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This issue of the Annals of the Missouri Botanical Garden is devoted to advances in the Apocynaceae s.l. and is based on the symposium, “Recent Progress in the Systematics of Apocynaceae,” held at the XVII International Botanical Congress in Vienna in 2005. The collection of papers presented here spans the phylogenetic and geographic breadth of the family and includes at least one study focused on representatives from each of the five subfamilies: Rauvolfioideae, Apocynoideae, Periplocoideae, Secamonoideae, and Asclepiadoideae. The papers range from higher-level phylogenetic analyses to more narrowly defined case studies and include new results in phylogenetics, taxonomy, biogeography, pollination biology, and a pharmacophagous plant–butterfly interaction involving pyrrolizidine alkaloids, as well as a new hypothesis for the evolution of pollinia and loss of a compitum in some advanced taxa. An updated classification scheme of the Apocynaceae is presented, with one additional tribe recognized in Rauvolfioideae (the Aspidospermeae) and three in Apocynoideae (the Nerieae and Odontadenieae as well as the Baisseeae, which are elevated in rank here). In Asclepiadoideae, seven subtribes are recognized within Asclepiadeae (the Asclepiadinae, Cynanchinae, Tylophorinae, Metastelmatinae, Orthosiinae, Oxypetalinae, and Gonolobinae) and four within Ceropegieae (the Anisotominae, Leptadeniinae, Heterostemminae, and Stapeliinae). Taken together, the papers here present the most up-to-date overview of the family available at this time.
To elucidate deeper relationships within Rauvolfioideae (Apocynaceae), a phylogenetic analysis was conducted using sequences from five DNA regions of the chloroplast genome (matK, rbcL, rpl16 intron, rps16 intron, and 3′ trnK intron), as well as morphology. Bayesian and parsimony analyses were performed on sequences from 50 taxa of Rauvolfioideae and 16 taxa from Apocynoideae. Neither subfamily is monophyletic, Rauvolfioideae because it is a grade and Apocynoideae because the subfamilies Periplocoideae, Secamonoideae, and Asclepiadoideae nest within it. In addition, three of the nine currently recognized tribes of Rauvolfioideae (Alstonieae, Melodineae, and Vinceae) are polyphyletic. We discuss morphological characters and identify pervasive homoplasy, particularly among fruit and seed characters previously used to delimit tribes in Rauvolfioideae, as the major source of incongruence between traditional classifications and our phylogenetic results. Based on our phylogeny, simple style-heads, syncarpous ovaries, indehiscent fruits, and winged seeds have evolved in parallel numerous times. A revised classification is offered for the subfamily, its tribes, and inclusive genera.
A parsimony cladistic analysis based on 55 morphological characters was performed for the Cascabela Raf.–Thevetia L. species complex (Apocynaceae), including 22 terminals, sampling at least one species of each genus in Plumerieae sensu Endress and Bruyns. The consensus of the 12 most parsimonious trees (length = 164, consistency index = 0.50, retention index = 0.75) can be correlated to three previous subtribal classifications. The topology supports the monophyly of the Cascabela–Thevetia species complex, but it is not conclusive to whether Cascabela should be recognized as a genus or as a subgenus of Thevetia. Because there are two important and easy-to-diagnose characters supporting each clade (digitiform suprastaminal appendages and embryos not compressed in Cascabela; reniform fruits and segmented endocarp in Thevetia), the recognition of two genera is preferred here. Therefore, the new combination C. pinifolia (Standl. & Steyerm.) Alvarado-Cárdenas & Ochot.-Booth is proposed. Keys and synoptic descriptions for the two genera and their species are provided.
Phylogenetic relationships were reconstructed among 59 of 77 genera of subfamily Apocynoideae and exemplars of Periplocoideae, Secamonoideae, and Asclepiadoideae (collectively the APSA clade) using sequences from four regions of the chloroplast genome (trnL intron and trnL-trnF spacer, rpl16 intron, rps16 intron, matK and 3′ half of trnK intron) and 16 morphological characters. Apocynoideae are resolved as paraphyletic. The five tribes recognized within this subfamily in the classification of Endress and Bruyns are all paraphyletic or polyphyletic. Seven major clades of Apocynoideae are identified. The first three include genera classified predominantly in tribes Wrightieae and Malouetieae sensu Endress and Bruyns and form a paraphyletic grade to a crown clade. The crown clade includes four clades of Apocynoideae genera classified in tribes Apocyneae, Mesechiteae, and Echiteae together with Periplocoideae, Secamonoideae, and Asclepiadoideae; the latter three constitute the traditional Asclepiadaceae. Asclepiadaceae are resolved as polyphyletic, although the node that precludes a paraphyletic Asclepiadaceae does not have bootstrap support. The clade of Secamonoideae–Asclepiadoideae is well supported as sister to a clade of three African Apocynoideae genera (Baissea A. DC., Motandra A. DC., and Oncinotis Benth.). There is a strong correlation between geographic distribution and phylogeny among crown clade Apocynoideae. A New World clade is composed of American genera plus the predominantly Australasian Parsonsia R. Br. and Artia Guillaumin. An Asian clade is composed of Asian, Malesian, and Australasian genera plus the north temperate Apocynum L. Trachelospermum Lem. is polyphyletic with American and Asian species nested in the New World and Asian clades, respectively. The implications of this phylogeny for the evolution of pollen aggregation and mass transfer, the traits that were used to separate Asclepiadaceae from Apocynaceae s. str., are discussed.
Phylogenetic relationships within Periplocoideae (Apocynaceae s.l.) were investigated using sequence data from nuclear ribosomal DNA and two plastid regions: trnD-trnT and trnT-trnF. We included 43 ingroup taxa, representing all but three of 32 currently recognized genera. In the ITS and total evidence analyses, Phyllanthera grayi (P. I. Forst.) Venter is supported as sister to the rest of the subfamily. We identified several well-supported clades, and three of six genera represented here by more than one species (Cryptolepis R. Br., Pentopetia Decne., and Periploca L.) are supported as monophyletic. Pollinial species appear in four distinct, well-defined clades, suggesting either three or four independent origins of pollinia within the subfamily. It is most parsimonious, therefore, to view pollinia in Periplocoideae as non-homologous with those of Secamonoideae and Asclepiadoideae, a hypothesis that is supported by their structural differences.
Phylogenetic relationships between derived subfamilies of Apocynaceae s.l. as well as within the subfamily Secamonoideae have been inferred using maximum parsimony and Bayesian analyses. Characters are provided by four chloroplast sequences: matK, trnT-L and trnL-F spacers, and trnL intron. Phylogenies from both analyses show a sister group relationship between a clade of derived Apocynoideae included in the subtribe Baisseinae (tribe Apocyneae) and another clade including representatives from the Secamonoideae and Asclepiadoideae. Within the Secamonoideae, two genera, Pervillaea Decne. and Secamonopsis Jum., are strongly supported as monophyletic, whereas the monophyly of the largest genus, Secamone R. Br., remains uncertain. Palynological and morphological characters are discussed for the Malagasy Secamone in relation to one of the most parsimonious molecular trees.
Even though the species-rich genus Ceropegia L. (Apocynaceae, Ceropegieae) is convincingly characterized by its pitfall flowers, investigation of non-coding markers of chloroplast DNA (cpDNA) (trnT-L and trnL-F spacers and the trnL intron) and nuclear ribosomal DNA (nrDNA) (ITS) has shown that Ceropegia is twice paraphyletic. The 36 analyzed Ceropegia taxa scatter over a grade of seven clades. One clade is shared by Ceropegia and all Brachystelma R. Br. species investigated, making Ceropegia (without Brachystelma) paraphyletic. All endemic Madagascan Ceropegia taxa investigated and the East African C. robynsiana Werderm. share a terminal, but not further-resolved clade with the stapeliads. Thus, again, Ceropegia without the stapeliads is paraphyletic. These results are incongruent with current taxonomy. In the absence of adequate morphological, anatomical, or karyological characters supporting a taxonomic reclassification of the genus in accordance with the retrieved clades of the phylogenetic analysis, it is proposed that the current taxonomy be maintained.
Plastid sequences of trnL-F are used to estimate the age of biogeographical events in New World Asclepiadoideae. These data suggest that the subfamily arose somewhere in the Old World in the Late Eocene (40 million years ago (Ma)) and that there were at least four independent episodes of dispersal to the New World. The MOG clade, comprising Metastelmatinae, Oxypetalinae, and Gonolobinae, probably colonized South America through transoceanic dispersal from Africa at 32 Ma. The three subtribes emerged at 24 Ma, radiating 15–16 Ma. Cynanchum L. subg. Mellichampia (A. Gray) Woodson (Cynanchinae) only arrived in the New World at 24 Ma and has since diversified gradually. Asclepias L. (Asclepiadinae) probably arrived in the New World through the Bering Strait at 20 Ma, dispersing to South America before the emergence of the Isthmus of Panama. More recently, tropical Marsdenia R. Br. (Marsdenineae) probably arrived in the New World by long-distance dispersal at 16 Ma. Most diversification in New World Asclepiadoideae is estimated to have occurred during the Miocene. The synchrony of events suggests an environmental influence on the diversification of the lineages. Nevertheless, individual rates of diversification point out the importance of intrinsic factors.
A first approximation of evolutionary relationships within the Asclepiadinae (Apocynaceae: Asclepiadoideae) is inferred from two DNA data sets, from the nuclear ITS region, and from plastid trnT-L and trnL-F spacers and trnL intron. Both the subtribe as a whole and the phylogenetic radiation of largely herbaceous genera around Asclepias are monophyletic and well supported. While resolution within the Asclepias complex is limited, the lineages identified demonstrate that current generic delimitation is unsatisfactory. Asclepias should be either restricted to New World members of the subtribe or expanded to encompass the entire radiation. In the African species, it is shown that, although the corona is taxonomically important for recognizing species, it can be misleading as an indicator of phylogenetic relationship. Vegetative similarities often prove a more reliable guide, but more detailed studies are needed to refine these lineages and to detect morphological characters to aid in their practical recognition.
Most genera of the subfamily Asclepiadoideae (i.e., 29 genera) can be found in the southeastern Brazilian region. Among these, the most representative is Oxypetalum R. Br., with 71 taxa (including specific and infraspecific). In Rio de Janeiro State, there are 25 taxa of Oxypetalum that are climbers, with the exception of O. patulum E. Fourn., which is a suberect shrub and decumbent. Most taxa from Rio de Janeiro occur in secondary Atlantic Forest, but four are from sandy coastal plain (restinga) vegetation, namely O. alpinum (Vell.) Fontella & E. A. Schwarz var. alpinum, O. pachyglossum Decne., O. banksii Schult. subsp. banksii, and O. banksii subsp. corymbiferum (E. Fourn.) Fontella & C. Valente. The latter species is restricted to restingas. Some taxa occur in high-altitude grasslands, namely O. costae Occhioni, O. lanatum Decne ex E. Fourn., O. patulum E. Fourn., O. sublanatum Malme, O. insigne (Decne.) Malme var. insigne, O. insigne var. glabrum (Decne.) Fontella & E. A. Schwarz, O. insigne var. glaziovii (E. Fourn.) Fontella & E. A. Schwarz, and O. regnellii (Malme) Malme. Four species and one subspecies are endemic to the state of Rio de Janeiro: O. costae, O. glaziovianum Loes., O. lutescens E. Fourn., O. schottii E. Fourn., and O. banksii subsp. corymbiferum. Two species are cited here as new records for the state of Rio de Janeiro: O. molle Hook. & Arn. and O. pannosum Decne. var. pannosum. The following taxa are proposed as new synonyms: O. sobralii Occhioni (= O. schottii), O. villosum E. Fourn. (= O. pachyglossum Decne.), and O. mourai Hoehne (= O. glaziovianum Loes.). Oxypetalum appendiculatum Mart., O. molle, O. pannosum var. pannosum, O. sublanatum, O. wightianum Hook. & Arn., and O. banksii subsp. banksii are widely distributed, the first five reaching Paraguay and Argentina, while O. banksii subsp. banksii is limited to Brazil (from Alagoas to Rio Grande do Sul). Lectotypifications were made for the following species: Calostigma guilleminianum Decne., Cystostemma glandulosum Silveira, Oxypetalum glaziovianum Loes., O. lanatum, O. mourai, O. pachyglossum,
Four species of Ithomiinae butterflies (Lepidoptera: Nymphalidae) were observed in nature taking up pyrrolizidine alkaloids (PAs) from withered flowers of Prestonia amabilis J. F. Morales (Apocynaceae, Echiteae) in a montane rainforest in southern Ecuador (ca. 1000 m a.s.l.). Quantitative experiments were subsequently carried out using either withered flowers or crushed roots of P. amabilis. Field trials were conducted in November 2000 at six locations in the area of the Reserva Biológica San Francisco (1800–2000 m a.s.l., ca. 15 km from the first site) where P. amabilis was not known to occur. A total of 40 specimens of 10 species of the Ithomiinae butterflies and 40 specimens of eight species of Arctiidae moths were quantitatively sampled. While the first group showed a clear preference for baits with withered flowers, the latter preferred the crushed roots. In total, 13 species of Ithomiinae were observed visiting PA sources. Eight of these 13 species have no previous records of pharmacophagy for PAs. Within the Ithomiinae, there is evidence of phylogenetic difference in attraction, with a noticeably high proportion of recorded species belonging to the Napeogenini. Analysis of plant material by gas chromatography–mass spectrometry revealed the presence of two novel retronecine monoesters of the lycopsamine type, tentatively identified as 5′-demethyllycopsamine (ideamine A) and 5′-demethylisolycopsamine or one of its diastereoisomers. The highest PA levels were found in flowers of P. amabilis (0.13%, dry weight basis), followed by roots (0.075%) and leaves (0.044%). In flowers, ideamine A accounted for 84% of total PAs, whereas roots contained ideamine A (53%) and 32% of its 3′-acetyl ester. We suggest that Prestonia R. Br. may have served as an ancestral source of PAs in the evolution of pharmacophagous behavior in the Ithomiinae.
The demonstration of postzygotic self-incompatibility in Asclepias L. prompted us to reconsider explanations for several unusual features of the Apocynaceae. With such late-acting self-incompatibility, mixed loads of self- and cross-pollen can be extremely wasteful by causing abortion of whole fruits and consequent wastage of both cross-pollen and cross-fertilized ovules. We contend that the evolution of pollinia and loss of carpel fusion in certain Apocynaceae represent adaptations to prevent or compensate for these negative effects of mixed pollen loads. Trends in the agglutination of pollen can be seen in the tetrads of Apocynum L., which are transported on sticky band-like translators; the masses of tetrads of Periplocoideae, which are deposited onto the sticky scoop portion of a spoon-like translator; the pollinia of Secamonoideae, which have a clip-like translator but no outer covering; and the pollinia of Asclepiadoideae, which are completely enclosed by a waxy outer covering. In many genera of the Rauvolfioideae, the ovary is syncarpous, but in most Apocynoideae and all Periplocoideae and Secamonoideae, the gynoecium consists of two carpels that are free in the ovule-bearing region but fused in the upper region to produce a compitum, which enables pollen placed on one stigmatic area to supply pollen tubes to both ovaries. In at least some Asclepiadoideae, however, a compitum is lacking, although postgenital fusion between the carpel apices still takes place. Parallel trends in pollen delivery and receipt also occur in taxa from other angiosperm families in which late-acting self-incompatibility systems have been implicated.
Apocynaceae have a precise pollination mechanism. However, broad pollinator assemblages, including several insect orders, have often been recorded. We test how the corolla tube length and operative width required for effective release of the pollination mechanism could restrict the pollinator assemblage in putatively hawkmoth-pollinated Apocynaceae that differ in flower depth. If corolla tube length were effective in filtering pollinators, a broader pollen vector assemblage would be expected in short-flowered species. For this to occur, the operative width of the pollinating apparatus would be additionally expected not to be specific to any particular pollinator. Alternatively, if the pollination mechanism were to have any effect in the exclusion of pollinators, access to short flowers would be expected to be limited by proboscis width rather than length. Pollination of three species in the Apocynaceae was studied in seven populations through direct observations and palynological analysis of hawkmoths. Proboscis widths of hawkmoths carrying and not carrying pollen were compared with operative floral width as measured by proboscis analogues of different diameters that could successfully release the pollination mechanism. Species studied were exclusively hawkmoth pollinated. Pollen was always attached to pollinator proboscides, either near the base or on the apical half. The long-tongued hawkmoth species Manduca sexta (L.) was the major pollinator of Mandevilla longiflora (Desf.) Pichon and Mandevilla petraea (A. St.-Hil.) Pichon. Surprisingly, another long-tongued species, Manduca tucumana (Rothschild & Jordan), was the main pollinator of the short-flowered Mandevilla laxa (Ruiz & Pav.) Woodson. Here, the operative flower width was a decisive factor restricting the pollinator spectrum to hawkmoths with proboscides narrow enough to release the pollination apparatus. Short-tongued hawkmoths, which also have wider proboscides, cannot release the pollination mechanism. In M. petraea, the operative length, and not the operative width, restricts the pollinator assemblage. Thus, two different plant strategies were observed to restrict the pollinator spectrum: floral tube length and the operative width of the pollination mechanism.
Plant-pollinator interactions constitute one of the most widely recognized mutualisms, yet most investigations focus on single species or specialized pollinators. We used multiple measures to evaluate the efficiency and effectiveness of a diverse assemblage of pollinators on three co-flowering species: Asclepias syriaca L., A. incarnata L., and A. verticillata L. Hymenopterans exceeded other insects in their prevalence as major pollinators, but most did not vary significantly among plant species in the number of flowers visited or in visit duration per plant, except for native Bombus griseocollis. Significant variation in visit duration was also uncommon among insects foraging on a single taxon, except for Apis mellifera, which foraged longer on plants of A. syriaca than native hymenopterans and lepidopterans. Among the hymenoptera, bumblebees, carpenter bees, and wasps visited more plants per foraging bout, respectively, on A. syriaca, A. incarnata, and A. verticillata. Insect fidelity also varied seasonally and among plant species. Thus, honeybees, lepidopterans, and sphecid wasps foraged with greater relative constancy on A. syriaca, A. incarnata, and A. verticillata, respectively. All bees and wasps carried more pollinaria of A. incarnata and A. verticillata than of the larger-flowered A. syriaca, but most insects had higher inferred pollinium transfer rates on A. syriaca than on its congeners, especially sphecid wasps. Overall, the actions of pollinators were individualistic and indices of pollinator effectiveness based on pre-contact foraging versus vector pollinium loads were not strongly congruent. Our results highlight the need for new and creative approaches to studying the role of generalized pollination systems in the origin and maintenance of sympatrically flowering species.
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