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Mesoamerica Is a Cradle and the Atlantic Forest Is a Museum of Neotropical Butterfly

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Mesoamerica Is a Cradle and the Atlantic Forest Is a Museum of Neotropical Butterfly bioRxiv preprint doi: https://doi.org/10.1101/762393; this version posted February 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 Title Page 2 Running title: Evolutionary history of Brassolini butterflies 3 Title: Mesoamerica is a cradle and the Atlantic Forest is a museum of Neotropical butterfly 4 diversity: Insights from the evolution and biogeography of Brassolini (Lepidoptera: 5 Nymphalidae) 6 7 Authors: Pável Matos-Maraví1,2,3*, Niklas Wahlberg4, André V. L. Freitas5, Phil DeVries6,7, 8 Alexandre Antonelli1,2,8,9, Carla M. Penz6 9 10 Institutions: 11 1 Department of Biological and Environmental Sciences, University of Gothenburg, Carl 12 Skottbergs gata 22B, 41319 Gothenburg, Sweden 13 2 Gothenburg Global Biodiversity Centre, Carl Skottbergs gata 22B, 41319 Gothenburg, Sweden 14 3 Biology Centre of the Czech Academy of Sciences, Institute of Entomology, Branišovská 15 1160/31, 37005 České Budějovice, Czech Republic 16 4 Department of Biology, Lund University, Sölvegatan 37, 22362 Lund, Sweden 17 5 Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, 18 Rua Monteiro Lobato 255, CEP 13.083-862 Campinas, São Paulo, Brazil 19 6 Department of Biological Sciences, University of New Orleans, 2000 Lakeshore Drive, New 20 Orleans, LA 70148, USA 21 7 Courtesy Curators of Lepidoptera, Florida Museum of Natural History, 1659 Museum Road, 22 Gainesville, FL 32611, USA 23 8 Royal Botanical Gardens Kew, TW9 3AE Richmond, United Kingdom 1 bioRxiv preprint doi: https://doi.org/10.1101/762393; this version posted February 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 24 9 Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB Oxford, 25 United Kingdom 26 27 Corresponding author: 28 Pável Matos-Maraví; Institute of Entomology, Biology Centre CAS, Branišovská 1160/31, 370 29 05 České Budějovice, Czech Republic; E-mail: [email protected], ORCID: 30 https://orcid.org/0000-0002-2885-4919 31 32 ORCID ids: 33 Pável Matos-Maraví, https://orcid.org/0000-0002-2885-4919 34 Niklas Wahlberg, https://orcid.org/0000-0002-1259-3363 35 André V. L. Freitas, https://orcid.org/0000-0002-5763-4990 36 Phil DeVries, https://orcid.org/0000-0002-5692-6684 37 Alexandre Antonelli, https://orcid.org/0000-0003-1842-9297 38 Carla M. Penz, https://orcid.org/0000-0002-2544-3508 39 40 2 bioRxiv preprint doi: https://doi.org/10.1101/762393; this version posted February 23, 2021. 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. 41 ABSTRACT 42 Regional species diversity is ultimately explained by speciation, extinction, and dispersal. Here 43 we estimate dispersal and speciation rates of Neotropical butterflies to propose an explanation 44 for their distribution and diversity of extant species. We focus on the tribe Brassolini (owl 45 butterflies and allies): a Neotropical group that comprises 17 genera and 108 species, most of 46 them endemic to rainforest biomes. We infer a robust species tree using the multispecies 47 coalescent framework and a dataset including molecular and morphological characters. This 48 formed the basis for three changes in Brassolini classification: 1) Naropina, SYN. NOV. is 49 subsumed within Brassolina; 2) Aponarope, SYN. NOV. is subsumed within Narope; 3) 50 Selenophanes orgetorix, COMB. NOV. is reassigned from Catoblepia to Selenophanes. By 51 applying biogeographical stochastic mapping, we found contrasting species diversification and 52 dispersal dynamics across rainforest biomes, which might be partly explained by the geological 53 and environmental history of each bioregion. Our results reveal a mosaic of biome-specific 54 evolutionary histories within the Neotropics, where butterfly species have diversified rapidly 55 (cradles: Mesoamerica), have accumulated gradually (museums: Atlantic Forest), or have 56 alternately diversified and accumulated (Amazonia). Our study contributes evidence from a 57 major butterfly lineage that the Neotropics are a museum and cradle of species diversity. 58 59 KEYWORDS: Ancestral state inference – biogeographical stochastic mapping – bioregion 60 delimitation – dispersal – multispecies coalescent – speciation – total-evidence analyses. 61 3 bioRxiv preprint doi: https://doi.org/10.1101/762393; this version posted February 23, 2021. 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. 62 INTRODUCTION 63 Terrestrial biomes are heterogeneous in terms of species composition and distribution, and some 64 areas have accumulated greater diversity and endemicity than others. A combination of three 65 evolutionary mechanisms explains this biogeographical pattern: species origination, extinction, 66 and dispersal (Goldberg et al., 2005; Jablonski et al., 2006). For example, a species-rich region 67 can attain its present diversity by recent and exceptionally high rates of speciation, becoming a 68 “cradle of diversity”, or by the persistence of old lineages via low species extinction rates, 69 becoming a “museum of diversity” (e.g., Stebbins, 1974; Gaston & Blackburn, 1996; 70 Bermingham & Dick, 2001; Richardson et al., 2001). Furthermore, a species-rich region might 71 be a “source of diversity” when dispersal out of the region is high, or a “sink of diversity” when 72 regional species diversity is accrued from external sources via dispersal into the region 73 (Antonelli et al., 2018a). Characterizing the interplay among speciation, extinction, and dispersal 74 is thus highly relevant for understanding the origin and evolution of total regional diversity and 75 endemism (Wiens & Donoghue, 2004; Roy & Goldberg, 2007). 76 77 Much of the world’s biodiversity and endemism are concentrated in Neotropical rainforests in 78 Central America, the Amazon basin, and the Atlantic Forest in southeastern Brazil. However, 79 there is no consensus on whether these currently separated rainforests were connected once or 80 multiple times, nor for how long (Jaramillo & Cárdenas, 2013). It is also unclear whether 81 Neotropical rainforests represent centers of ecological stability that share a common evolutionary 82 history (Moritz et al., 2000). Mammals and birds in Neotropical biodiversity hotspots, including 83 the Brazilian Atlantic Forest and rainforests in Mesoamerica and the neighboring Chocó in the 84 northwestern side of the Andes (Myers et al., 2000), apparently underwent rapid diversification 4 bioRxiv preprint doi: https://doi.org/10.1101/762393; this version posted February 23, 2021. 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. 85 (Igea & Tanentzap, 2019). In other groups, a larger number of lineages seem to have dispersed 86 out of those areas compared to the rest of the Neotropics (e.g., Machado et al., 2018; Toussaint et 87 al., 2019), suggesting that such rainforests are both cradles and sources of diversity (Igea & 88 Tanentzap, 2019). Other Neotropical regions are, in contrast, museums of diversity given the old 89 and gradual accumulation of species through time, such as Amazonia for Euptychiina 90 (Nymphalidae) (Peña et al., 2010) and Troidini butterflies (Papilionidae) (Condamine et al., 91 2012). It thus seems that the checkered spatial assemblage of rainforest areas where speciation 92 rates are high plus those where extinction rates are low might explain why the Neotropical region 93 as a whole is considered both a cradle and museum of diversity (McKenna & Farrell, 2006; 94 Moreau & Bell, 2013; Antonelli et al., 2018b). However, the impacts of geological and 95 paleoenvironmental changes in the Neotropics together with the roles of speciation and dispersal 96 have seldom been jointly elucidated among taxa occurring in individual rainforest areas. 97 98 Here we examine biogeographical patterns for butterflies in the tribe Brassolini (Nymphalidae: 99 Satyrinae), an exclusively Neotropical monophyletic group (Freitas & Brown, 2004; Wahlberg et 100 al., 2009; Espeland et al., 2018; Chazot et al., 2019a) consisting of 17 genera and 108 species 101 found mainly in the rainforests of Mesoamerica, the northwestern slope (NW) of the Andes 102 (including e.g., Chocó), the Atlantic Forest, and Amazonia (see Penz, 2007, for an overview). 103 Studies that focused on individual brassoline genera used adult morphology (Penz, 2008, 104 2009a,b; Garzón-Orduña & Penz, 2009) and DNA data (Penz, Mohammadi, & Wahlberg, 2011a; 105 Shirai et al., 2017) to infer species-level phylogenies, but several deep nodes had weak or even 106 conflicting phylogenetic support in tribal-level analyses (Penz et al., 2013). We infer a time- 107 calibrated species phylogeny of Brassolini by merging all
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