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    Dark-centred umbels in Apiaceae: diversity, development and evolution
    (Oxford Univ Press, 2023) Classen-Bockhoff, Regine; Celep, Ferhat; Ajani, Yousef; Frenken, Lisa; Reuther, Kerstin; Dogan, Musa
    The wild carrot (Daucus carota) is famous for its dark flowers in the umbel centre. Several studies have been conducted to figure out their functional significance, but the evolution of the dark centre remains an enigma. In the present paper, we consider all known apioid species with dark-centred umbels to get a deeper understanding of their biology and evolution. Based on herbaria studies, literature and field work, we reconstructed the distribution area of 10 species (7 genera, 6 clades) of Apiaceae-Apioideae. To recognize homology of the dark structures, developmental studies were conducted in Artedia squamata and Echiophora trichophylla Field studies included architecture, flower morph distribution (andromonoecy) and flowering sequence within the plants, abundancy and behaviour of umbel visitors and preliminary manipulation experiments (removal/adding of dark structures). The dark structures are not homologous to each other. In the Daucus alliance, central flowers or umbellets are conspicuous, whereas in other species dark brush-like (A. squamata) or club-shaped structures (Dicyclophora persica, Echinophora trichophylla, Tordylium aegyptiacum, T. cappadocicum) develop from a naked receptacle. Species are andromonoecious, have a modular architecture and flower in multicyclic protandrous sequence. Among the many umbel visitors, beetles were the most abundant group. Only visitors found on umbels in both flowering phases were recognized as possible pollinators. Manipulation experiments indicated that the dark structures influence the behaviour of some, but not all umbel visitors. In Echinophora trichophylla, a massive gall infection was observed. It is evident that the dark structures evolved several times in parallel. The brush- and club-shaped structures are interpreted as the results of mutations affecting umbel development. Dark umbel centres are most likely stabilized by selection due to their general adaptive function. Their appearance in an area known as a hotspot of beetle pollination gives rise to the assumption that they may act as beetle marks. The wild carrot is famous for its red flower in the umbel centre. The function of this flower has been discussed since the time of Darwin. Experiments have led to the general conclusion that it is adaptive addressing at least part of the unspecialized visitors and pollinators. We show that Daucus carota is not the only species with dark umbel-centres. At least 10 apioid species from 7 genera and 6 clades have conspicuous dark structures in their umbels. It is evident that the morphologically diverse structures evolved in parallel. Some receptacle structures appear to be inherited mutations linked with the peculiarities of the umbel meristem. As the diversity centre of the species with dark-centred umbels is SW Asia, an area known as a hotspot of beetle pollination, we speculate that the dark umbel centres may act as beetle marks not only but primarily attracting beetles as pollinators.
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    An expanded molecular phylogeny of Plumbaginaceae, with emphasis on Limonium (sea lavenders): Taxonomic implications and biogeographic considerations
    (Wiley, 2018) Koutroumpa, Konstantina; Theodoridis, Spyros; Warren, Ben H.; Jimenez, Ares; Celep, Ferhat; Dogan, Musa; Conti, Elena
    Plumbaginaceae is characterized by a history of multiple taxonomic rearrangements and lacks a broad molecular phylogenetic framework. Limonium is the most species-rich genus of the family with ca. 600 species and cosmopolitan distribution. Its center of diversity is the Mediterranean region, where ca. 70% of all Limonium species are endemic. In this study, we sample 201 Limonium species covering all described infrageneric entities and spanning its wide geographic range, along with 64 species of other Plumbaginaceae genera, representing 23 out of 29 genera of the family. Additionally, 20 species of the sister family Polygonaceae were used as outgroup. Sequences of three chloroplast (trnL-F, matK, and rbcL) and one nuclear (ITS) loci were used to infer the molecular phylogeny employing maximum likelihood and Bayesian analyses. According to our results, within Plumbaginoideae, Plumbago forms a non-monophyletic assemblage, with Plumbago europaea sister to Plumbagella, while the other Plumbago species form a clade sister to Dyerophytum. Within Limonioideae, Ikonnikovia is nested in Goniolimon, rejecting its former segregation as genus distinct from Goniolimon. Limonium is divided into two major clades: Limonium subg. Pteroclados s.l., including L. sect. Pteroclados and L. anthericoides, and L. subg. Limonium. The latter is divided into three well-supported subclades: the monospecific L. sect. Limoniodendron sister to a clade comprising a mostly non-Mediterranean subclade and a Mediterranean subclade. Our results set the foundation for taxonomic proposals on sections and subsections of Limonium, namely: (a) the newly described L. sect. Tenuiramosum, created to assign L. anthericoides at the sectional rank; (b) the more restricted circumscriptions of L. sect. Limonium (= L. sect. Limonium subsect. Genuinae) and L. sect. Sarcophyllum (for the Sudano-Zambezian/Saharo-Arabian clade); (c) the more expanded circumscription of L. sect. Nephrophyllum (including species of the L. bellidifolium complex); and (d) the new combinations for L. sect. Pruinosum and L. sect. Pteroclados subsect. Odontolepideae and subsect. Nobiles.
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    Nutlet micromorphology and its taxonomic and phylogenetic significance in Salvia (Lamiaceae)
    (TAYLOR & FRANCIS LTD, 2020) Celep, Ferhat; Kahraman, Ahmet; Guerin, Greg R.; Karabacak, Ersin; Akaydin, Galip; Dogan, Musa
    Salvia (sage) is a species rich and medicinally important genus. Species-level identification is usually very difficult, particularly in closely related species. Here, we investigated nutlet micromorphological characteristics of 51 taxa belonging to S. subg. Salvia, S. subg. Sclarea and Salvia verticillata clade (S. subg. Heterosphace) by stereo binocular microscopy and scanning electron microscopy to show their taxonomic and phylogenetic value. The present study is the most comprehensive nutlet micromorphological study based on the number of taxa studied in the genus so far. The size of nutlets varies from 1.61 mm (S. verticillata subsp. verticillata) to 8.44 mm (S. albimaculata) in length, 1.02 mm (S. verticillata subsp. verticillata) to 4.20 mm (S. macrochlamys) in width. Nutlet length/width ratio ranges from 1.02 (S. bracteata and S. indica) to 3.06 (S. albimaculata). The basic shape of nutlets is elliptic, widely elliptic, circular, ovate or obovate. Five nutlet sculpturing patterns are present namely colliculate, reticulate, verrucate, rugose and foveate. The variation of surface sculpturing, nutlet shape, size, and exocarp cell shape provide useful diagnostic properties at species and subgenus level. However, nutlet micromorphological characters are of low phylogenetic value in studied Salvia species.
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    Pollination Ecology, Specialization, and Genetic Isolation in Sympatric Bee-PollinatedSalvia(Lamiaceae)
    (UNIV CHICAGO PRESS, 2020) Celep, Ferhat; Atalay, Zeynep; Dikmen, Fatih; Dogan, Musa; Sytsma, Kenneth J.; Classen-Bockhoff, Regine
    Premise of research. Previous pollination ecology studies ofSalviahave shown that there is low specialization for certain subgroups of bees and that pollinator number varies with species and locality. We studied 12Salviaspecies (three clades with different corolla morphologies and staminal lever mechanisms) that in part co-occur and coflower to examine prezygotic isolation mechanisms and the degree of specialization versus generalization in pollination ecology. Methodology. Pollinators were identified using field observations, photos, and related literature across three sites in Turkey. Video documentation of the visitation rate and the site of pollen placement on the pollinator body, morphometric measurements between flowers and pollinators, flowering time, flower color, handling time, and stigma contact ratio were analyzed. Plant-pollinator networks were constructed. Pivotal results. Mechanical, phenological, and ethological isolation occurs among sympatricSalviaspecies. A morphological fit is evident between flower tube length and the proboscis length of the main pollinators. Pollinator networks indicate that most species are ecological generalists and that only a few are specialists. Conclusions. The 12Salviaspecies, though phenotypically and functionally specialized by their zygomorphic, bilabiate flowers and bee-pollination syndrome, differ in the degree of their ecological specialization. Most of the sympatricSalviaspecies tend to be ecologically generalized, with two or more main pollinators and a few additional secondary pollinators, while a fewSalviaspecies are clearly specialized. Some floral traits (e.g., flower color, morphology, size, corolla tube length and width of the corolla tube entrance, type and size of the staminal lever mechanism, small numbers of flowers in the inflorescence), a short flowering time, and a small population size appear to be correlated with the degree of ecological specialization.