrated by ITS and rbcL sequences and morphological and combined data. The three genera are united by such characters as male flowers without perianth, pollen with operculate apertures and endexine not thickening at apertural region, and a haploid chromosome number of eight. In addition, the close relationship between Carpinus and Ostrya is confirmed by this study. Among all clades in the trees generated by ITS and rbcL sequences and morphological and combined data, the one uniting Carpinus and Ostrya is one of the most strongly supported. In these genera the vessels all have simple perforations and tyloses, and their inflorescences, cymules, flowers, and pollen are also very similar. However, Carpinus is readily distinguished by leaf epidermal characters, including brachyparacytic stomata and a double-layered outer stomatal rim (Chen and Zhang, 1991
).
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PHYTOGEOGRAPHIC IMPLICATIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPHYLOGENETIC IMPLICATIONSPHYTOGEOGRAPHIC IMPLICATIONSLITERATURE CITED |
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; Manos, Nixon, and Doyle, 1993
; Manos and Steele, 1997
; Chen et al., 1998
). Nevertheless, the family appears to have originated in Laurasia during the Cretaceous, judging from distribution patterns of fossil and extant representatives. Late Cretaceous and Early Tertiary fossil occurrences of betulaceous fossils are almost exclusively from temperate latitudes of the Northern Hemisphere.
By the Oligocene, it is safe to say that all six extant genera of the Betulaceae had differentiated. Only Ostryopsis has not yet been confirmed by fossil fruit or involucre remains. During the Cretaceous and Early Tertiary, migration between Eurasia and North America was possible via the North Atlantic and Bering land bridges (Tiffney, 1985
). The effect of these intercontinental migrations can still be observed among several genera of the family today, although the land connections have been severed.
The migration of the Betulaceae southward and into the Southern Hemisphere might have begun from Oligocene with the climatic deterioration around the globe, and this process might have accelerated during the glacial epoch of the Quaternary. Based on fossil pollen evidence, it is likely that Alnus reached Kalimantan during the Oligocene (Sun et al., 1981
). Alnus, Carpinus, and Ostrya arrived in Central America during the Miocene (Martin and Harrell, 1957
; Graham, 1973
). By the end of the Pleistocene, Alnus and Carpinus might have been dispersed to Africa and South America (van der Hammen, 1989
) and Alnus and Carpinus to Taiwan (Chung and Huang, 1972
) when the sea level lowered sufficiently to permit overland migration.
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FOOTNOTES |
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3 Author for correspondence (e-mail: chenzd@sun.ihep.ac.cn).
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LITERATURE CITED |
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———. 1938 Studies in the Phylogeny of the Betulaceae. 2. Extremes in the variation of floral and inflorescence morphology. Botanical Gazette 99: 431–469.[CrossRef]
———. 1974 Flowers and inflorescences of the "Amentiferae." Botanical Review 40: 159–261.
Banerjee, D. C., M. Misra, and V. N. Koshal. 1971 Palynology of the Tertiary subcrops of upper Assam. Palaeobotanist 20: 1–6.
Behnke, H.-D. 1973 Sieve-tube plastids of Hamamelididae. Taxon 22: 205–210.
———, L. Simon, and M. Lalonde. 1990 DNA amplification from vegetative and sexual tissues of trees using polymerase chain reaction. Canadian Journal of Forest Research 20: 254–257.
Bousquet, J., S. H. Strauss, and P. Li. 1992 Complete congruence between morphological and rbcL-based molecular phylogenies in birches and related species (Betulaceae). Molecular Biology Evolution 9: 1076–1088.
Bratzeva, G. M. 1967 The problem of the Tsagaiansk flora with regard to spore and pollen analytical data. Review of Palaeobotany and Palynology 2: 119–126.
Brunner, F., and D. E. Fairbrothers. 1979 Serological investigations of the Corylaceae. Bulletin of the Torrey Botanical Club 106: 97–103.[CrossRef][ISI]
Chase, M. W., et al. 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528–588.[CrossRef][ISI]
Chen, Z.-D. 1991 Pollen morphology of the Betulaceae. Acta Phytotaxonomica Sinica 29: 464–475 (in Chinese with English summary).
———. 1994 Phylogeny and phytogeography of the Betulaceae. Acta Phytotaxonomica Sinica 32: 1–32, 101–153 (in Chinese with English summary).
———, A.-M. Lu, and K.-Y. Pan. 1990 The embryology of the genus Ostryopsis (Betulaceae). Cathaya 2: 53–62.
———, X.-Q. Wang, H.-Y. Sun, Y. Han, Z.-X. Zhang, Y.-P. Zou, and A.-M. Lu. 1998 Systematic position of the Rhoipteleaceae: evidence from nucleotide sequences of rbcL gene. Acta Phytotaxonomica Sinica 36: 1–7.
———, and Z.-Y. Zhang. 1991 A study on foliar epidermis in the Betulaceae. Acta Phytotaxonomica Sinica 29: 156–165 (in Chinese with English summary).
Chung, T.-F., and T.-C. Huang. 1972 Paleoecological study of Taipei Basin. Taiwania 17: 117–141, 239–247.
Crane, P. R. 1981 Betulaceous leaves and fruits from the British upper Palaeocene. Botanical Journal of the Linnean Society 83: 103–136.
———. 1989 Early fossil history and evolution of the Betulaceae. In P. R. Crane and S. Blackmore [eds.], Evolution, systematics, and fossil history of the Hamamelidae, vol. 2, ‘Higher’ Hamamelidae, 87–116. Clarendon Press, Oxford.
———, S. R. Manchester, and D. L. Dilcher. 1990 A preliminary survey of fossil leaves and well-preserved reproductive structures from the Sentinel Butte Formation (Paleocene) near Almont, North Dakota. Fieldiana Geology, New Series, no. 20: 1–63.
———, and R. A. Stockey. 1987 Betula leaves and reproductive structures from the Middle Eocene of British Columbia, Canada. Canadian Journal of Botany 65: 2490–2500.
Dahlgren, R. 1983 General aspects of angiosperm evolution and macrosystematics. Nordic Journal of Botany 3: 119–149.
Doyle, J. A. 1969 Cretaceous angiosperm pollen of the Atlantic Coastal Plain and its evolutionary significance. Journal of the Arnold Arboretum 50: 1–35.
Frascaria, N., L. Maggia, M. Michaud, and J. Bousquet. 1993 The rbcL gene sequence from chestnut indicates a slow rate of evolution in the Fagaceae. Genome 36: 668–671.[Medline]
Frederiksen, N. O. 1989 Late Cretaceous and Tertiary floras, vegetation, and paleoclimate of New England. Rhodora 91: 25–48.[ISI]
Furlow, J. J. 1990 The genera of Betulaceae in the southeastern United States. Journal of the Arnold Arboretum 71: 1–67.[ISI]
Graham, A. 1973 Literature on vegetational history in Latin America. In A. Graham [ed.], Vegetation and vegetational history of northern Latin America, 315–360. Elsevier, Amsterdam.
Gunter, L. E., G. Kochert, and D. E. Giannasi. 1994 Phylogenetic relationships of the Juglandaceae. Plant Systematics and Evolution 192: 11–29.[CrossRef][ISI]
Guo, S.-X. 1983 Late Cretaceous and Tertiary phytogeographical regions and ecological environment in China. In Commission of Palaeontological Basic Theory [ed.], Palaeontological regions of China, 164–177. Science Press, Beijing.
Hall, J. W. 1952 The comparative anatomy and phylogeny of the Betulaceae. Botanical Gazette 113: 235–270.[CrossRef]
Hardin, J. W., and J. M. Bell. 1986 Atlas of foliar surface features in woody plants, IX. Betulaceae of eastern United States. Brittonia 38: 133–144.
Hickey, L. J. 1977 Stratigraphy and paleobotany of the Golden Valley Formation (Early Tertiary) of western North Dakota. Geological Society of America Memoir 150: 1–295.
Hjelmqvist, H. 1948 Studies on the floral morphology and phylogeny of amentiferae. Botaniska Notiser, Supplement 2: 1–171.
Hutchinson, J. 1967 The genera of flowering plants, vol. 2, 124–126; 132–134. Clarendon Press, Oxford.
Jury, S. L. 1978 Betulaceae. In V. H. Heywood [ed.], Flowering plants of the world, 59–60. Oxford University Press, Oxford.
Kedves, M., and I. Uri-Kiss. 1968 Etudes comparatives sur les pollens du genre Alnus de Tertiaire de Hongrie. Acta Botanica Academiae Scientarum Hungaricae 14: 315–321.
Kikuzawa, K. 1982 Leaf survival and evolution in Betulaceae. Annals of Botany 50: 345–354.
Kuprianova, L. A. 1963 On a hitherto undescribed family belonging to the Amentiferae. Taxon 12: 12–13.[CrossRef]
———. 1965 The palynology of the Amentiferae, 118–158. Academy of sciences of the USSR, The Komarov Botanical Institute (Russian).
Li, P.-C., and S.-X. Cheng. 1979 Betulaceae. In K.-Z. Kuang and P.-C. Li [eds.], Flora Republicae Popularis Sinicae 21: 44–137. Science Press, Beijing (Chinese).
Maggia, L., and J. Bousquet. 1994 Molecular phylogeny of actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia. Molecular Ecology 3: 459–467.
Manchester, S. R. 1999 Biogeographical relationships of North American Tertiary floras. Annals of the Missouri Botanical Garden 86: 472–522.[CrossRef][ISI]
———, and Z.-D. Chen. 1996 Palaeocarpinus aspinosa sp. nov. (Betulaceae) from the Paleocene of Wyoming, USA. International Journal of Plant Sciences 157: 644–655.[CrossRef]
———, and ———. 1998 A new genus of Coryloideae (Betulaceae) from the Paleocene of North America. International Journal of Plant Sciences 159: 522–532.[CrossRef]
Manchester, S. R., and P. R. Crane. 1987 A new genus of Betulaceae from the Oligocene of western North America. Botanical Gazette 148: 263–273.[CrossRef]
———, and S.-X. Guo. 1996 Palaeocarpinus (extinct Betulaceae) from northwestern China: new evidence for Paleocene floristic continuity between Asia, North America and Europe. International Journal of Plant Sciences 157: 240–246.[CrossRef]
Manos, P. S. 1997 Systematics of Nothofagus (Nothofagaceae) based on rDNA spacer sequences (ITS): Taxonomic congruence with morphology and plastid sequences. American Journal of Botany 84: 1137–1155.[Abstract]
———, K. C. Nixon, and J. J. Doyle. 1993 Cladistic analysis of restriction site variation within the chloroplast DNA inverted repeat region of selected Hamamelididae. Systematic Botany 18: 551–562.[CrossRef][ISI]
———, and K. P. Steele. 1997 Phylogenetic analyses of "higher" Hamamelididae based on plastid sequence data. American Journal of Botany 84: 1407–1419.[Abstract]
Martin, P. S., and B. E. Harrell. 1957 The Pleistocene history of temperate biotas in Mexico and eastern United States. Ecology 38: 468–480.
Metcalfe, C. R., and L. Chalk. 1950 Anatomy of the dicotyledons, vol. 2, 1302–1309. Clarendon Press, Oxford.
Miki, A. 1977 Late Cretaceous pollen and spore floras of northern Japan: composition and interpretation. Journal of the Faculty of Science, Hokkaido University, Ser. IV. Geology and Mineralogy 17: 399–436.
Morgan, D. R., and D. E. Soltis. 1993 Phylogenetic relationships among members of Saxifragaceae sensu lato based on rbcL sequence data. Annals of the Missouri Botanical Garden 80: 631–660.[CrossRef][ISI]
Muller, J. 1981 Fossil pollen records of extant angiosperms. Botanical Review 47: 1–142.
Olmstead, R. G., H. J. Michaels, K. M. Scott, and J. D. Palmer. 1992 Monophyly of the Asteridae and identification of their major lineages inferred from DNA sequences of rbcL. Annals of the Missouri Botanical Garden 79: 249–265.
Oltz, D. F. 1969 Numerical analyses of palynological data from Cretaceous and early Tertiary sediments in east central Montana. Palaeontographica B 128: 90–166.
Prantl, K. 1894 Betulaceae. In A. Engler and K. Prantl [eds.], Die Natürlichen Pflanzenfamilien, 3 (1): 38–46. Engelmann, Leipzig.
Rendle, A. B. 1925 The classification of flowering plants, vol. 2, 23–30. Cambridge University Press, Cambridge.
Savard, L., M. Michaud, and J. Bousquet. 1993 Genetic diversity and phylogenetic relationships between birches and alders using ITS, 18S rRNA, and rbcL gene sequences. Molecular Phylogenetics and Evolution 2: 112–118.[CrossRef][Medline]
Seward, A. C., and R. E. Holltum. 1924 Tertiary plants from Mull. In E. B. Bailey et al. [eds.], Tertiary and post-Tertiary geology of Mull, 67–98. HMSO Edinburgh.
Soltis, D. E., P. S. Soltis, M. T. Clegg, and M. Durbin. 1990 rbcL sequence divergence and phylogenetic relationships in Saxifragaceae sensu lato. Proceedings of the National Academy of Sciences, USA 87: 4640–4644.
