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The Abrupt Climate Change at the Eocene-Oligocene Boundary and the Emergence of South-East Asia Triggered the Spread of Sapindaceous Lineages

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The Abrupt Climate Change at the Eocene-Oligocene Boundary and the Emergence of South-East Asia Triggered the Spread of Sapindaceous Lineages Research Collection Journal Article The abrupt climate change at the Eocene-Oligocene boundary and the emergence of South-East Asia triggered the spread of sapindaceous lineages Author(s): Buerki, Sven; Forest, Félix; Stadler, Tanja; Alvarez, Nadir Publication Date: 2013-07 Permanent Link: https://doi.org/10.3929/ethz-b-000070329 Originally published in: Annals of Botany 112(1), http://doi.org/10.1093/aob/mct106 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Annals of Botany 112: 151–160, 2013 doi:10.1093/aob/mct106, available online at www.aob.oxfordjournals.org The abrupt climate change at the Eocene–Oligocene boundary and the emergence of South-East Asia triggered the spread of sapindaceous lineages Sven Buerki1,*, Fe´lix Forest1, Tanja Stadler2,† and Nadir Alvarez3,† 1Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK, 2Institute of Integrative Biology, ETH Zu¨rich, Universita¨tsstr. 16, 8092 Zu¨rich, Switzerland and 3Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland †These authors contributed equally to this work and are considered co-last authors. * For correspondence. E-mail [email protected] Received: 23 November 2012 Revision requested: 18 March 2013 Accepted: 3 April 2013 Published electronically: 30 May 2013 † Background and Aims Paleoclimatic data indicate that an abrupt climate change occurred at the Eocene–Oligocene (E–O) boundary affecting the distribution of tropical forests on Earth. The same period has seen the emergence of South-East (SE) Asia, caused by the collision of the Eurasian and Australian plates. How the combination of these climatic and geomorphological factors affected the spatio-temporal history of angiosperms is little known. Thistopic is investigated by using the worldwide sapindaceous clade as a case study. † Methods Analyses of divergence time inference, diversification and biogeography (constrained by paleogeog- raphy) are applied to a combined plastid and nuclear DNA sequence data set. Biogeographical and diversification analyses are performed over a set of trees to take phylogenetic and dating uncertainty into account. Results are ana- lysed in the context of past climatic fluctuations. † Key Results An increase in the numberof dispersal events at the E–O boundary is recorded, which intensified during the Miocene. This pattern is associated with a higher rate in the emergence of new genera. These results are discussed in light of the geomorphological importance of SE Asia, which acted as a tropical bridge allowing multiple contacts between areas and additional speciation across landmasses derived from Laurasia and Gondwana. † Conclusions This study demonstrates the importance of the combined effect of geomorphological (the emergence of most islands in SE Asia approx. 30 million years ago) and climatic (the dramatic E–O climate change that shifted the tropical belt and reduced sea levels) factors in shaping species distribution within the sapindaceous clade. Key words: Biogeography, climate change, diversification, Eocene–Oligocene boundary; Sapindaceae; South- East Asia. INTRODUCTION phytogeographical connections between the southern hemi- sphere landmasses that were assembled during the Cretaceous Although not considered as one of the ‘Big five’ mass extinctions (for more details on fossils from Antarctica, see also Cantrill (Jablonski, 2001), the abrupt cooling near the Eocene– and Pool, 2005). Oligocene (E–O) boundary, approx. 33.7 million years ago During the same geological period, intensive volcanic activ- (Ma), had great impacts on biodiversity (Katz et al., 2008; ities were recorded in South-East (SE) Asia as a result of the col- Zhonghui et al., 2009). During this period, Earth’s climate lision of the Eurasian and Australian plates (Metcalfe, 1998; shifted from a relatively ice-free world to one with glacial condi- Hall, 2009). Although the western part of SE Asia (also known tions in polar regions characterized by substantial ice sheets as Sundaland and referred to as proto-SE Asia by Buerki et al., (Bowen, 2007). In a relatively short time span, high-latitude 2011a) already formed a large emergent land area by the Late (45–70 8 in both hemispheres) temperatures decreased from Cretaceous (including, for example, the older parts of Malaysia approx. 20 8C to approx. 5 8C(Zhonghui et al., 2009). and Southwest Borneo), most of the islands at the margin of Explanations for this cooling include changes in ocean circula- Sundaland and New Guinea, known as Wallacea (Hall, 2009), tion due to the opening of Southern Ocean gateways, a decrease were created from this period onwards, with a peakof tectonic ac- in atmospheric CO2 and a decrease in solar insulation (see tivity during the Miocene (Hall, 2009). Wallacea is at present a Zhonghui et al., 2009, and references therein). This period also region of high endemism for plants and animals (for a review, coincided with drought in southern regions (especially in see Richardson et al., 2012). Australia and Africa; Bowen, 2007) and subsequent reduction Currently, little is known about the consequences of the abrupt of the tropical belt (see Morley, 2003; Lohman et al., 2011). change in abiotic factors – the combination of climate change As a consequence, this abrupt cooling seemed to be related to a and intense tectonic/volcanic activities, especially in SE Asia – decrease in species diversity as shown, for instance, in the that occurred from the E–O boundary onwards on angiosperm decline of the Neotropical floras (Jaramillo et al., 2006). In add- biodiversity. Did sapindaceous lineages follow the same trend ition, Coetzee and Muller (1984) advocated that this event as marine biota (Rohde and Muller, 2005; Mayhew et al., 2012) (whose effects lasted until the Miocene) disrupted previous and neotropical flora (Jaramillo et al., 2006) in declining in # The Author 2013. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 152 Buerki et al. — Biogeography of sapindaceous lineages species diversity during this period? Alternatively, could (internal transcribed spacer) region. This data set includes the establishment of SE Asia have acted as a refugium for .60 % of the generic diversity of the group (147 samples) and tropical angiosperms and triggered their diversification? In this one outgroup taxon, Harrisonia abyssinica (Simaroubaceae; study, we propose to investigate this topic by focusing on for more details, see Buerki et al., 2009). We have included four closely related families – Xanthoceraceae, Aceraceae, only one outgroup taxon based on previous phylogenetic infer- Hippocastanaceae and Sapindaceae, hereafter referred to as the encesthat stronglysupported the monophylyof the sapindaceous sapindaceous clade (Buerki et al., 2010). Recently, the authors clade (e.g. Gadek et al., 1996; APG III, 2009; Buerki et al., have focused their effort in circumscribing generic entities 2011b). within the worldwide sapindaceous clade and proposing a new fa- A partitioned Bayesian inference approach implemented in milial classification based on molecular and morphological data the package BEAST v.1.5.4 (Drummond and Rambaut, 2007) (see, for example, Buerki et al.,2009, 2010). This clade was was used to infer a temporal framework for the evolution of the also used as a case study to assess the performance of various bio- sapindaceous clade. Two partitions (plastid and nuclear) were geographical methods and propose a worldwide stratified paleo- defined following Buerki et al. (2011a) with an uncorrelated geographical model (from Late Cretaceous to the present) to relaxed molecular clock assuming a log normal distribution of constrain biogeographical inference (Buerki et al.,2011a). rates and a Yule speciation model. Two runs of 20 × 106 genera- Moreover, the four families within the sapindaceous clade are tions were performed, sampling one tree every 1000th gener- characterized by several features making them an ideal case ation. Average branch lengths and 95 % confidence intervals studytoinvestigatethe effect ofpast climateand geomorphologic- on nodes were calculated using TreeAnnotator v.1.5.4 al change on the diversification and biogeography of flowering (Drummond and Rambaut, 2007) after burn-in and reported on plants: (1) worldwide distribution (centres of diversity in South a majority rule consensus tree. Six calibration points based on America and SE Asia); (2) available plastid and nuclear phyl- fossil records (see Buerki et al., 2011a) were used to constrain ogeny at the generic level (Buerki et al., 2009); (3) occurrence the BEAST analysis (see below). With the exception of the cali- of reliable fossils dating back to the Eocene (Buerki et al., bration point associated with the root, all points were modelled as 2011a); (4) fairly good taxonomic knowledge (see references in follows: log normal distribution, mean ¼ 0, s.d. ¼ 1, offset ¼ Buerki et al., 2009, 2010); and (5) a temporal framework compat- fossil age (see below). In the case of the root calibration point, ible with the examination of processes that occurred at the E–O (a) a normal distribution was applied with the mean fixed at boundary (i.e. the clade originated during the Late Cretaceous; 125 million years and s.d. ¼ 1. The calibration points
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