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Is Persea (Lauraceae) Monophyletic? Evidence from Nuclear Ribosomal ITS Sequences

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Is Persea (Lauraceae) Monophyletic? Evidence from Nuclear Ribosomal ITS Sequences TAXON 58 (4) • November 2009: 1153–1167 Rohwer & al. • Is Persea monophyletic? Is Persea (Lauraceae) monophyletic? Evidence from nuclear ribosomal ITS sequences Jens G. Rohwer1, Jie Li2, Barbara Rudolph1, Sabrina A. Schmidt1, Henk van der Werff 3 & Hsi-wen Li2 1 Biozentrum Klein Flottbek und Botanischer Garten, Universität Hamburg, Ohnhorststr. 18, 22609 Hamburg, Germany. [email protected] (author for correspondence) 2 Laboratory of Plant Phylogenetics and Conservation Biology, Xishuangbanna Tropical Botanical Garden, The Chinese Academy of Sciences, 88 Xuefu Rd., Kunming, Yunnan 650223, P.R. China 3 Missouri Botanical Garden, P.O.Box 299, St. Louis, Missouri 63166-0299, U.S.A. The delimitation of genera within the Persea group (Lauraceae) has always been controversial. In an attempt to resolve the phylogenetic lines within this group, we analyzed ITS sequences of 61 species of the Persea group (Lauraceae) and 30 other species of Lauraceae. Several of the traditional genera or subgenera form well-supported groups, viz., Persea subg. Eriodaphne, Machilus, Persea subg. Persea, and Alseodaphne including Dehaasia. The included species of Phoebe form two clades that are unresolved with respect to Alseodaphne. However, Persea subg. Eriodaphne (together with the Macaronesian Apollonias barbujana) forms one of the clades of an unresolved basal trichotomy within the Persea group, whereas Persea subg. Persea is well supported as member of an oth- erwise Asian clade including Alseodaphne and Phoebe. This indicates that Persea, as currently circumscribed, is not monophyletic. The affinities of the Macaronesian Persea indica are clearly American rather than Asian. KEYWORDS: ITS, Lauraceae, neotropics, paleotropics, Persea group, phylogeny group. The species in this group have paniculate-cymose INTRODUCTION inflorescences, in which the lateral flowers of a cyme are The Persea group, with about 400 to 450 species, strictly opposite. In most species the staminodes of the is a subset of the Lauraceae, consisting of the currently fourth androecial whorl are distinct, often with a glandular often recognized genera Alseodaphne Nees, Apollonias head. The fruit is not seated in a cupule, but sometimes Nees, Dehaasia Blume, Machilus Nees, Nothaphoebe on a swollen pedicel. Blume, Persea Mill. and Phoebe Nees. Most of them are Recent molecular studies confirmed that the Per- mainly distributed in the tropics to subtropics of Asia, sea group (excluding Caryodaphnopsis) is monophy- while Persea has about 90 species in subtropical to tropi- letic (Rohwer, 2000; Chanderbali & al., 2001; Rohwer cal America. Apollonias and Persea each have one species & Rudolph, 2005), but the generic delimitation in the in the Macaronesian Islands (Canary Islands and Madeira, group has always been controversial. Bentham (1880) Persea indica also on the Azores). The genus Mutisioper- treated Alseodaphne, Nothaphoebe and Phoebe as sec- sea, described by Kostermans (1993) to accommodate a tions within Persea (keeping Machilus separate), whereas number of American species previously placed in Persea Kostermans (1957) placed Alseodaphne, Machilus and subg. Eriodaphne Nees, so far did not gain widespread Nothaphoebe (plus Caryodaphnopsis, see above) in the acceptance (see van der Werff, 2002). synonymy of Persea (keeping Phoebe separate). Later, The Persea group was first recognized almost in however, he reinstated Alseodaphne and Nothaphoebe its present circumscription by Rohwer (1993, as Persea (Kostermans, 1973a), as well as Caryodaphnopsis (Kos- subgroup) based on morphological evidence, except for termans, 1974), but he retained Machilus within Per- the explicitly provisional inclusion of the aberrant genus sea. Other authors (e.g., Li & al., 1984) continued to use Caryodaphnopsis Airy-Shaw. The group largely cor- Machilus as an accepted genus. Rohwer (1993) followed responds to Kostermans’ (1957) subtribe Perseineae of Kostermans in treating Machilus as a subgenus of Persea, tribe Perseeae, except that Kostermans referred the gen- but he remarked that the Macaronesian species, Persea era with disporangiate anthers, Apollonias and Dehaasia, indica, was “possibly misplaced in this genus”, and that to the subtribe Beilschmiediineae, which also included the two species of Apollonias (one from Macaronesia, several genera now known to belong to other evolution- the other from India) were “probably independently de- ary lineages. All non-cupulate genera of van der Werff rived from Phoebe.” Van der Werff (2001) also used the & Richter’s (1996) Perseeae are members of the Persea generic name Persea in a sense including Machilus. He 1153 Rohwer & al. • Is Persea monophyletic? TAXON 58 (4) • November 2009: 1153–1167 placed Nothaphoebe in the synonymy of Alseodaphne tepals reaching only slightly more than half the length of because none of the differences between them appeared the inner tepals. The same is found in cultivated Persea to be discontinuous and concepts of the two genera had americana (P. subg. Persea ; Fig. 1A, B), which is often always been rather vague. In addition, he expressed doubts keyed out using statements like “tepals (sub)equal.” There- about the delimitation between Persea and Phoebe, and fore, this character should be used only with caution for between Alseodaphne and Dehaasia. the delimitation of genera. On the basis of their disporangiate anthers, Apollonias The fate of the perianth in fruit (2) appears to be a and Dehaasia used to be kept separate from the other more reliable character, but it isn’t entirely discontinuous, genera (with predominantly tetrasporangiate anthers), either. The tepals are usually described as deciduous in often at different infrafamilial levels varying from sub- fruit in Alseodaphne, Dehaasia, and Persea subg. Per- tribe (Kostermans, 1957) to subfamily (Pax, 1889). On sea, whereas they are persistent in Apollonias, Machilus, the other hand, Kostermans (1973b) noted that “Dehaasia Phoebe, and Persea subg. Eriodaphne (Fig. 1C–E). In and Alseodaphne are very closely related; the only differ- Nothaphoebe, they are described as either deciduous or ence is the number of anther cells, 2 in the former, 4 in persistent, but small and inconspicuous. Indurate (i.e., the latter.” Van der Werff (2001) came to the same con- more or less lignified) tepals in fruit are characteristic clusion. This statement also receives some support from of Apollonias, Phoebe and Persea subg. Eriodaphne. In an analysis based on trnK intron sequences (Rohwer & Apollonias (Fig. 1D) and Phoebe they are appressed to Rudolph, 2005), in which Alseodaphne perakensis (Gam- the base of the fruit, whereas in Persea subg. Eriodaphne ble) Kosterm. and Dehaasia cuneata (Blume) Blume form they are often (but not always, see Fig. 1C) spreading. The a strongly supported clade. tepals of Machilus are sometimes slightly enlarged but not Kopp (1966) already accepted species with dispo- significantly thickened in fruit (Fig. 1E), and in herbarium rangiate and with tetrasporangiate anthers within Persea specimens they are often shriveled and reflexed. These subg. Eriodaphne, sometimes as closest relatives to one differences, however, are not as clear as they may seem. another. She also documented different numbers of pollen Quite often, the tepals do not fall off as a whole, but their sacs in the different androecial whorls within the same bases persist while their tips break off. Then it depends flower, and even a variable number of pollen sacs in the on the relative size of the deciduous and the persistent stamens of the third whorl of P. urbaniana Mez. In re- parts, as well as on the size of the fruit, whether they are cent years it has become increasingly clear that number regarded as persistent (as in Apollonias barbujana ; Fig. of pollen sacs is not sufficient to distinguish genera, and 1D) or as deciduous (as in Persea americana ; Fig. 1F, may sometimes vary within species (Rohwer & al., 1991; where the tepal bases persist as well). In addition, a few Rohwer, 1993; Li & Christophel, 2000; van der Werff, species in each of the larger genera do not conform to the 2001; Chanderbali, 2004; Li & al., 2004). most frequent pattern of their group. In Persea, e.g., most Other important characters for generic delimitation species have unequal tepals persistent in fruit (= P. subg. in the Persea group are (1) the structure of the perianth Eriodaphne), while a few have (supposedly) equal to (sub) (equal vs. unequal tepals) and (2) its fate in fruit (decidu- equal tepals deciduous in fruit (= P. subg. Persea) or equal ous vs. persistent; indurate or not; reflexed, spreading or tepals persistent in fruit (e.g., P. albida Kostermans and clasping the base of the fruit), as well as (3) the structure P. rigens C.K. Allen); one species (Persea julianae van of the pedicel in fruit (see Kostermans, 1957; Rohwer, der Werff) has strongly unequal tepals deciduous in fruit 1993; van der Werff, 2001). (van der Werff, 1989, 2001, 2002; Rohwer & al., 1991). The tepals (1) are supposed to be equal or subequal The pedicel (3) changes relatively little during fruit in Apollonias, Machilus, Phoebe and Persea subg. Per- development in most genera, except that it usually gets sea, while they are described as more or less unequal in somewhat stronger, depending on the size of the fruit. Alseodaphne, Dehaasia, Nothapoebe and Persea subg. Thickened, fleshy, and vividly colored fruit pedicels are Eriodaphne. However, this is by no means a sharp discon- characteristic of Alseodaphne and Dehaasia,
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