The Cenozoic biogeographical evolution of woody angiosperms inferred from fossil distributions

RESEARCHPAPER

The Cenozoic biogeographical evolutionof woody angiosperms inferred fromfossil distributionsYaowu Xing1*, Maria A. Gandolfo2 and H. Peter Linder1

1Institute of Systematic Botany, University of

Zurich, Zurich, Switzerland, 2L. H. Bailey

Hortorium, Plant Biology Section, School of

Integrative Plant Science, Cornell University,

Ithaca, NY, USA

ABSTRACT

Aim We test whether the modern regionalization of the angiosperm flora is theresult of Cenozoic barriers to dispersal.

Location Global.

Methods We used a database of Cenozoic woody angiosperm fossils to build amatrix of family and genus occurrence at 11 continents/regions for five timeperiods of the Cenozoic, thus defining 55 floras. We used ordinations and clusteranalyses to infer the relationships among these floras. We tested for the effects oftime, land connections and dispersal barriers on the similarities between thesewoody angiosperm floras.

Results For all time periods of the Cenozoic the world’s woody angiosperm floraswere grouped into three large clusters: a very compact Northern Hemispherecluster (North America, Europe, temperate Asia and Palaeogene south China), asomewhat less compact Palaeotropical cluster (Africa, India, Southeast Asia andNeogene south China) and a rather diffuse Gondwanan cluster (Antarctica, Aus-tralia, New Zealand, temperate South America and the Neotropics). The primaryclustering is evidently geographical, and reflects the barriers formed by the Tethysand the southern Atlantic–southern Indian oceans. There is evidence that the morerecent Gondwanan floras are more divergent than the older floras, possibly due tolong isolation by oceans and multiple extinction events, whereas the similaritiesamong Northern Hemisphere floras increased during the Neogene.

Main conclusions The modern regionalization is mainly the result of dispersalbarriers that existed at diverse times in the Cenozoic, resulting in several woodyangiosperm floras that evolved in parallel. Climatic change and dispersal alsoplayed important roles in shaping biogeographical patterns of Cenozoic woodyangiosperms.

KeywordsAngiosperm, Cenozoic, Cenozoic Angiosperm Database, cluster analysis,floristic kingdom, Gondwana, ordination, regionalization, Tethys.

*Correspondence: Yaowu Xing, IntegrativeResearch Center, the Field Museum of NaturalHistory, 1400 S Lake Shore Drive, Chicago, IL60605, USA.E-mail: [email protected]

INTRODUCTION

The modern angiosperm flora is strongly regionalized. This geo-graphical patterning had already been detected by de Candolleat the beginning of the 19th century (de Candolle, 1820) andwas elaborated and quantified throughout the next 150 years.This regionalization led to a series of systems, for example thesix floristic kingdoms system (Good, 1953), which was elabo-rated by Takhtajan (1986). Although there is debate on whether

all these kingdoms should be recognized, or whether theboundaries among them should be drawn somewhat differently(Cox, 2001, 2010; Morrone, 2002), there is no dispute thatregionalization exists at a continental scale. This regionalizationcould be the result of two processes. Firstly, divergence may bedue to the fragmentation of the global land surface into conti-nents separated by relatively wide oceans. A prediction of thishypothesis is that the regions will be separated by obvious bar-riers to dispersal (usually oceans). Secondly, inter-regional dif-

bs_bs_banner

Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2015)

© 2015 John Wiley & Sons Ltd DOI: 10.1111/geb.12383http://wileyonlinelibrary.com/journal/geb 1

ferentiation may be the result of climatic differences, which mayfilter out those families that cannot survive in that climate. Mostlikely both processes contributed to the current regionalization.

The ‘barriers to dispersal hypothesis’ is, at least partially, avicariance hypothesis. It postulates that an initially global florawas fragmented into geographical regions which are more orless isolated from each other, and that each regional floraevolved largely independently from all other regional floras. Thismay result in a pattern similar to the kingdoms proposed by Cox(2001), where each kingdom is bounded by oceans. If geo-graphical differentiation is relatively slow, then the kingdomsmay reflect past barriers. The ‘barrier to dispersal hypothesis’leads to the prediction that the evolution of regionalizationthrough the Cenozoic should track the evolution of the barriersto dispersal. Consequently, this hypothesis comprises two sub-hypotheses based on two key barriers: (1) the Tethyan hypoth-esis (the Tethys, separating North America, Europe and Asiafrom the remaining continents) and (2) the Afro-Indianhypothesis (the southern Atlantic–southern Indian oceans,separating Africa and India from the remainder of Gondwana inthe Cretaceous).

Alternatively, the kingdoms could be the result of climaticdifferentiation, for example between the cold temperateHolarctic, the warm and wet tropical Neotropical andPalaeotropical kingdoms, and the warm temperate Australianand Cape kingdoms. There is substantial evidence that clades areecologically conservative (Crisp et al., 2009), and that they dis-perse more readily than they change ecologically (Donoghue,2008). This hypothesis predicts, firstly, that floras exposed tosimilar climates should group together, irrespective of the barri-ers that separate them. The magnitude of the climatic changesthroughout the Cenozoic (Zachos et al., 2008) most likely farexceeds the differences among the continents, and therefore it isexpected that floras from the same period should group together,irrespective of their geographical locations. If clades are largelyclimatically constrained, these climate changes should have led tomajor floristic restructuring through time. The second predic-tion is that the boundaries between kingdoms should followclimatic boundaries. This is consistent with the Takhtajan systemthat separates the temperate southern tips of South America andAfrica from the tropical central parts of these continents.

Time-calibrated molecular phylogenies show that mostangiosperm families originated in the Cretaceous (Magallónet al., 2015). Therefore the biogeographical pattern of angio-sperms should be profoundly affected by the complex anddynamic patterns of isolation and connectivity among conti-nents during the Cenozoic. Gondwana fragmented into Africaand a large block including Australia, New Zealand, SouthAmerica and Antarctica during the Late Cretaceous. Australia,New Zealand, South America and Antarctica separated duringthe Palaeogene. By the Pliocene all the continents had reachedtheir current positions, and in particular, Australia, Africa andSouth America had docked against Asia, Europe and NorthAmerica, respectively. The position of India in the Indian Oceanat the time of the Cretaceous–Palaeogene boundary (65 Ma) isstill debated. It was either situated in the middle of the Indian

Ocean (Scotese, 2001) or lay in close proximity to Africa, Asiaand Madagascar (Briggs, 2003). India continued to move north-ward and collided with Asia between 65 Ma (Yin & Harrison,2000) and c. 50 Ma (Rowley, 1998; Zhu et al., 2005). In theNorthern Hemisphere, the North American and Eurasian platesbegan to separate in the middle Cretaceous and the AtlanticOcean has been widening ever since (Hamilton, 1983). However,Europe was directly connected to North America until the earlyEocene by the North Atlantic Land Bridge and was separatedfrom Asia by the Turgai Strait in the Palaeogene (Tiffney &Manchester, 2001). This epicontinental sea between Europe andAsia started to retreat in the late Eocene and finally disappearedin the Oligocene (Akhmetiev & Beniamovski, 2009; Akhmetievet al., 2012). The Bering Land Bridge connected North Americaand Asia from at least the early Palaeogene until the lateMiocene–early Pliocene (Marincovich & Gladenkov, 2001). Thebroad outlines of the Cenozoic climate changes are well docu-mented (Zachos et al., 2001, 2008). The Palaeocene and Eocenewere much warmer than today. During the late Eocene a coolingtrend set in, with small, ephemeral ice sheets appearing at theend of this epoch (Zachos et al., 2001), and culminating in adramatic cooling event during the Eocene/Oligocene transition.This resulted in the establishment of seasonal climates, eventu-ally leading to the differentiation of cold-temperate climates andseasonal deserts (Zachos et al., 2001; Mosbrugger et al., 2005;Eldrett et al., 2009).

Palaeontological data provide a unique resource for evaluat-ing the impact of these geological and climatic events on thephytogeography of angiosperms (Tiffney, 1985; Manchester,1999; Hill, 2001; Tiffney & Manchester, 2001; Kooyman et al.,2014). However, to date there has been no analysis of angio-sperm regionalization in the several epochs of the Cenozoic;consequently it is unknown to what extent the modernregionalization is a result of patterns in the past. Here we use avery large, global, compilation of the angiosperm Cenozoicfossil record (Xing et al., 2015) to trace the floristic divergenceamong regions, and to explore whether the regionalization ofthe angiosperm flora through the Cenozoic reflects barriersand continents (vicariance), or epochs and climates (biome-controlled long-distance dispersal). Specifically, we ask if we candetect a signal of Gondwana, Laurasia and the Palaeotropics inthe extant floras, and whether this can be interpreted to reflectthe Tethys and the late Mesozoic opening of the southern Atlan-tic and Indian oceans. Secondly, we test if there is an increasingsimilarity among Northern Hemisphere regions due to continu-ous biotic exchanges through land connectivities in the Ceno-zoic and a decreasing similarity among Gondwanan regions dueto long isolation by oceans.

METHODS

Data

Data were downloaded from our newly compiled database forCenozoic angiosperm macrofossils (the Cenozoic AngiospermDatabase, CAD), available at the CAD website (http://

Y. Xing et al.

Global Ecology and Biogeography, © 2015 John Wiley & Sons Ltd2

www.fossil-cad.net/; Xing et al., unpublished data). The CADcontains data from 2512 assemblages representing 2007 sites. Itincludes 49,965 occurrences, of which 40,799 have been assignedto 220 angiosperm families, 1859 genera and 9747 species.However, this fossil record is biased in several aspects: (1) woodylineages are over-represented in the macrofossil record comparedwith herbaceous lineages (Xing et al., unpublished data); (2)there may be regional variation in which taxonomic groups areover-represented, as palaeobotanists usually work regionally andtarget the groups they understand best. To deal with the first bias,we focus on the biogeographical pattern of woody taxa. Weassigned a growth form (mainly woody or mainly herbaceous) tothe fossil genera based on the nearest living relative concept.Genera not assigned to families, or for which growth form couldnot be inferred, were excluded from the analyses. To address thesecond bias, we use higher taxonomic level (generic and familylevels) because higher taxonomic levels are more likely to becompletely represented. In addition, we performed separateanalyses on the rosids, which is the best-sampled angiospermclade. We extracted the lists of woody genera and families rec-orded from each region for each geological period. We subdi-vided the Cenozoic into five periods of relatively equal length toreduce the sampling bias. These are the Palaeocene–early Eocene(starting 65.5 Ma), middle–late Eocene (47.8 Ma), Oligocene(33.9 Ma), early–middle Miocene (23.0 Ma) and late Miocene–Pleistocene (11.6 Ma). These five time slices also match climati-cally different periods in the Cenozoic: the hothouse Palaeocene–early Eocene, the cooling middle–late Eocene, the cold andseasonal Oligocene, the warm-tropical early–middle Mioceneand the cold and seasonal late Miocene–Pleistocene (Zachoset al., 2001). Fossil assemblages with uncertain ages wereexcluded.

Ideally, the optimal unit for the analyses would be the assem-blages, as each can be assigned to a specific site and time slice.However, most assemblages are strongly under-sampled, and thegeographical scale is too fine for our analysis. Consequently, weassumed that each region would have a distinct flora. We defined

11 regions: Europe (west of the Urals), temperate Asia (east ofthe Urals and north of the Himalaya), south China (south of23.5° N), India (south of the Himalaya), Australia, New Zealand,Africa, the Neotropics (tropical South America, north of30.0° S), temperate South America (south of 30.0° S), NorthAmerica and Antarctica. We use the term flora to refer to the setof fossil taxa from a particular region and time period (Table 1).As under-sampled floras may lead to improbable results (Kreft &Jetz, 2010), we deleted all floras with fewer than five taxa(families/genera). To explore the impact of the Cenozoic historyon the current biogeography, we also mapped modern floras,based on the present distributions of extant genera of woodyangiosperms, and woody rosids that were also recorded in thefossil record (Table 1). The modern native (non-anthropogenic)distributions were mainly based on the Angiosperm PhylogenyWebsite (http://www.mobot.org/) and Global BiodiversityInformation Facility website (http://www.gbif.org/) (bothaccessed 31 May 2015). The final data set includes 133 familiesand 1077 genera of woody angiosperms. However, differentregions had very different numbers of genera and families(Table 1). The best-sampled floras are those of the temperateAsian and European Neogene and the North American andEuropean Palaeogene, while under-sampled or species-poorfloras are the Neotropical, African, south Chinese, Antarctic andSoutheast Asian Palaeogene floras.

Analyses

Following the framework for delineating biogeographicalregions suggested by Kreft & Jetz (2010), we explored the pat-terns of relationships among the floras using both ordinationand clustering methods. We used the beta-sim index (!sim) tocalculate the distance between floras. !sim was calculated as:!sim = min(b,c)/min(b,c) + a, where a is the number of sharedspecies and b and c are the number of species unique to eachflora, respectively. Therefore, the similarity was calculated as1 " !sim. We used this index because it is independent of richness

Table 1 Number of angiosperm families (left of the back-slash) and genera (right of the back-slash) recorded for each time period.

Paleocene–earlyEocene

Middle–lateEocene Oligocene

Early–middleMiocene

Late Miocene–Pleistocene Present

Antarctica (AN) 16/18 6/8 –/– –/– –/– –/–Africa (AF) –/– –/6 11/34 27/56 49/171 90/248Australia (AU) 9/18 10/19 9/21 10/13 8/12 87/163New Zealand (NZ) –/– 8/10 –/– 7/8 26/31 45/28Temperate South America (TSA) 47/103 17/29 43/81 6/6 –/– 45/21Neotropics (NEO) –/– –/– –/– 9/13 29/46 107/224North America (NA) 56/143 67/220 51/134 44/80 45/91 76/176Europe (EU) 45/110 56/101 58/160 74/240 73/206 55/100Temperate Asia (AS) 36/76 53/136 65/173 55/151 62/171 90/230India (IN) 18/29 8/12 19/26 43/157 30/85 80/154Southeast Asia (SEAS) –/– 7/8 –/– –/– 7/17 116/303South China (SCH) –/– –/– 14/21 13/17 21/55 106/329

‘–’ Indicates that floras are not sampled or with fewer than five families or genera.

Angiosperm Cenozoic biogeography

Global Ecology and Biogeography, © 2015 John Wiley & Sons Ltd 3

and such turnover is more informative for the purposes of bio-geographical regionalization (Kreft & Jetz, 2010), especially inour very unevenly sampled dataset. These similarities were sim-plified to a two-dimensional ordination using non-metricmulti-dimensional scaling (NMDS) to visualize the relation-ships among the floras. The quality of the results was assessed asthe difference between the ranked distances in the ordinationand the original ranked distances (the stress). In addition, thefloras were clustered using the unweighted pair group methodwith arithmetic mean (UPGMA) to test whether the floras weregrouped by region or by time. This clustering approach presentsa balance between chaining and grouping approaches and hasgenerally been found to result in the best grouping estimates(Kreft & Jetz, 2010). We also clustered the Palaeogene andNeogene floras separately to test whether the clusters are con-sistent through time. The degree of distortion between the dis-similarity matrix and the phenogram was quantified with thecophenetic correlation coefficient, comparing the calculatedsimilarities among the floras with the similarities implied by thephenogram. All analyses were done for both genera and familiesusing past (Hammer, 2001).

Impact of time, palaeobarriers and continental drifton dissimilarities among floras

We tested whether the divergence among the angiosperm florasincreased through time by comparing similarities among theregions for each time slice with Tukey’s pairwise comparisonafter running a one-way ANOVA. The floristic similarities of thefloras for both genera and families were quantified by the !sim

index calculated using past (Hammer, 2001; Table 2). Greatersimilarities among older floras than among the younger floraswould indicate increasing floristic differentiation among thecontinents through the Cenozoic. We also tested the effect ofpalaeobarriers and continental drift on the similarities amongthe Northern Hemisphere floras, as well as among theGondwanan floras. We predicted an increasing similarity in theNeogene among the Northern Hemisphere floras due to theNorth Atlantic and Bering land bridges and the retreat of theTurgai Strait. On the contrary, we expected a decreasing simi-larity among the Gondwanan floras due to absence of any Ceno-zoic connections among the austral continents.

RESULTS

Generic patterns

The NMDS ordinations for all woody angiosperms and for therosids alone show very similar patterns. Three large clusters wereretrieved (for all woody angiosperms, Fig. 1a; for the woodyrosids alone, Fig. S1 in Appendix S1 in Supporting Information):the Northern Hemisphere (‘NH’) floras, the Gondwanan floras(Australia, New Zealand, temperate South America and theNeotropics) and the Palaeotropical floras (Africa, India, early–middle Miocene and present south China and Southeast Asia).The overall stress of the NMDS ordination is 0.29, which is a fairvalue (Sneath & Sokal, 1973). The NH floras cluster much more

tightly together than the other two clusters of flora. Three smallgroups are recognized within the Gondwanan group, i.e. Aus-tralia + New Zealand, temperate South America + Antarctica,and the Neotropics. The three Neotropical floras are more or lesslocated between the other Gondwanan and the other two clusters.The early–middle Miocene and present south Chinese floras liebetween the other Palaeotropical and the NH floras.

The clustering analyses for all woody angiosperms and therosids alone reveal the same three groups of floras (all woodyangiosperms,Fig. 2a; only woody rosids,Fig. S2 in Appendix S1).In the Gondwanan group, the Australian and New Zealand florasgroup together. However, whereas this group is sister to all otherfloras in the analysis of all woody angiosperms, it is clustered withthe Antarctic, Neotropical and temperate South American florasin the analysis of the rosids alone. The Neotropical, Antarctic andtemperate South American floras group together, with the Ant-arctic and temperate South American floras forming a subgroup.The NH includes all European, temperate Asian and NorthAmerican floras, plus the Oligocene and late Miocene–Pleistocene south Chinese floras. The NH regions are intermin-gled in the phenogram, while the Gondwanan regions are allretrieved as separate groups. The Palaeocene–Eocene Europeanfloras are somewhat isolated from the other NH floras. ThePalaeotropical group includes the African, Indian and SoutheastAsian floras plus the early–middle Miocene and present southChinese floras. Of these, the only region that is retrieved as aseparate cluster is Africa. All extant floras are nested in theirancestral floras except for the south Chinese flora. Thecophenetic correlation of 0.76 indicates that the obtainedphenogram is a good reflection of the patterns of similarityamong the floras (Sneath & Sokal, 1973). Similar groups wereretrieved based on independent clusters for the Palaeogene(cophenetic correlation 0.88) and Neogene (cophenetic correla-tion 0.87), though positions for some regional floras are incon-sistent with the whole Cenozoic analysis (Fig. 2b,c).

Family pattern

Not surprisingly, the differences in taxon richness in the familysamples are smaller than the differences in generic richness(Table 1). The NMDS ordinations for all woody angiospermsand the rosids at family level show that the floras are morescattered in the ordination space compared with the genericpattern, albeit with fair values of stress, 0.36 and 0.34 respec-tively (Figs 1b & S3 in Appendix S1). The same three largeclusters can largely be recognized. However, the tropical SouthAmerican floras are placed as intermediate between thePalaeotropical and the Gondwanan clusters (Figs 1b & S3 inAppendix S1). As in the generic-level ordination, the NH clusteris more tightly clustered than the other two clusters and wellretrieved in both Palaeogene and Neogene analyses (Fig. 1b).The early–middle Miocene south Chinese flora is placed in theNH cluster rather than the Palaeotropical cluster (Fig. 1b).

The cluster analysis of the family-level floras using !sim

approximates the same three clusters that were found in thegeneric analysis (Figs 3 & S4 in Appendix S1). However, the

Y. Xing et al.


Table 2 Similarities among differentfloras based on !sim algorithm at familyand generic levels (below the diagonal:family level similarity; above thediagonal: generic level similarity). SeeTable 1 for region acronym definitions.PAEE: Paleocene – early Eocene; MLEO:middle – late Eocene; OLIGO:Oligocene; EMMIO: early – middleMiocene; LMPL: late Miocene –Pleistocene.

PAEE AF AN AS AU EU IN NA NEO NZ TSA SEAS SCH

AF – – – – – – – – – – –AN – 0.17 0.06 0.11 0 0.11 – – 0.44 – –AS – 0.5 0.11 0.24 0.28 0.55 – – 0.11 – –AU – 0.56 0.44 0.22 0.06 0.11 – – 0.06 – –EU – 0.5 0.72 0.56 0.07 0.2 – – 0.05 – –IN – 0.31 0.67 0.33 0.67 0.28 – – 0.1 – –NA – 0.63 0.92 0.56 0.73 0.61 – – 0.2 – –NEO – – – – – – – – – – –NZ – – – – – – – – – – –TSA – 0.75 0.53 0.67 0.47 0.78 0.57 – – – –SEAS – – – – – – – – – – –SCH – – – – – – – – – – –

MLEO AF AN AS AU EU IN NA NEO NZ TSA SEAS SCH

AF 0 0 0 0 0 0.17 – 0 0 0 –AN – 0.25 0.38 0.13 0.13 0.5 – 0.13 0.13 –AS – 0.67 0.05 0.46 0.17 0.52 – 0.2 0.14 0 –AU – 0.67 0.5 0.05 0 0.1 – 0.1 0.05 0 –EU – 0.5 0.81 0.5 0.25 0.51 – 0.1 0.14 0 –IN – 0.17 0.75 0.25 0.75 0.42 – 0.1 0.08 0 –NA – 0.67 0.85 0.6 0.88 0.75 – 0 0.31 0 –NEO – – – – – – – – – – –NZ – 0.33 0.63 0.5 0.5 0.38 0.63 – 0 0 –TSA – 0.5 0.59 0.5 0.59 0.25 0.71 – 0.5 0 –SEAS – 0.33 0.57 0.14 0.71 0.29 0.86 – 0.14 0.29 –SCH – – – – – – – – – – –

OLIGO AF AN AS AU EU IN NA NEO NZ TSA SEAS SCH

AF – 0.03 0.04 0 0.04 0 – – 0 – 0AN – – – – – – – – – – –AS 0.81 – 0 0.54 0.04 0.55 – – 0.11 – 0.57AU 0.11 – 0.33 0.05 0.57 0 – 0.05 0.1 – 0EU 0.73 – 0.88 0.56 0.04 0.43 – – 0.19 – 0.48IN 0.45 – 0.47 0.22 0.42 0.08 – – 0.08 – 0.05NA 0.82 – 0.84 0.22 0.76 0.53 – – 0.12 – 0.52NEO – – – – – – – – – – –NZ – – – 0 0 – – – – – –TSA 0.64 – 0.55 0.44 0.63 0.53 0.58 – 0.5 – 0.29SEAS – – – – – – – – 0.14 – –SCH 0.36 – 0.93 0.11 0.86 0.36 0.93 – – 0.79 –

EMMIO AF AN AS AU EU IN NA NEO NZ TSA SEAS SCH

AF – 0.07 0.08 0.21 0.3 0.02 0.08 0 0.17 – 0.21AN – – – – – – – – – – –AS 0.56 – 0.15 0.72 0.13 0.63 0.15 0.13 0.17 – 0.5AU 0.2 – 0.3 0.38 0.23 0.08 0 0 0.17 – 0EU 0.74 – 0.98 0.5 0.17 0.71 0.15 0.25 0.5 – 0.43IN 0.67 – 0.53 0.4 0.63 0.13 0.08 0 0.33 – 0.64NA 0.44 – 0.82 0.4 0.95 0.49 0.08 0 0.17 – 0.29NEO 0.56 – 0.67 0.44 1 0.78 0.78 0 0 – 0.08NZ 0.43 – 0.57 0.43 0.86 0.57 0.43 0.43 0 – 0TSA 0.5 – 0.67 0.5 0.83 0.67 0.67 0.33 0.17 – 0SEAS – – – – – – – – – – –SCH 0 – 1 0.1 1 0.4 0.8 0.22 0.14 0.17 –

LMPL AF AN AS AU EU IN NA NEO NZ TSA SEAS SCH

AF – 0.07 0.08 0.1 0.11 0.09 0.15 0.06 – 0.13 0.12AN – – – – – – – – – – –AS 0.53 – 0 0.64 0.14 0.67 0.15 0.16 – 0 0.73AU 0.25 – 0.25 0.17 0 0 0.08 0.25 – 0 0EU 0.67 – 0.9 0.38 0.13 0.73 0.24 0.19 – 0.06 0.58IN 0.8 – 0.6 0.25 0.8 0.05 0.11 0.03 – 0.65 0.2NA 0.47 – 0.82 0.13 0.89 0.53 0.09 0.06 – 0 0.38NEO 0.66 – 0.52 0.38 0.66 0.41 0.48 0.03 – 0.06 0.11NZ 0.5 – 0.5 0.75 0.66 0.35 0.42 0.38 – 0 0.03TSA – – – – – – – – – 0 0SEAS 0.86 – 0.43 0.14 0.71 1 0.29 0.43 0.29 – 0SCH 0.62 – 0.95 0.25 0.93 0.57 0.86 0.38 0.29 – 0.14

AF, Africa; AN, Antarctica; AS, temperate Asia; AU, Australia; EU, Europe; IN, India; NA, North America; NEO,Neotropics; NZ, New Zealand; TSA, temperate South America; SCH, south China; SEAS, Southeast Asia. PAEE,Palaeocene–early Eocene; MLEO, middle–late Eocene; OLIGO, Oligocene; EMMIO, early–middle Miocene; LMPL,late Miocene–Pleistocene.



cophenetic correlations for all woody angiosperms and rosidsare 0.54 and 0.64, respectively, showing that the phenograms donot accurately reflect the variation in similarity among thefloras. In the cluster for all woody angiosperms, the NH clusteris retrieved as in the generic-level analysis, but now includes themiddle to late Eocene Southeast Asian flora and the early–

middle Miocene south Chinese flora. The Neotropical floras areintermingled with African and Indian floras, as part of thePalaeotropical cluster. The Gondwanan cluster includes all Aus-tralian, New Zealand, temperate South American and Antarcticfloras, with the present Southeast Asian flora nested in thisgroup. Independent clustering for the Palaeogene (cophenetic

stress = 0.29

Coordinate 1

AU

AU

AUAU

AN IN

AN

AUAU

IN

IN

ININ

AF

AFAF

AF

INAF

NEO

NZ

NZ

NZTSA

TSA

TSATSA

TSA

NA

NANA

NA

NA

NA

NEO

NEO

NZ

ASAS

AS

AS

ASAS

EU

EU

EUEU

EUEUSCH

SCH

SCHSCH

SEAS

SEAS

SEAS

-0.25 -0.20 -0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

Coor

dina

te 2

0.16

0.12

0.08

0.04

0.00

-0.04

-0.08

-0.12

-0.16

-0.20

Palaeotropical floras

Gondwanan floras

stress = 0.36

Coordinate 1

AU

AU

AU AU

AN

IN

AN

AU

AU

IN

IN

IN

IN

AF

AFAF

AF

IN

NEO

NZ

NZNZ

TSA

TSA

TSA

TSA

NA

NA

NA

NA

NA

NA

NEO

NEO

NZ

AS ASAS

AS

ASAS

EUEU

EUEU

EU

EU

SCH

SCH

SCH

SCH

SEAS

SEAS

SEAS

-0.15 -0.10 -0.05 -0.00 0.05 0.10 0.15 0.20 0.25

Coor

dina

te 2

0.16

0.12

0.08

0.04

0.00

-0.04

-0.08

-0.12

-0.16

-0.20

Palaeotropical floras

Gondwanan floras

TSA

Northern Hemisphere floras

Northern Hemisphere floras

A

B

Palaeocene-early Eocene middle-late Eocene Oligocene early-middle Miocene late Miocene-Pleistocene

Figure 1 Ordination using non-metric multidimensional scaling based on the !sim algorithm for all woody taxa. (a) Generic-level analysis:stress = 0.29, R2 for axis 1 = 0.30 and axis 2 = 0.22. (b) Family-level analysis: stress = 0.36, R2 for axis 1 = 0.38 and axis 2 = 0.13. Key: AN,Antarctica; AF, Africa; AS, temperate Asia; AU, Australia; EU, Europe; IN, India; NA, North America; NEO, Neotropics; NZ, New Zealand;TSA, temperate South America; SCH, south China; SEAS, Southeast Asia.

Y. Xing et al.


correlation 0.70) and the Neogene (cophenetic correlation 0.74)are consistent with the overall pattern (Fig. 3b,c). In the analysisfor the rosids, the NH cluster is retrieved, but now includes thepresent south China. The Oligocene Indian flora is sister to NHfloras and other Palaeotropical floras (Fig. S4 in Appendix S1).The Cenozoic temperate South American floras are separatedwith other Gondwanan floras in the Gondwanan cluster.

Dissimilarities among floras

According to NMDS and clustering, both geography and timeinfluence the similarities among the continental floras, but thegeographical (continental) effect is stronger than the time effectat both family and generic levels. Simply, floras are similarbecause they come from the same region rather than from the

same time period. There is no significant influence of time onthe intercontinental similarity at family and generic levelsamong floras globally (Fig. 4a, Table S1 in Appendix S2): earlyCenozoic floras are globally as (dis-)similar as late Cenozoicfloras. As expected, there is a tendency towards increased simi-larities among NH floras through the Cenozoic, this is particu-larly evident at generic level (Fig. 4b,e, Table S2 in Appendix S2).This is in contrast to the Gondwanan floras, in which the diver-gence increases during the Cenozoic (Fig. 4c,f, Table S3 inAppendix S2).

DISCUSSION

We show that at both generic and family levels three regionalfloras are retrieved for all woody angiosperms and the rosids. The

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

AS#LMPL

EU#MLEO

TSA#PAEE

SCH#LMPL

TSA#OLIGO

NZ#EMMIO

AF#OLIGO

TSA#EMMIOAN#MLEO

AU#OLIGO

IN#MLEO

EU#PAEE

SCH#EMMIO

NZ#MLEO

NZ#LMPL

NA#PAEE

AF#PRE

AS#MLEO

TSA#PRE

EU#PREEU#OLIGO

AU#LMPL

NA#PRENA#LMPL

AF#MLEO

IN#LMPL

AS#OLIGO

NA#MLEO

AU#MLEO

NA#OLIGO

IN#OLIGO

EU#LMPL

AS#EMMIO

NEO#PRE

SEAS#LMPL

AS#PRE

AF#EMMIO

SCH#OLIGO

NEO#LMPL

SEAS#MLEO

AU#EMMIO

TSA#MLEO

AS#PAEE

NA#EMMIO

IN#PAEE

IN#PRESCH#PRE

AF#LMPL

AU#PAEE

EU#EMMIO

SEAS#PRE

IN#EMMIO

NZ#PRE

AN#PAEE

AU#PRE

NEO#EMMIO

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

AU#PAEE

AF#OLIGO

SCH#OLIGO

TSA#PAEE

NA#PAEE

AS#PAEE

IN#PAEE

NA#OLIGO

AU#MLEO

SEAS#MLEO

AN#MLEO

TSA#MLEO

EU#PAEE

AS#OLIGO

EU#MLEO

IN#OLIGO

TSA#OLIGO

IN#MLEO

AU#OLIGO

AN#PAEE

AF#MLEO

AS#MLEO

NZ#MLEO

NA#MLEOEU#OLIGO

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

IN#LMPL

NEO#LMPL

AS#EMMIO

IN#EMMIO

NA#EMMIO

SCH#LMPL

NA#LMPL

AS#LMPL

AF#EMMIO

TSA#EMMIO

AU#EMMIONZ#LMPL

NEO#EMMIO

AF#LMPL

AU#LMPL

SEAS#LMPLSCH#EMMIO

NZ#EMMIO

EU#EMMIOEU#LMPL

Similarity

Similarity

Similarity

A B

C

Gondw

anaN

. Hem

ispherePalaeotropic

Gondw

anaN

. Hem

ispherePalaeotropic

N. H

emisphere

PalaeotropicG

ondwana 1

Gondw

ana 2

Figure 2 Phenogram of all woody angiosperm recorded for each flora (region–time period combination), based on the !sim index andclustered using UPGMA at the generic level. (a) Whole Cenozoic analysis (cophenetic correlation = 0.76). (b) Palaeogene analysis(cophenetic correlation = 0.88). (c) Neogene analysis (cophenetic correlation = 0.87). Key: AN, Antarctica; AF, Africa; AS, temperate Asia;AU, Australia; EU, Europe; IN, India; NA, North America; NEO, Neotropics; NZ, New Zealand; TSA, temperate South America; SCH,South China; SEAS, Southeast Asia; PAEE, Palaeocene–early Eocene; MLEO, middle–late Eocene; OLIGO, Oligocene; EMMIO, early–middleMiocene; LMPL, late Miocene–Pleistocene; PRE, present.



most narrowly defined, and consistently retrieved, is the NHcluster, which includes all the floras of Europe, temperate Asiaand North America. Oligocene and late Miocene south Chinesefloras are also grouped in the NH cluster. Straddling the equatoris the Palaeotropical cluster, including all African, Indian, South-east Asian and early–middle Miocene Chinese floras. This clusterhas a broader scatter than the NH one. The Gondwanan clusterincludes the Antarctic, Australian, Neotropical, temperate SouthAmerican and New Zealand floras. There is no significant influ-ence of time on the intercontinental similarity at family andgeneric levels among floras when all floras are considered.However, it is evident that there is an increase in similarity amongNH floras while there is some evidence that younger Gondwananfloras are more dissimilar than the older ones.

Three floras

The NH cluster matches the Holarctic kingdom of Takhtajan(1986) and Morrone (2002) and the Arcto-Tertiary flora of

Engler (1879–82). Ecologically, this also matches the northerntemperate region (Rubel & Kottek, 2010). However, during mostof the Cenozoic at least the southern half of this region wastropical, along the northern border of the Tethys. It seems morelikely, therefore, that this is better seen as a geographical regionthan a climatic one.

Although the three NH continents were separated by theAtlantic and Pacific oceans during most of Cenozoic and by theTurgai Strait during the Palaeogene, biotic exchanges were facili-tated by the North Atlantic and Beringian land bridges (Tiffney& Manchester, 2001). According to geological evidence, therewas no direct land connection between Greenland and Europeafter the early Eocene; nevertheless, a shallow sea might havelinked the Arctic Ocean and the North Sea allowing continuousbiotic exchange between Greenland and Europe (Marincovichet al., 1990; Tiffney & Manchester, 2001). The Beringian LandBridge that existed from the Palaeocene until its closure in thelate Miocene and the early Pliocene has been invoked to explainthe Cenozoic distribution patterns of mammals (Bowen et al.,

0 0.1 0.2 0.3 0.4 0.5

SCH#OLIGO

AF#LMPL

N A # O L I G O

TSA#OLIGO

N A # E M M I O

I N # M L E O

NZ#LMPL

NEO#LMPL

TSA#MLEO

AF#PRE

NA#PRE

A U # M L E O

IN#LMPL

EU#LMPL

AU#PRE

SEAS#PRE

AS#EMMI O

AS#MLEO

N Z # E M M I O

SEAS#MLEO

IN#OLIGO

AF#OLIGO

SCH#PRE

EU#OLIGO

I N # E M M I O

S C H # E M M I O

IN#PAEE

EU#PRE

AS#LMPL

EU#PAEE

NEO#PRE

A F # E M M I O

A N # M L E O

AU#LMPL

E U # E M M I O

IN#PRE

NA#PAEE

NEO#EMM I O

NA#LMPL

SCH#LMPL

NZ#PRE

SEAS#LMPL

AS#PAEE

TSA#PRE

AS#OLIGO

AU#PAEE

N A # M L E O

A U # E M M I O

EU#MLEO

AS#PRE

TSA# E M M I O

TSA#PAEE

AN#PAEE

N Z # M L E O

AU#OLIG O

Similarity

Gondw

anaN

. Hem

ispherePalaeotropic

A

0 0.1 0.2 0.3 0.4 0.5 0.6

N Z # M L E O

A U # P A E ETSA# M L E O

A N # P A E E

A U # O L I G O

I N # P A E E

A F # O L I G O

S C H # O L I G O

SEAS#MLEO

I N # M L E O

E U # O L I G O

TSA# O L I G O

TSA# P A E E

A N # M L E O

A U # M L E O

N A # O L I G O

E U # M L E O

A S # O L I G O

A S # M L E O

I N # O L I G O

N A # M L E O

N A # P A E EAS#PAEEEU#PAEE

B

TSA#EMMIO

SCH#LMPL

AU#LMPL

EU#EMMI O

AF#EMMIO

IN#LMPL

NEO#LMPL

N A # E M M I O

A U # E M M I O

AS#EMMIO

N Z # E M M I O

NZ#LMPL

NEO#EMMIO

I N # E M M I OSCH#EMMIO

AF#LMPL

AS#LMPL

NA#LMPL

EU#LMPL

SEAS#LMPL

Similarity

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7Similarity

C

N. H

emisphere

Gondw

anaN

. Hem

isphereG

ondwana

Palaeotropic

Figure 3 Phenogram of angiosperm recorded for each flora (region–time period combination), based on the !sim index and clusteredusing UPGMA at the family level. (a) Whole Cenozoic analysis, the cophenetic correlation is 0.54. (b) Palaeogene analysis, the copheneticcorrelation is 0.70. (c) Neogene analysis, the cophenetic correlation is 0.74. Abbreviations are the same as in Fig. 2.

Y. Xing et al.


2002). Extensive dispersal events through these two land bridgeshave been documented by both fossil and molecular evidence ofseed plants (e.g. Manchester, 1999; Wen, 1999). The late Eoceneretreat of the Turgai Strait (Tiffney & Manchester, 2001) may belinked to extensive biological exchanges between Asia andEurope (Denk et al., 2012). This is consistent with our resultsthat there was an increasing similarity among the NH florasthrough the Cenozoic at both family and generic levels (Fig. 4).The European Palaeocene flora is isolated within the NH cluster,supporting the hypothesis that western Europe was an archi-pelago in the Palaeocene, and geographically isolated by theopening North Atlantic, the Turgai Strait and the Tethys (Rögl,1999). This period of isolation ended as the Turgai Strait driedout (Tiffney & Manchester, 2001). Though south China is nowincluded in the Palaeotropical kingdom of Takhtajan (1986),Oligocene south China is still grouped with NH floras, and thesimilarities between the Oligocene floras of south China andthose of India and Africa are very low (Table 2).

The Palaeotropical flora, including the African, Indian,Southeast Asian and South Chinese floras, coincides with thePalaeotropical kingdom of Takhtajan (1986). It is unclear howisolated the Indian biota was between its separation from

Gondwana and its docking with Asia at c. 50 Ma (Rowley, 1998;Zhu et al., 2005). However, recent evidence suggests that Indiaremained close to Africa and Madagascar during its northwardjourney (Briggs, 2003), allowing biotic exchange. There is bothfossil (Morley, 2000) and molecular biogeographical (Contiet al., 2002; Rutschmann et al., 2004; Ali et al., 2012) evidencefor such an exchange. This is consistent with our grouping of theAfrican floras with Indian ones throughout the Cenozoic. Theearliest fossil record for Southeast Asia is from the late Eoceneand it is grouped with the Palaeotropical floras, indicating theexpansion of Palaeotropical elements into Southeast Asia at nolater than the late Eocene, and probably from there to southChina by the Neogene. The earliest fossil flora showing clearSino-Indian affinity was found in the middle Miocene of south-eastern China (Jacques et al., 2015); however, there is no evi-dence of clear Indian affinity for the south-western ChineseMiocene floras. Thus, they suggest that immigration ofPalaeotropical elements into China was through Southeast Asia(Jacques et al., 2015). Tropical floras are relatively undersampledin the fossil record, consequently our postulation of aPalaeotropical flora is based on a weaker foundation than that ofa Northern Hemisphere flora.

Figure 4 Interregional similarities for each time period: (a)–(c) generic-level similarity; (d)–(f) family-level similarity. Parts (a) and (d)show the mean and ranges of the similarities for all interregional comparisons, (b) and (e) the similarities among the Northern Hemisphereregions, and (c) and (f) the similarities among the Gondwana regions. The solid dots indicate the mean, the lines indicate the standarddeviation. Key: PAEE, Palaeocene–early Eocene; MLEO, middle–late Eocene; OLIGO, Oligocene; EMMIO, early–middle Miocene; LMPL,late Miocene–Pleistocene.



Although India and Africa were also part of Gondwanaduring the Triassic, by the end of the Jurassic they had beenisolated by the opening southern Atlantic and Indian oceans(Ali & Aitchison, 2008). Consequently Palaeogene Gondwanaincluded modern South America, Antarctica and Australasia.The land connections between Antarctica, Australia and SouthAmerica were severed towards the end of the Palaeogene by theopening of the Drake Passage (Sher & Martin, 2006) and theSouthern Ocean between Australia and Antarctica (Lawver et al.,1992). In our analysis the floras of Australia, Antarctica, NewZealand and both temperate and tropical parts of SouthAmerica group together. This is consistent with the recent studyby Kooyman et al. (2014) that Australia, New Zealand, Patagoniaand Antarctica shared a Gondwanan history. However, theextant temperate South American flora is very different from theNeotropical and Australasian floras (Simpson, 2014). Kooymanet al. (2014) attributed this to Neogene extinctions in this region(e.g. Casuarina and Eucalyptus; Zamaloa et al., 2006; Gandolfoet al., 2011), whereas Simpson (2014) suggested that thePatagonian divergence may be the result of the evolution ofautochthonous elements through the Cenozoic. The relation-ships of the Neotropics with other floras also remains unclear, asthe Neotropical floras are located among the Gondwanan,Palaeotropical and NH floras in the NDMS analyses. Cox (2001)grouped the temperate and tropical parts of South America intoone kingdom. In contrast, Crisci et al. (1991) argued that theNeotropics shows more Palaeotropical affinities. This is consist-ent with the result obtained from recent molecular phylogeneticstudies (Christenhusz & Chase, 2013), and is reflected in thesystem of Morrone (2002), who grouped all tropical regions intothe Holotropical kingdom. Unfortunately, the poor sampling ofGondwanan and tropical regions at both spatial and taxonomiclevels precludes a robust solution to this problem.

Barriers versus climate

Our data provide strong evidence supporting the importanceof barriers to dispersal in the development of globalregionalization patterns, and so of a vicariance model. The florasare grouped by region and not by time period. If climate weredominant, then floras from the hot Eocene should grouptogether with the recent equatorial floras, and northern andsouthern temperate floras should group together. At the broad-est level, the three major biogeographical clusters are separatedby (palaeo-)oceans. The Tethys separated the NH from thePalaeotropical and Gondwanan clusters, and the southernAtlantic and Indian oceans separate the Palaeotropical clusterfrom Gondwanan cluster. The width of the barrier also seems tofit the degree of divergence, with the southern continents havinga much lower similarity among themselves than the northerncontinents have, which is consistent with the width of the south-ern versus the northern oceans. There is also a possibility thatthere is also a lag time of several million years. The Tethysdisappeared by the late Miocene, but its effects are still seen notonly between Europe and Africa but also between North andSouth America, and between Asia and Australia. Although the

time resolution in our data is fairly coarse, it seems as if therewas a similar lag-time between the closure of the Turgai Straitand the convergence of the Asian and European floras.

There are also indications that climate played a role. Our threemajor groups could also be interpreted as northern temperate(= NH), equatorial (Palaeotropical) and south temperate(Gondwanan) bioclimates. The Palaeotropical flora includesregions from the Asian continent, which abut onto the NHfloras. The boundary between these is clearly climatic. Furtherweak evidence comes from the Neotropics, which show a closeaffinity with the Palaeotropical floras, particularly at the familylevel (Christenhusz & Chase, 2013). For a critical test of theclimate versus barrier argument we should cluster the assem-blages (the sites and their attendant floras), but unfortunatelythe data are not adequate for this. Furthermore, many climati-cally interesting parts of planet have few fossil sites (e.g. thesouthern African Cape, south-western Australia, Indonesia, theAmazon Basin), and so their past phytogeographical affinitiescannot be explored using the approach employed here. Thenumber of families and genera sampled from most fossil assem-blages is actually very small, and as a result there is little overlapamong the assemblage floras. Such a low overlap makes it moredifficult to find robust solutions to the clustering. The alterna-tive solution, grouping fossil sites by palaeoclimatic zone, isconfounded by the very incomplete palaeoclimate reconstruc-tions, which leaves many regions over many epochs as unknown(e.g. Utescher & Mosbrugger, 2007).

Impact of time, palaeobarriers and continental drifton dissimilarity among floras

The increase in divergence among the Gondwanan florastowards the present may be an effect of long-term isolation ofthese floras by oceans and multiple regional extinction events,and is consistent with predictions of increased divergencethrough time. The increase in similarities in the NH florasduring the Neogene may be due to extensive biotic exchangesamong three continents, suggesting that at the beginning of theCenozoic the angiosperm floras were already regionalized.

CONCLUSIONS

The modern regionalization of the global woody angiospermflora was already evident at the beginning of the Cenozoic, andreflects the major Cenozoic oceanic barriers (Tethys, Atlanticand Indian oceans). The much larger impact of the Palaeoceneand early Neogene connectivities (South American–Antarctica–Australasia, North America–Europe–Asia) rather than thelate Neogene–Quaternary connectivities (North America–SouthAmerica, Europe–Africa, Asia–Australia) suggests a slowresponse time to migration possibilities. The importance of abroad and enduring connection among continents to homog-enize the floras is also illustrated by the greater similarity amongthe floras of the NH compared with those of the SouthernHemisphere. The floras do not group by climate, except possiblythe Neotropical and Southeast Asian floras. All this indicates

Y. Xing et al.


that geography, rather than climate, is the primary driver in theglobal regionalization of the woody angiosperm flora, and thatextensive long-distance dispersal may not be so important at thisscale. Regionalization suggests that the global Cenozoic woodyangiosperm flora can be seen as three radiations: a well-integrated NH radiation, a highly divergent Gondwanan radia-tion and a Palaeotropical radiation.

ACKNOWLEDGEMENTS

We thank the Swiss National Science Foundation for funding(Grant 31003A_130847 to H.P.L.) and U.S. National ScienceFoundation grants (DEB 0918932 and DEB 0830020 to M.A.G.).We would like to thank the editor and three anonymous reviewersfor constructive comments and L.Coghill, J.Havstad,S.Leavitt,S.Lidgard, R. Ree, R. Sadleir and B. Sterner from the Field Museumof Natural History, Chicago for helpful discussions.

REFERENCES

Akhmetiev, M.A. & Beniamovski, V.N. (2009) Paleogene floralassemblages around epicontinental seas and straits in north-ern central Eurasia: proxies for climatic and paleogeographicevolution. Geologica Acta, 7, 297–309.

Akhmetiev, M.A., Zaporozhets, N.I., Benyamovskiy, V.N.,Aleksandrova, G.N., Iakovleva, A.I. & Oreshkina, T.V. (2012)The Paleogene history of the western Siberian seaway – aconnection of the Peri-Tethys to the Arctic Ocean. AustrianJournal of Earth Sciences, 105, 50–67.

Ali, J.R. & Aitchison, J.C. (2008) Gondwana to Asia: plate tec-tonics, paleogeography and the biological connectivity of theIndian sub-continent from the Middle Jurassic through latestEocene (166–35 Ma). Earth-Science Reviews, 88, 145–166.

Ali, S.S., Yu, Y., Pfosser, M. & Wetschnig, W. (2012) Inferences ofbiogeographical histories within subfamily Hyacinthoideaeusing S-DIVA and Bayesian binary MCMC analysis imple-mented in RASP (Reconstruct Ancestral State in Phylogenies).Annals of Botany, 109, 95–107.

Bowen, G.J., Clyde, W.C., Koch, P.L., Ting, S., Alroy, J.,Tsubamoto, T., Wang, Y. & Wang, Y. (2002) Mammalian dis-persal at the Paleocene/Eocene boundary. Science, 295, 2062–2065.

Briggs, J.C. (2003) The biogeographic and tectonic history ofIndia. Journal of Biogeography, 30, 381–388.

Christenhusz, M.J. & Chase, M.W. (2013) Biogeographical pat-terns of plants in the Neotropics – dispersal rather than platetectonics is most explanatory. Botanical Journal of the LinneanSociety, 171, 277–286.

Conti, E., Eriksson, T., Schonenberger, J., Sytsma, K.J. &Baum, D.A. (2002) Early Tertiary out-of-India dispersal ofCrypteroniaceae: evidence from phylogeny and moleculardating. Evolution, 56, 1931–1942.

Cox, C.B. (2001) The biogeographic regions reconsidered.Journal of Biogeography, 28, 511–523.

Cox, C.B. (2010) Underpinning global biogeographical schemeswith quantitative data. Journal of Biogeography, 37, 2027–2028.

Crisci, J.V., Cigliano, M.M., Morrone, J.J. & Roig-Junent, S.(1991) Historical biogeography of southern South America.Systematic Biology, 40, 152–171.

Crisp, M.D., Arroyo, M.T.K., Cook, L.G., Gandolfo, M.A.,Jordan, G.J., McGlone, M.S., Weston, P.H., Westoby, M., Wilf,P. & Linder, H.P. (2009) Phylogenetic biome conservatism ona global scale. Nature, 458, 754–756.

de Candolle, A.P. (1820) Essai élémentaire de géographiebotanique. F. G. Levrault, Paris.

Denk, T., Grimsson, F. & Zetter, R. (2012) Fagaceae from theearly Oligocene of Central Europe: persisting new world andemerging old world biogeographic links. Review of Palaeo-botany and Palynology, 169, 7–20.

Donoghue, M.J. (2008) A phylogenetic perspective on thedistribution of plant diversity. Proceedings of the NationalAcademy of Sciences USA, 105, 11549–11555.

Eldrett, J.S., Greenwood, D.R., Harding, I.C. & Huber, M.(2009) Increased seasonality through the Eocene toOligocene transition in northern high latitudes. Nature, 459,969–973.

Gandolfo, M.A., Hermsen, E.J., Zamaloa, M.C., Nixon, K.C.,González, C.C., Wilf, P., Cúneo, N.R. & Johnson, K.R. (2011)Oldest known Eucalyptus macrofossils are from SouthAmerica. PLoS ONE, 6, e21084.

Good, R. (1953) The geography of the flowering plants.Longmans, Green & Co., London.

Hamilton, W. (1983) Cretaceous and Cenozoic history of thenorthern continents. Annals of the Missouri Botanical Garden,70, 440–458.

Hammer, Ø. (2001) PAST: paleontological statistics softwarepackage for education and data analysis. PalaeontologiaElectronica, 4, art. 4.

Hill, R.S. (2001) Biogeography, evolution and palaeo-ecology of Nothofagus (Nothofagaceae): the contributionof the fossil record. Australian Journal of Botany, 49, 321–332.

Jacques, F.M., Shi, G., Su, T. & Zhou, Z. (2015) A tropical forestof the middle Miocene of Fujian (SE China) reveals Sino-Indian biogeographic affinities. Review of Palaeobotany andPalynology, 216, 76–91.

Kooyman, R.M., Wilf, P., Barreda, V.D., Carpenter, R.J., Jordan,G.J., Sniderman, J.K., Allen, A., Brodribb, T.J., Crayn, D. &Feild, T.S. (2014) Paleo-Antarctic rainforest into the modernOld World tropics: the rich past and threatened future of the‘southern wet forest survivors’. American Journal of Botany,101, 2121–2135.

Kreft, H. & Jetz, W. (2010) A framework for delineating biogeo-graphical regions based on species distributions. Journal ofBiogeography, 37, 2029–2053.

Lawver, L.A., Gahagan, L.M. & Coffin, M.F. (1992) The devel-opment of paleoseaways around Antarctica. Antarctic ResearchSeries, 56, 7–30.

Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L.L. &Hernández-Hernández, T. (2015) A metacalibrated time-treedocuments the early rise of flowering plant phylogeneticdiversity. New Phytologist, 207, 437–453.



Manchester, S.R. (1999) Biogeographical relationships of NorthAmerican tertiary floras. Annals of the Missouri BotanicalGarden, 86, 472–522.

Marincovich, L. & Gladenkov, A.Y. (2001) New evidence for theage of Bering Strait. Quaternary Science Reviews, 20, 329–335.

Marincovich, L., Brouwers, E.M., Hopkins, D.M. & McKenna,M.C. (1990) Late Mesozoic and Cenozoic paleogeographicand paleoclimatic history of the Arctic Ocean Basin, based onshallow marine faunas and terrestrial vertebrates. The geologyof North America. Vol. L. The Arctic Ocean region (ed. by A.Grantz, L. Johnson and J.F. Sweeney), pp. 403–426. GeologicalSociety of America, Boulder, CO.

Morley, R.J. (2000) Origin and evolution of tropical rain forests.Wiley, Chichester.

Morrone, J.J. (2002) Biogeographical regions under track andcladistic scrutiny. Journal of Biogeography, 29, 149–152.

Mosbrugger, V., Utescher, T. & Dilcher, D.L. (2005) Cenozoiccontinental climatic evolution of Central Europe. Proceedingsof the National Academy of Sciences USA, 102, 14964–14969.

Rowley, D.B. (1998) Minimum age of initiation of collisionbetween India and Asia north of Everest based on the subsid-ence history of the Zhepure Mountain section. Journal ofGeology, 106, 220–235.

Rögl, F. (1999) Mediterranean and Paratethys. Facts and hypoth-eses of an Oligocene to Miocene paleogeography (short over-view). Geologica Carpathica, 50, 339–349.

Rubel, F. & Kottek, M. (2010) Observed and projected climateshifts 1901–2100 depicted by world maps of the Köppen–Geiger climate classification. Meteorologische Zeitschrift, 19,135–141.

Rutschmann, F., Eriksson, T., Schönenberger, J. & Conti, E.(2004) Did Crypteroniaceae really disperse out of India?Molecular dating evidence from rbcL, ndhF, and rpl16 intronsequences. International Journal of Plant Science, 165(Suppl.4), S69–S83.

Scotese, C.R. (2001) Atlas of earth history. PALEOMAP Project.Department of Geology University of Texas at Arlington,Arlington, TX.

Sher, H.D. & Martin, E.E. (2006) Timing and climatic conse-quences of the opening of Drake Passage. Science, 312, 428–430.

Simpson, B.B. (2014) Whence the flora of southern SouthAmerica? Biases may distort our conclusions. Paleobotany andbiogeography: a festschrift for Alan Graham in his 80th year (ed.by W.D. Stevens, O.M. Montiel and P.H. Raven), pp. 338–366.Missouri Botanical Garden Press, St Louis, MO.

Sneath, P.H.A. & Sokal, R.R. (1973) Numerical taxonomy.Freeman, San Francisco, CA.

Takhtajan, A. (1986) Floristic regions of the world. University ofCalifornia Press, Berkeley, CA.

Tiffney, B. & Manchester, S. (2001) The use of geological andpaleontological evidence in evaluating plant phylogeographichypotheses in the Northern Hemisphere Tertiary. Interna-tional Journal of Plant Sciences, 162, S3–S17.

Tiffney, B.H. (1985) The Eocene North Atlantic land bridge: itsimportance in Tertiary and modern phytogeography of theNorthern Hemisphere. Journal of the Arnold Arboretum, 66,243–273.

Utescher, T. & Mosbrugger, V. (2007) Eocene vegetation pat-terns reconstructed from plant diversity – a global perspec-tive. Palaeogeography, Palaeoclimatology, Palaeoecology, 247,243–271.

Wen, J. (1999) Evolution of eastern Asian and eastern NorthAmerican disjunct distributions in flowering plants. AnnualReview of Ecology and Systematics, 30, 421–455.

Yin, A. & Harrison, T.M. (2000) Geologic evolution of theHimalayan-Tibetan orogen. Annual Review of Earth and Plan-etary Sciences, 28, 211–280.

Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. (2001)Trends, rhythms, and aberrations in global climate 65 Ma topresent. Science, 292, 686–693.

Zachos, J.C., Dickens, G.R. & Zeebe, R.E. (2008) An early Ceno-zoic perspective on greenhouse warming and carbon-cycledynamics. Nature, 451, 279–283.

Zamaloa, M.D.C., Gandolfo, M.A., González, C.C., Romero, E.J.,Cúneo, N.R. & Wilf, P. (2006) Casuarinaceae from the Eoceneof Patagonia, Argentina. International Journal of Plant Sci-ences, 167, 1279–1289.

Zhu, B., Kidd, W.S., Rowley, D.B., Currie, B.S. & Shafique, N.(2005) Age of initiation of the India–Asia collision in theeast-central Himalaya. Journal of Geology, 113, 265–285.

SUPPORTING INFORMATION

Additional supporting information may be found in the onlineversion of this article at the publisher’s web-site.

Appendix S1 Ordination and clustering of the rosids.Appendix S2 Comparisons of floral similarities through time.

BIOSKETCHES

Yaowu Xing studies Cenozoic diversification patternsof angiosperms using palaeontological and phylogeneticdata.

Maria A. Gandolfo studies Cretaceous and Tertiaryfloras of North and South America with emphasis onevolutionary aspects of the flowering plants.

H. Peter Linder is interested in the description andevolution of angiosperm diversity, particularly in theAfrican Cape flora, with a focus on the Restionaceaeand the grass subfamily Danthonioideae.

Editor: Greg Jordan

Y. Xing et al.


Documents

The Cenozoic biogeographical evolution of woody angiosperms inferred from fossil distributions