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Significance of Palynology for Phylogeny of Annonaceae: Experiments with Removal of Pollen Characters*

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Significance of Palynology for Phylogeny of Annonaceae: Experiments with Removal of Pollen Characters* See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/226945879 Significance of palynology for phylogeny ofAnnonaceae: Experiments with removal of pollen characters Article in Plant Systematics and Evolution · March 1997 DOI: 10.1007/BF00987945 CITATIONS READS 34 116 2 authors, including: James A. Doyle University of California, Davis 165 PUBLICATIONS 10,951 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Fossils and seed plant phylogeny View project early angiosperms View project All content following this page was uploaded by James A. Doyle on 27 April 2017. The user has requested enhancement of the downloaded file. Plant P1. Syst. Evol. 206:133-159 (1997) Systematics and Evolution © Springer-Verlag 1997 Printed in Austria Significance of palynology for phylogeny of Annonaceae: experiments with removal of pollen characters* JAMES A. DOYLE and ANNICKLE THOMAS Received July 12, 1996; in revised version December 11, 1996 Key words: Magnoliales, Annonaceae. - Palynology, phylogeny, cladistics. Abstract: Phylogenetic analyses based on morphology place Anaxagorea and other taxa with granular monosulcate pollen, as in other Magnoliales, at the base of Annonaceae. Taxa with columellar tetrads, granular tetrads, and inaperturate monads form a derived clade. To test the systematic importance of palynology, we analyzed the data set with pollen characters removed. The result was lowei" resolution and a different rooting of the family, between Uvariopsis and other groups with columellar tetrads. Anaxagorea and other monosulcates are higher in the tree, implying that granular monosulcate pollen, laminar stamens, and irregular endosperm ruminations are reversals. This rooting is highly unparsimonious when pollen characters are included, and only weakly supported over the Anaxagorea rooting when pollen is excluded. Together with preliminary molecular analyses, these experiments confirm the special value of palynology in systematics of Annonaceae. Palynology has played a major role in attempts to clarify higher-level relation- ships in Annonaceae, the largest family of primitive angiosperms ("Magnolii- dae"). Classification of Annonaceae has long been unstable, with little agree- ment on basal relationships and few generally accepted major subgroups. For example, FRIES (1959) proposed many groups of genera and sorted most of them (except the aberrant neotropical genus Tetrameranthus and the parasyn- carpous genera Monodora and Isolona) into the tribes Uvarieae and Unoneae, based on imbricate vs. valvate petals, but he acknowledged exceptions to this distinction in both tribes. In the first comprehensive palynological study, WALKER (1971), using light and scanning electron microscopy, divided the family into three informal subfamilies and seven tribes. He argued that the most primitive group is the Malmea tribe, with single monosulcate pollen grains and an exine with columellar infratectal structure, and he recognized independent trends to tetrad * This paper is dedicated to emer. Univ.-Prof. Dr FR1EDRICH EHRENDORFERon the occasion of his 70th birthday 134 J.A. DOYLE 8,: A. LE THOMAS: pollen in his Fusaea and Annona subfamilies. LE THOMAS & LUGARDON (1974, 1976; see also LE THOMAS 1980/1981), using transmission electron microscopy (TEM), found that monosulcate and other taxa that WAL~R (1971) called "microtectate" have granular infratectal structure, which they considered primitive based on its occurrence in other magnoliids and gymnosperms. Important TEM data have also been provided by HESSE & al. (1985), WAnA (1985, 1988), and WAHA & MO~WETZ (1988). In DOYLE & LE THOMAS (1994), we undertook to test these ideas by means of a cladistic analysis of Annonaceae, based on 11 pollen characters and 68 other micro- and macromorphological characters, and using other Magnoliales as out- groups. In selecting taxa of Annonaceae, we attempted to obtain a global sampling of major groups, while limiting our attention to taxa in which exine structure is known. This led to a certain bias in favor of African taxa, which are best studied with TEM. In general, this analysis confirmed the views of WALKER (1971) and LE THOMAS (1980/1981) concerning pollen evolution. The Asian-American genus Anaxagorea, with granular monosulcate pollen, was basal (i.e. the sister group of all other Annonaceae), followed by four small genera with similar pollen, the ambavioids. Tetrads originated in two main lines: the xylopioids (part of WALKZR'S Fusaea subfamily), in which exine structure remains granular, and the a n n o n o i d s (WALKER'SAnnona subfamily), where it becomes columellar. The xylopioids were linked with the u v a r i o i d s, which have granular inaperturate pollen; the annonoids, with Artabotrys, which has columellar single grains with a reduced aperture. The palynologically diverse genus Polyalthia was polyphyletic, with members scattered among other taxa with similar pollen. Other important trends were a shift to columellar monosulcate pollen in the m almeoids (WALKER'S Malmea tribe) and multiple origins of sulculate pollen. Many of the groups recognized by VAN SETTEN & KOEK-NOORMAN(1992) based on fruit and seed characters are monophyletic or paraphyletic on these trees. Subsequent studies extended or modified aspects of this analysis. LE THOMAS & al. (1994) described the ultrastructure of Fusaea and Duguetia and discussed the relationships of these and other pseudosyncarpous genera, which formed a clade within the uvarioids. LE THOMAS & DOYLE (1996) compared the cladistic results with geographic distributions in order to reconstruct the geographic history of the family. In a discussion of the phylogenetic position of African Annonaceae, DOYLE & LE THOMAS (1995) added two more African genera, Afroguatteria and Mkilua, and rescored some characters based on more recent information. The most important change (a result of a shift of the echinate Monanthotaxis group from the xylopioid line into the uvarioids, linked with Uvaria via Afroguatteria) was that the annonoid and xylopioid tetrad groups and the inaperturate uvarioids all formed a single clade. Since the Annona group and the other "annonoids" with columellar tetrads formed a basal paraphylefic group relative to the xylopioids and uvarioids, we extended the term annonoids to this whole clade. Most recently, molecular analyses by VAN ZUILEN(1996) and P. BYGRAVEand M. W. CHASE (pers. comm.) have provided an independent source of evidence on phylogeny of Annonaceae. These studies differ in the genes studied, the taxa included, and the precise arrangement of groups, but they both confirm the basal Palynology and phylogeny of Annonaceae 135 position of Anaxagorea and the conclusion that Artabotrys and the groups with tetrads and inaperturate single grains form a clade. The fact that pollen characters often define major clades and are generally consistent with other characters (as discussed in detail by DOYLE & LE THOMAS 1994, 1995, and LE THOMAS & al. 1994) indirectly supports the view that palynology is of major importance in systematics of Annonaceae, as palynologists have argued for many other groups (e.g., WALI~R & DOYLE 1975, NowIc~ & SKVARLA 1979). The present study is intended to provide a more direct empirical test of the relative systematic value of pollen and other characters, by comparing trees derived from the whole data set with trees based on a data set from which pollen characters have been removed. We undertook this exercise in response to a question by A. A. ANDE~ERG (pers. comm.), who asked if we would have obtained the same results if we had not included pollen characters. For these experiments, we have used a new version of our data set, presented in DOYLE & LE THOMAS (1996), which incorporates a considerable number of changes in delimitation of taxa and character analysis, based especially on VAN HEUSDEN'S (1992) monograph on floral morphology and recent work on relationships within groups. Detailed justification and documentation of character definitions and scoring and implications of the results for evolution of the entire spectrum of characters may be found in DOYLE & LE THOMAS (1996). Data and analyses Our "complete" data set (Appendix; DOYLE & LE THOMAS 1996) includes 42 taxa of Annonaceae and 79 characters, 51 of which are binary and 28 multistate, requiring a minimum of 113 character state changes for the whole data set. Most terminal taxa are genera, others groups of clearly related genera, or, in the variable genus Polyalthia, four palynologically homogeneous infrageneric groups. In some cases, we dealt with variation within groups by scoring them as uncertain (e.g., 0/1); in other cases, where there is evidence on internal relationships, we assumed that one or another state is basic. Multistate characters are unordered, except in 10 cases where there is a clear basis for ordering (e.g., pollen size, chromosome number). In continuous characters, we defined states in terms of average rather than extreme numbers and attempted to set limits between states at natural gaps in the distribution of measures. When two or more potential states often co-occur within taxa (e.g., leaf epidermal crystals), we tried to combine related states in a way that reduces the number of uncertain (polymorphic) scorings. Among the most important modifications, we replaced the character of (maximum) number of monocarps in the fruit stage (documented by VAN SETTEN ~ KOEK-NOORMAN 1992) with (average)
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