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Evolution and Classification of Figs (Ficus, Moraceae) and Their Close Relatives (Castilleae) United by Involucral Bracts

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Evolution and Classification of Figs (Ficus, Moraceae) and Their Close Relatives (Castilleae) United by Involucral Bracts applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Botanical Journal of the Linnean Society, 2020, 193, 316–339. With 3 figures. Downloaded from https://academic.oup.com/botlinnean/article-abstract/193/3/316/5854272 by University of Minnesota Libraries - Twin Cities user on 30 June 2020 Evolution and classification of figs (Ficus, Moraceae) and their close relatives (Castilleae) united by involucral bracts Keywords=Keywords=Keywords_First=Keywords 1 2 1,3 4 HeadA=HeadB=HeadA=HeadB/HeadA WENDY L. CLEMENT , SAM BRUUN-LUND , ALANNA COHEN , FINN KJELLBERG , 5 2,6, HeadB=HeadC=HeadB=HeadC/HeadB GEORGE D. WEIBLEN and NINA RØNSTED * HeadC=HeadD=HeadC=HeadD/HeadC 1Department of Biology, The College of New Jersey, 2000 Pennington Road, Ewing, New Jersey, NJ 08638, USA Extract3=HeadA=Extract1=HeadA 2The Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, DK 2100 REV_HeadA=REV_HeadB=REV_HeadA=REV_HeadB/HeadA Copenhagen, Denmark 3 REV_HeadB=REV_HeadC=REV_HeadB=REV_HeadC/HeadB Department of Biochemistry and Microbiology, Rutgers University, 76 Lipman Dr., New Brunswick, New Jersey, NJ 08901-8525, USA REV_HeadC=REV_HeadD=REV_HeadC=REV_HeadD/HeadC 4CEFE, CNRS, University of Montpellier, University Paul Valéry Montpellier, EPHE, IRD, 1919 Route de REV_Extract3=REV_HeadA=REV_Extract1=REV_HeadA Mende, F-34293 Montpellier Cédex 5, France BOR_HeadA=BOR_HeadB=BOR_HeadA=BOR_HeadB/HeadA 5Department of Plant Biology, University of Minnesota, 140 Gortner Laboratory, 1479 Gortner Avenue BOR_HeadB=BOR_HeadC=BOR_HeadB=BOR_HeadC/HeadB Saint Paul, Minnesota, MN 55108, USA 6 BOR_HeadC=BOR_HeadD=BOR_HeadC=BOR_HeadD/HeadC National Tropical Botanical Garden, 3530 Papalina Road, Kalaheo, Kaua’i, Hawai’i, HI 96741, USA BOR_Extract3=BOR_HeadA=BOR_Extract1=BOR_HeadA Received 4 March 2019; revised 6 September 2019; accepted for publication 29 February 2020 EDI_HeadA=EDI_HeadB=EDI_HeadA=EDI_HeadB/HeadA EDI_HeadB=EDI_HeadC=EDI_HeadB=EDI_HeadC/HeadB EDI_HeadC=EDI_HeadD=EDI_HeadC=EDI_HeadD/HeadC Figs and fig wasps are a classic example of an obligate pollination mutualism. Decades of work untangling the EDI_Extract3=EDI_HeadA=EDI_Extract1=EDI_HeadA ecology and evolution of these organisms has simultaneously contributed to development of the fields of mutualism, CORI_HeadA=CORI_HeadB=CORI_HeadA=CORI_HeadB/HeadA coevolution and plant–insect interactions at large. With > 800 species, figs (Ficus, Moraceae) are among some of the larger genera of angiosperms. Phylogenetic studies of Moraceae have supported the clade Castilleae as the CORI_HeadB=CORI_HeadC=CORI_HeadB=CORI_HeadC/HeadB sister lineage of Ficus. Compared to Ficus, Castilleae have many fewer species (60 species in 11 genera), suggesting CORI_HeadC=CORI_HeadD=CORI_HeadC=CORI_HeadD/HeadC changes in rates of diversification along these two branches. Relatively little is known about Castilleae compared to CORI_Extract3=CORI_HeadA=CORI_Extract1=CORI_HeadA Ficus, and we argue that defining the clade comprising Ficus and Castilleae, hereafter Involucrata, focuses attention on opportunities for comparative studies of pollination mutualisms and diversification rates. In this study, we define ERR_HeadA=ERR_HeadB=ERR_HeadA=ERR_HeadB/HeadA Involucrata and propose a revised classification scheme that accounts for the phylogenetic reconstruction based on ERR_HeadB=ERR_HeadC=ERR_HeadB=ERR_HeadC/HeadB the most comprehensive sampling of this group to date. Moving forward, this classification will better guide and ERR_HeadC=ERR_HeadD=ERR_HeadC=ERR_HeadD/HeadC support evolutionary, ecological and comparative pollination biology studies of this group. ERR_Extract3=ERR_HeadA=ERR_Extract1=ERR_HeadA ADDITIONAL KEYWORDS: Asperae – external transcribed spacer – Involucrata – Mixtiflores – Noyera – INRE_HeadA=INRE_HeadB=INRE_HeadA=INRE_HeadB/HeadA paralogy – phylogenetic reconstruction. INRE_HeadB=INRE_HeadC=INRE_HeadB=INRE_HeadC/HeadB INRE_HeadC=INRE_HeadD=INRE_HeadC=INRE_HeadD/HeadC INRE_Extract3=INRE_HeadA=INRE_Extract1=INRE_HeadA INTRODUCTION study of pollination mutualisms, coevolution and cospeciation (Bronstein, 1988; Herre, 1989; Herre & With at least 800 named species, Ficus L. accounts App_Head=App_HeadA=App_Head=App_HeadA/App_Head West, 1997; Lopez-Vaamonde et al., 2001; Weiblen, for more than half of the species diversity of the BList1=SubBList1=BList1=SubBList 2001; Weiblen, Yu & West, 2001; Weiblen & Bush, 2002; mulberry family, Moraceae (c. 1100 species; Clement Cook & Rasplus, 2003; Jousselin, Rasplus & Kjellberg, BList1=SubBList3=BList1=SubBList2 & Weiblen, 2009). Phylogenetic analyses of Moraceae 2003; Weiblen, 2004; Machado et al., 2005; Rønsted SubBList1=SubSubBList3=SubBList1=SubSubBList2 have strongly supported Castilleae as sister to Ficus et al., 2005; Marussich & Machado, 2007; Silvieus, SubSubBList3=SubBList=SubSubBList=SubBList based on plastid (Datwyler & Weiblen, 2004), nuclear Clement & Weiblen, 2007; Jackson et al., 2008; (Zerega et al., 2005) and morphological data (Clement SubSubBList2=SubBList=SubSubBList=SubBList Jousselin et al., 2008; Herre, Jandér & Machado, 2008; & Weiblen, 2009). Ficus has been central to advancing SubBList2=BList=SubBList=BList Cruaud et al., 2012a; Cruaud et al., 2012b; McLeish & van Noort, 2012; Conchou et al., 2014; Bain et al., 2016; *Corresponding author. E-mail: [email protected] Rodriguez et al., 2017). Ficus spp. occur in tropical and © 2020 The Linnean Society of London, Botanical Journal of the Linnean Society, 2020, 193, 316–339 316 EVOLUTION OF FICUS AND CASTILLEAE 317 subtropical regions worldwide and include trees, hemi- benefit of pollinator production. Thrips pollinating epiphytes, epiphytes, shrubs, climbers, rheophytes and Castilleae do not depend on successful pollination as lithophytes. In contrast, Castilleae are a group of 11 thrips eat pollen and mate on male inflorescences. Downloaded from https://academic.oup.com/botlinnean/article-abstract/193/3/316/5854272 by University of Minnesota Libraries - Twin Cities user on 30 June 2020 genera and 60 species of trees and shrubs with four Selective pressure on host choice also differs among fig species distributed in the Palaeotropics and 56 species and Castilleae pollination syndromes. In many species, in the Neotropics. Ficus and Castilleae diverged from foundress fig wasps lose their wings and antennae on one another at least 65 Mya (Zerega et al., 2005), entering a fig so that they cannot reach another tree, and the striking difference in contemporary species probably resulting in intense selection to discern host richness suggests differing rates of diversification. quality before host selection. Castilleae pollinators can Together, Ficus and Castilleae differ from other visit multiple inflorescences per generation with little Moraceae in having involucral bracts that subtend consequence for visiting a non-rewarding inflorescence. the inflorescences on a disc or urn-shaped receptacle. Differing selective pressures resulting from the nature In Castilleae, the involucral bracts do not completely of these pollination interactions may have impacted the enclose the inflorescence like they do in Ficus. The evolutionary trajectory of both lineages (Moe et al., 2012). positioning of these bracts has profound implications Further testing of this hypothesis requires additional for their reproductive ecology. In Ficus, the involucral study of pollination biology of Castilleae and an improved bracts form a tight pore, or ostiole, at the apex of the phylogenetic framework for Ficus and Castilleae. receptacle. Mated pollinating wasps force themselves Our current understanding of Ficus classification is through this opening into the cavity of the fig largely based on a massive Malesian revision of Ficus (syconium) where they pollinate flowers, lay eggs and initiated by Corner and completed by Berg after Corner’s usually die. Pollinator offspring emerge from galls death (Berg, 2003a, b, c, d, e, 2004a, b; Berg & Corner, inside the fig to mate and collect pollen from staminate 2005) building on earlier work (summarized in Corner, flowers before exiting in search of other receptive 1965). Berg’s classification based on morphological and figs. In contrast to the ‘cradle to grave’ relationship anatomical characters added emphasis on vegetative between figs and their pollinating wasps, Castilleae characters compared to Corner’s treatments that inflorescences are only partially enclosed by involucral focused on floral and fruit characters (Corner, 1965). bracts thereby allowing pollinators to come and go. Ultimately, Berg & Corner (2005) subdivided Ficus From the limited study of pollination in Castilleae, into six subgenera: (1) Pharmacosycea (Miq.) Miq. wind (Osmaston, 1965; Croat, 1978) and insect (Sakai, (monoecious); (2) Urostigma (Gasp.) Miq. (monoecious) Kato & Nagamasu, 2000; Zerega, Mound & Weiblen, (3) Ficus (gyno-dioecious); (4) Sycidium (Miq.) Mildbr. 2004) pollination syndromes are present. As in Ficus, & Burret (gyno-dioecious); (5) Synoecia (Miq.) Miq. insect-pollinated Castilleae are also involved in brood- (gyno-dioecious) and (6) Sycomorus (Gasp.) Miq. (gyno- site pollination mutualisms in which pollinators mate dioecious and monoecious). Subgenera Pharmacosycea, and lay eggs in the inflorescences. Pollination by thrips Sycidium, Sycomorus and Urostigma are distributed has been documented for two species of Castilleae, from the Pacific to West Africa, with subgenera Antiaropsis decipiens K.Schum. (endemic to New Pharmacosycea and Urostigma additionally including Guinea; Zerega
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