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Comparative Anatomy of the Fig Wall (Ficus, Moraceae)

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Comparative Anatomy of the Fig Wall (Ficus, Moraceae) Botany Comparative anatomy of the fig wall (Ficus, Moraceae) Journal: Botany Manuscript ID cjb-2018-0192.R2 Manuscript Type: Article Date Submitted by the 12-Mar-2019 Author: Complete List of Authors: Fan, Kang-Yu; National Taiwan University, Institute of Ecology and Evolutionary Biology Bain, Anthony; national Sun yat-sen university, Department of biological sciences; National Taiwan University, Institute of Ecology and Evolutionary Biology Tzeng, Hsy-Yu; National Chung Hsing University, Department of Forestry Chiang, Yun-Peng;Draft National Taiwan University, Institute of Ecology and Evolutionary Biology Chou, Lien-Siang; National Taiwan University, Institute of Ecology and Evolutionary Biology Kuo-Huang, Ling-Long; National Taiwan University, Institute of Ecology and Evolutionary Biology Keyword: Comparative Anatomy, Ficus, Histology, Inflorescence Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 29 Botany Comparative anatomy of the fig wall (Ficus, Moraceae) Kang-Yu Fana, Anthony Baina,b *, Hsy-Yu Tzengc, Yun-Peng Chianga, Lien-Siang Choua, Ling-Long Kuo-Huanga a Institute of Ecology and Evolutionary Biology, College of Life Sciences, National Taiwan University, 1, Sec. 4, Roosevelt Road, Taipei, 10617, Taiwan b current address: Department of Biological Sciences, National Sun Yat-sen University, 70 Lien-Hai road, Kaohsiung, Taiwan.Draft c Department of Forestry, National Chung Hsing University, 145 Xingda Rd., South Dist., Taichung, 402, Taiwan. * Corresponding author: [email protected]; Tel: +886-75252000-3617; Fax: +886-75253609. 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 29 Abstract The genus Ficus is unique by its closed inflorescence (fig) holding all flowers inside its cavity, which is isolated from the outside world by a fleshy barrier: the fig wall. The fig wall is the main structure of the fig giving its shape but the wall has also important ecological functions such as protection of fig seeds and fig wasp larvae. Nevertheless, the fig wall anatomy is poorly understood. This study aims to examine the fig wall anatomy of 22 Ficus taxa (21 species, one species having two varieties) in Taiwan in order to reveal the diversity in anatomy of the fig Draftwall. We found that these 21 fig species exhibited a great variety in fig wall anatomy, from the simplest parenchymatic wall to complex fig walls. Fig walls of 12 sampled taxa developed aerenchyma and sclerenchyma formations whereas seven taxa had fig walls containing tanniferous cells. Five anatomical types of fig walls have been identified according to the presence or absence of the different differentiated tissues. These types are distributed among the Ficus subgenera. Further studies on tissue differentiations of the fig wall should be investigated in other Ficus species as well as the ecological functions of the fig wall. Keywords: Comparative Anatomy; Ficus; Histology; Inflorescence 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 29 Botany 1. Introduction The Moraceae family comprises about 38 genera and 1180 species (Christenhusz and Byng 2016) displaying a great diversity of life history traits with few synapomorphic characters such as laticifers, anatropous ovules, and apical placentation (Sytsma et al. 2002). Among the six Moraceae tribes (Clement and Weiblen 2009), the Ficeae tribe is monogeneric with the single genus Ficus (Berg 2001) defined by a common feature: a closed inflorescence with a single tight orifice (ostiole) closed by bracts called fig (or syconium) (Berg and Corner 2005). Draft The Moraceae phylogeny shows that the Ficeae tribe is not basal and the inflorescence morphology within the Moraceae family has evolved in many directions (Clement and Weiblen 2009). This diversity is also present within the tribes. For instance, figs display many shapes from the ellipsoid figs of Ficus dammaropsis measuring about 10cm in diameter with conspicuous lateral bracts to the globose minute figs of F. caulocarpa measuring half a centimetre (Berg and Corner 2005) or to the Australian banana fig, F. pleurocarpa (Dixon 2003). In addition to the fig morphology, Ficus species are mostly famous for being pollinated by minute wasps from the Agaonidae family (Hymenoptera: Chalcidoidea) and solely by the wasps of this family. Together, the fig tree and the pollinating wasp are mutualistic partners: the fig provides oviposition sites 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 29 for the agaonid wasp which bring pollen inside the fig in order to pollinate the enclosed flowers (Kjellberg et al. 2005). This nursery pollination mutualism is targeted by many nonpollinating wasp (NPFW) species parasitizing either the fig ovules or fig wasp larvae (Bronstein 1991; Tzeng et al. 2008). These NPFWs can drastically reduce the number of seeds and pollinating wasps produced in a single fig (Cardona et al. 2013). The specificity of these NPFWs is their way to reach the fig ovules or the fig wasp larvae inside the figs. Indeed, they are laying eggs from outside the figs, using their long ovipositor (Ghara et al. 2011). They are not using the fig ostiole to penetrate the fig but pass through the fig Draft wall.The fig wall is the tissue between the ovules and the outside world (Fig. 1). The thickness of the fig wall increases during the fig development with the size of the fig (Galil et al. 1970). Moreover, some figs of Ficus erecta var. beecheyana, in Taiwan, have a fig wall thick enough to protect their flowers from nonpollinating fig wasp oviposition (Tzeng et al. 2014). Other than laticifers (Marinho et al. 2017), the anatomy of the fig wall is poorly understood. To our knowledge, the general description is “the fig wall generally parenchymatic and contains some 30-40 cell layers. Various sclerified cell layers may occur […] and contains many laticifers, tannin cells, and a vascularization” (Verkerke 1989). This general description based on information from different reviewed studies but the fig wall can contain more cell layers than in the Verkerke’s description reaching up to 48 cell layers in F. ingens in South Africa (Baijnath and Naicker 1989). 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 29 Botany One of the common feature seems to be that, when it occurs, sclerenchyma becomes a larger part of the fig wall during the fig development (Galil et al. 1970; Verkerke 1986; Baijnath and Naicker 1989) but not all the fig species have a hardened fig wall (Verkerke 1988). This statement leads to the question why some fig species have developed a hardened fig wall. Considering the cost of the NPFWs (Cardona et al. 2013) and the adaptation of these NPFWs to the oviposition through the fig wall (Ghara et al. 2011), the fig wall may be an important organ for the fig trees to manage the parasitism by NPFWs. For instance, some closely related fig species, such as F. caulocarpa and F. subpisocarpa, Draft have a very a different NPFW community (Bain et al. 2015): 20 species for F. subpisocarpa and only two species for F. caulocarpa. Then, is the fig wall of these two species very different? Another example is F. erecta var. beecheyana which can have a very thick fig wall excluding any NPFWs. What does the fig wall of F. erecta var. beecheyana consist of? And more generally, what are the fig walls made of? Other than the simple description from Verkeke’s work (1988), we have little information except that fig walls display some anatomical diversity. Moreover, what happens in dioecious fig species? In these species, the male trees bear figs with pollinating fig wasps and are the targets of many NPFWs whereas the female trees are producing only seeds and NPFWs are rarely breeding in female figs (Wu et al. 2013). If the fig wall is ecologically linked to the presence of the NPFWs, we can expect to see morphological differences 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 29 between male and female trees. Thus, this study aims to investigate the fig wall anatomy of most of the Taiwan Ficus species (21 species, one of which has two varieties, from six subgenera) and tentatively link the anatomical structures to ecological functions such as the parasitism from NPFWs. We also discuss the effect of phylogeny on the distribution of the anatomical structures within the genus Ficus. 2. Methods Draft 2.1. Fig development and reproductive biology of pollinating fig wasps The pollinating fig wasps grow as larva inside the figs and mate shortly after the eclosion of their gall (pupal case) when they are still inside their natal fig (Kjellberg et al. 2005). Only the winged female pollinating fig wasps will leave the fig to find another fig of the same species because pollinating fig wasps pollinate only one fig tree species (few exceptions to this rule have been found (Compton et al. 2009)). Once the female pollinating wasp has found a receptive fig (see below for the descriptions of fig developmental phases), it enters inside the fig to pollinate it and lay eggs. In the figs, pollinating and nonpollinating fig wasps have a very similar life cycle but, instead of entering to figs to lay eggs, NPFWs lay eggs from outside of the fig and have to penetrate 6 https://mc06.manuscriptcentral.com/botany-pubs Page 7 of 29 Botany the fig wall with their ovipositors (Weiblen et al. 2002). Based on the definition by Galil and Eisikowitch (1968), fig development is divided into five phases. The A phase (prefemale phase) is the earliest stage, in which all the flowers are immature. In the B phase (female phase), the female flowers are receptive, and pollinating fig wasps can pollinate them, thus entering the figs through the ostiole. During the C phase (interfloral phase), both the fig wasp larvae and seeds develop.
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