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Moraceae) and Allied Genera, Including a Revised 2 Subgeneric System 3 4 Running Title: Phyogenomics of Brosimum (Moraceae) 5 6 ELLIOT M

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Moraceae) and Allied Genera, Including a Revised 2 Subgeneric System 3 4 Running Title: Phyogenomics of Brosimum (Moraceae) 5 6 ELLIOT M bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098566; this version posted May 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Phylogenomics of Brosimum Sw. (Moraceae) and allied genera, including a revised 2 subgeneric system 3 4 Running title: Phyogenomics of Brosimum (Moraceae) 5 6 ELLIOT M. GARDNER1,2,3,4,*, LAUREN AUDI1,2,5,a, QIAN ZHANG6,7,a, HERVÉ 7 SAUQUET6,8, ALEXANDRE K. MONRO9, AND NYREE J.C. ZEREGA1,2 8 9 1 Chicago Botanic Garden, Negaunee Institute for Plant Conservation Science and Action, 1000 10 Lake Cook Road, Glencoe, IL, 60022, USA 11 2 Northwestern University, Plant Biology and Conservation Program, 2205 Tech Dr., Evanston, 12 IL, 60208, USA 13 3 Singapore Botanic Gardens, National Parks Board, 1 Cluny Road, 259569, Singapore (current 14 affiliation) 15 4 Case Western Reserve University, Department of Biology, Cleveland, Ohio, USA (current 16 affiliation) 17 5 American Museum of Natural History, Sackler Institute for Comparative Genomics, 200 18 Central Park West, New York, NY 10024 19 6 Laboratoire Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, 20 Université Paris-Saclay, 91400, Orsay, France 21 7 Key Laboratory of Systematic and Evolutionary Botany, Chinese Academy of Sciences, 22 Beijing, China 23 8 National Herbarium of New South Wales (NSW), Royal Botanic Gardens and Domain Trust, 24 Sydney, Australia 25 9 Identification & Naming Department, Royal Botanic Gardens, Kew, TW9 3AE, United 26 Kingdom 27 a These two authors contributed equally. 28 * For correspondence, email [email protected] 29 30 31 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098566; this version posted May 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 32 Abstract 33 We present a phylogenomic study of Brosimum and the allied genera Trymatococcus and 34 Helianthostylis, with near-complete taxon sampling. Distributed from Mexico and the Greater 35 Antilles to the Amazon, this clade contains the underutilized crop ramón (bread nut) (Brosimum 36 alicastrum) as well as other species valued for timber or medicinal uses. Target enrichment for 37 333 genes produced a well-resolved phylogenetic tree and showed that Trymatoccocus and 38 Helianthostylis are nested within Brosimum. We present a revised subgeneric classification of 39 Brosimum based on phylogenetic and morphological considerations, including the reduction of 40 Trymatococcus and Helianthostylis to subgenera. The monophyletic subgenera can be diagnosed 41 based on stipule, pistillode, and cotyledon synapomorphies. Divergence date estimates suggest a 42 Miocene origin for Brosimum, and ancestral area reconstruction indicated that all four subgenera 43 originated and initially diversified in Amazonia before dispersing into other parts of South and 44 Central America. 45 46 47 Resumen 48 Presentamos un estudio filogenómico del género Brosimum y sus aliados, Trymatococcus y 49 Helianthostylis, y que incluye prácticamente todas las especies descritas. Su distribución va 50 desde México y las Antillas Mayores hasta el Amazonas y comprende especies como el ramón 51 (B. alicastrum), un cultivo infrautilizado, y otras especies empleadas como madera o en 52 medicina. La secuenciación masiva dirigida de 333 marcadores nucleares de copia única 53 permitió la reconstrucción de una filogenia bien resuelta, en la que se demuestra que 54 Trymatococcus y Helianthostylis están anidados en Brosimum. Presentamos, por lo tanto, una 55 clasificación revisada a nivel de especies, teniendo en cuenta los resultados moleculares y las 56 características morfológicas, y donde Trymatococcus y Helianthostylis pasan a ser subgéneros de 57 Brosimum. Estos subgéneros monofiléticos pueden ser identificados por caracteres de las 58 estípulas y de los pistilodios. 59 60 Keywords: Brosimum; Trymatoccocus; Helianthostylis; Dorstenieae; Brosimeae; Moraceae; 61 ramón; bread nut; Maya nut; phylogenetics; target enrichment; HybSeq 62 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098566; this version posted May 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 63 Introduction 64 The mulberry family (Moraceae) has approximately 1,100 species and 39 genera, with a 65 worldwide distribution and a center of diversity in the tropics. It includes economically and 66 ecologically important species such as breadfruit and jackfruit (Artocarpus J.R. Forst. & G. 67 Forst.), mulberries (Morus L.) and figs (Ficus L.). Moraceae are characterized by latex in all 68 parenchymatous tissue and tiny inconspicuous, unisexual flowers arranged in a wide variety of 69 inflorescence forms, ranging from simple spikes to condensed heads, discs and the unique fig 70 syconium. 71 While monophyly of Moraceae is not in doubt (Datwyler & Weiblen, 2004; Zerega & al., 72 2005; Zhang & al., 2011, 2019b), diverse morphology and widespread homoplasy within 73 Moraceae has made the establishment of a robust and stable sub-familial taxonomy problematic 74 (Corner, 1962; Berg, 1977, 2001; Rohwer, 1993; Clement & Weiblen, 2009; Gardner & al., 75 2020a). The most recent family-wide phylogenetic studies recognized seven tribes based on 76 molecular and morphological evidence, with inflorescence morphology most closely reflecting 77 the clades (Artocarpeae, Olmedieae, Dorstenieae, Ficeae, Maclureae, Moreae, and 78 Parartocarpeae) (Clement & Weiblen, 2009; Zerega & Gardner, 2019; Gardner & al., 2020a). Of 79 these, the Dorstenieae are particularly heterogenous, comprising species with both unisexual and 80 bisexual inflorescences ranging from mulberry-like spikes (Sloetia) to condensed heads 81 (Brosimum) or flattened discs (Dorstenia). This has led to conflicting views of phylogenetic 82 relationships within the tribe (Berg, 2001; Clement & Weiblen, 2009; Zerega & al., 2010; 83 Gardner & al., 2020a). A recent phylogenomic study of Dorstenieae, based on a target 84 enrichment approach (Zhang & al., 2019a), confirmed the monophyly of Dorstenieae, which 85 includes Brosimum together with fifteen other genera (Zerega & Gardner, 2019; Gardner & al., 86 2020a). These include members of the now-obsolete Brosimeae as well as others (Bleekrodea, 87 Broussonetia, Fatoua, Sloetia, and Sloetiopsis) that were previously assigned to Moreae. 88 89 Study system 90 Brosimum Sw. sensu Berg (Figure 1) comprises 15 neotropical species whose distribution 91 extends from Mexico and the Greater Antilles to southern Brazil. The morphology and 92 taxonomic history of the genus were most recently reviewed in detail by Berg (1972). Berg 93 (1970) united the poorly differentiated genera Brosimum, Galactodendrum, Ferolia Aubl., and 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098566; this version posted May 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 94 Piratinera Aubl. into Brosimum as currently circumscribed, based on inflorescence characters, 95 maintaining Ferolia (Aubl.) C.C. Berg as a subgenus. The genera Brosimum, Helianthostylis (2 96 spp.) and Trymatococcus (2 spp.) comprised the tribe “Brosimeae” Tréc. (Berg, 1972), later 97 included within Dorstenieae (Berg, 2001) but used here as an informal clade name. The species 98 in these three genera are all latex-producing trees, native to habitats ranging from wet to 99 seasonally dry forest. As is the case with most members of the Dorstenieae, inflorescences can 100 be bisexual (but are not always so). “Brosimeae” inflorescence morphology is unique within 101 Dorstenieae, typically consisting of a capitate inflorescence covered with many staminate 102 (“male”) flowers and one (to several) central pistillate (“female”) flower immersed in the 103 receptacle-like inflorescence axis, visible only by virtue of its exserted style (Figure 1C–D). The 104 immature inflorescence is initially covered completely by peltate bracts, which may persist in 105 fruit (Figure 1B,F). In fruit, the inflorescence axis becomes fleshy, surrounding the seed(s). Berg 106 (1970, 1972) divided Brosimum into two subgenera: subgenus Brosimum, with non-amplexicaul 107 stipules (Figure 1H) and more or less globose-capitate inflorescences, and subgenus Ferolia, 108 with fully amplexicaul stipules (Figure 1J) and often with lobed inflorescences resembling small 109 cauliflower heads. Trymatococcus and Helianthostylis closely resemble Brosimum, differing in 110 the presence of pistillodes (always lacking in Brosimum), as well as inflorescence sexuality 111 (always bisexual in Trymatococcus and always bisexual or pistillate in Helianthostylis), the 112 presence of a well-developed staminate perianth (usually vestigial or lacking in Brosimum) and 113 the number of stamens in the flower,. Helianthostylis, remarkable for its long pistillodes, 114 protruding up to 2 cm from the staminate
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