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The Evolution of the Brownea Clade (Detarioideae, Leguminosae)

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The Evolution of the Brownea Clade (Detarioideae, Leguminosae) Accepted Manuscript Is Amazonia a ‘museum’ for Neotropical trees? The evolution of the Brownea clade (Detarioideae, Leguminosae) Rowan J. Schley, Manuel de la Estrella, Oscar Alejandro Pérez-Escobar, Anne Bruneau, Timothy Barraclough, Félix Forest, Bente Klitgård PII: S1055-7903(17)30528-6 DOI: https://doi.org/10.1016/j.ympev.2018.04.029 Reference: YMPEV 6139 To appear in: Molecular Phylogenetics and Evolution Received Date: 4 August 2017 Revised Date: 28 February 2018 Accepted Date: 19 April 2018 Please cite this article as: Schley, R.J., Estrella, M.d.l., Alejandro Pérez-Escobar, O., Bruneau, A., Barraclough, T., Forest, F., Klitgård, B., Is Amazonia a ‘museum’ for Neotropical trees? The evolution of the Brownea clade (Detarioideae, Leguminosae), Molecular Phylogenetics and Evolution (2018), doi: https://doi.org/10.1016/j.ympev. 2018.04.029 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Is Amazonia a ‘museum’ for Neotropical trees? The evolution of the Brownea clade (Detarioideae, Leguminosae) Rowan J. Schleya,b*, Manuel de la Estrellaa, Oscar Alejandro Pérez-Escobara, Anne Bruneauc, Timothy Barracloughb, Félix Foresta, and Bente Klitgårda a Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK bDepartment of Life Sciences, Imperial College London, Silwood Park, Ascot, Berkshire, UK, SL5 7PY cInstitut de recherche en biologie végétale and Département de Sciences biologiques, Université de Montréal, 4101 Sherbrooke est, Montréal, QC H1X 2B2, Canada *Corresponding author at: Room E.2.6, Herbarium, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK E-mail address: [email protected] (R. J. Schley). Highlights: The Brownea clade diversified gradually, following the ‘museum’ model The Brownea clade originated in the Eocene, and diversified throughout the Neogene The clade diversified mainly in Amazonia, with subsequent migrations across the Neotropics Abstract The flora of the Neotropics is unmatched in its diversity, however the mechanisms by which diversity has accumulated are debated and largely unclear. The Brownea clade (Leguminosae) is a characteristic component of the Neotropical flora, and the species within it are diverse in their floral morphology, attracting a wide variety of pollinators. This investigation aimed to estimate species divergence times and infer relationships within the group, in order to test whether the Brownea clade followed the ‘cradle’ or ‘museum’ model of diversification, i.e. whether species evolved rapidly over a short time period, or gradually over many millions of years. We also aimed to trace the spatio- temporal evolution of the clade by estimating ancestral biogeographical patterns in the group. We used BEAST to build a dated phylogeny of 73 Brownea clade species using three molecular markers (ITS, trnK and psbA-trnH), resulting in well-resolved phylogenetic relationships within the clade, as well as robust divergence time estimates from which we inferred diversification rates and ancestral biogeography. Our analyses revealed an Eocene origin for the group, after which the majority of diversification happened in Amazonia during the Miocene, most likely concurrent with climatic and geological changes caused by the rise of the Andes. We found no shifts in diversification rate over time, suggesting a gradual accumulation of lineages with low extinction rates. These results may help to understand why Amazonia is host to the highest diversity of tree species on Earth. Keywords: Diversification; Phylogenetics; Biogeography; Amazonia; Legumes 1. Introduction The tropical Americas are home to a great number of seed plant species (ca.100,000 species (Antonelli and Sanmartín, 2011; Hughes, et al, 2013)), however the evolutionary and biogeographical forces which led to the formation of this superlative diversity are unclear for many groups. The time period over which this diversity has accumulated has been a topic of much debate, largely surrounding two theories. The first is the ‘museum’ model of diversification, whereby radiations dating from the Neogene or earlier have persisted in Amazonia due to climatic stability and niche conservatism, allowing many thousands of lineages to accumulate over the past 30 million years (Antonelli and Sanmartín, 2011). By contrast, the ‘cradle’ model of diversification suggests that geologically recent events, such as the orogeny of the Andes and the rise of the Panama isthmus, triggered large scale climatic, geographical and edaphic changes, resulting in rapid speciation due to reproductive isolation (Richardson, et al, 2001; Hughes and Eastwood, 2006). It is worth noting that these theories are not mutually exclusive, and indeed both are evident in different lineages, such as Bromeliaceae (Givnish, et al, 2011), Orchidaceae (Pérez‐ Escobar, Chomicki, et al, 2017; Pérez‐ Escobar, Gottschling, et al, 2017) and Annonaceae (Couvreur, et al, 2011). In addition to this, the interactions between speciation, extinction and geographical range fluctuation are also considered to be important in the accumulation of diversity (Jablonski, et al, 2017). In the low-to-mid elevation forests of the Neotropics plant families show a bipartite pattern of diversity (Gentry, 1982). The first of these two major portions of Neotropical plant diversity includes the Andean-centred taxa, which are those lineages whose centre of diversity lies in North-western South America, within the foothills, valleys and montane zones of the Andes. The majority of the species in this portion are epiphytes and understory shrubs (Gentry and Dodson, 1987). The second portion includes the Amazonian-centred taxa, whose taxonomic diversity is highest in the Amazon basin. The majority of the species in this portion are canopy trees or lianas (Gentry, 1982; Prance, 1994). Several overlapping hypotheses are used to explain this biogeographical pattern (known as the ‘Gentry Pattern’ (Antonelli and Sanmartín, 2011)), the most prominent of which relates the rapid, punctuated rise of the Andes to the evolution of the Neotropical flora (Gentry, 1982). For the Amazonian-centred taxa it is well documented that the Andean orogeny drove much of the diversification of the modern flora (Hoorn, et al, 2010), as mountain building processes would have driven large scale hydrological and climatic changes throughout what is now Amazonia (Gregory- Wodzicki, 2000). Around 50 Ma, during the Eocene, the lowland forests of northern South America were much more extensive than in modern times, with an area known as ‘pan-Amazonia’ stretching over much of South America unimpeded (Hoorn, et al, 2010). The Andean orogeny, beginning in earnest around the early Miocene (~23 Ma), would have caused the formation of the Pebas system, an enormous matrix of wetland and terra firme forest, and subsequently the Acre system (another vast area of wetlands in what is now western Amazonia) which could have driven speciation in situ through allopatry (Hoorn, et al, 2010; Antonelli and Sanmartín, 2011). During the Miocene, as the Andes rose, the drainage of the Amazon basin changed direction, resulting in a west-to-east flow; this would have gradually reduced the size of the Pebas and subsequent Acre wetlands until their disappearance. As well as this, fluvial regimes arising from the Andes would have deposited nutrient-rich sediments into the western Amazon basin, resulting in an ‘edaphic mosaic’ on a large scale (Hoorn, et al, 2010). This high edaphic heterogeneity was likely also a strong driver for local adaptation and concurrent speciation (Pennington and Lavin, 2016). As such, hydrological regimes, edaphic heterogeneity and dispersal with subsequent diversification of taxa into novel niches (Erkens, et al, 2007) may help to explain the hyperdiversity of tree species found in the western Amazon (Valencia, et al, 2004). Trees belonging to the Leguminosae (alternatively ‘Fabaceae’) are among the most common species found in Neotropical rainforests (Terborgh and Andresen, 1998). As such, they are an excellent system for studying the evolution of plant species in the Neotropics. The Brownea clade, which belongs to the legume subfamily Detarioideae (LPWG, et al, 2017) is made up of 111 species belonging to nine genera (Mackinder, 2005), which are all sub-canopy or canopy-level trees found in lowland Neotropical rainforests (Redden and Herendeen, 2006). While the majority of species in the Brownea clade occur in Amazonia, there are several species that are endemic to only one region, such as the Chocó-Darien moist forests or Central America. The seeds of most species within the clade are dispersed by explosively dehiscing woody pods, and as such many species are locally common, forming stands (Klitgaard, 1991), with relatively low dispersal. A few species, such as Macrolobium acaciifolium, are, however, very widely dispersed and are ‘hyperdominant’ in Amazonia (ter Steege, et al, 2013) due to their hydrophilic habitat preference and floating fruits. The Brownea clade is particularly diverse in floral morphology and attracts a wide variety of pollinators. Many species are adapted to attract vertebrate pollinators (mainly
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