SEARCH

SEARCH BY CITATION

Keywords:

  • biodiversity hotspot;
  • biogeography;
  • conservation;
  • divergence time estimation;
  • molecular phylogenetics;
  • taxonomy

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

Madagascar is renowned for its unparalleled species richness and levels of endemism, which have led, in combination with species extinction caused by an unprecedented rate of anthropogenic deforestation, to its designation as one of the most important biodiversity hotspots. It is home to 10 650 species (84% endemic) of angiosperms in 1621 genera (19% endemic). During the last two centuries, botanists have focused their efforts on the provision of a taxonomic framework for the flora of the island, but much remains to be investigated regarding the evolutionary processes that have shaped Madagascan botanical diversity. In this article, we review the current state of phylogenetic and biogeographical knowledge of the endemic angiosperm genera. We also propose a new stratified biogeographical model, based on palaeogeographical evidence, allowing the inference of the spatio-temporal history of Madagascan taxa. The implications of past climate change and extinction events on the evolutionary history of the endemic genera are also discussed in depth. Phylogenetic information was available for 184 of the 310 endemic genera (59.3%) and divergence time estimates were available for 67 (21.6%). Based on this evidence, we show the importance of phylogenetic clustering in the assemblage of the current Madagascan diversity (26% of the genera have a sister lineage from Madagascar) and confirm the strong floristic affinities with Africa, South-East Asia and India (22%, 9.1% and 6.2% of the genera, respectively). The close links with the Comoros, Mascarenes and Seychelles are also discussed. These results also support an Eocene/Oligocene onset for the origin of the Madagascan generic endemic flora, with the majority arising in the Miocene or more recently. These results therefore de-emphasize the importance of the Gondwanan break-up on the evolution of the flora. There is, however, some fossil evidence suggesting that recent extinctions (e.g. Sarcolaenaceae, a current Madagascan endemic, in southern Africa) might blur vicariance patterns and favour dispersal explanations for current biodiversity patterns. © 2013 The Linnean Society of London


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

Madagascar is located in the south-western Indian Ocean and is a significant distance from other large landmasses, such as Africa (450 km), India (3800 km), Indonesia (5600 km) and Australia (6800 km). The unique richness of the Madagascan biodiversity and its unparalleled levels of endemism have been acknowledged since the first naturalists set foot on the island in the 1700s (see, for example, Perrier de la Bâthie, 1936; Goodman & Benstead, 2005; Yoder & Nowak, 2006). As an example of this unique diversity, Madagascar is home to 11 220 species of vascular plants, > 80% of which are endemic (Callmander et al., 2011). The angiosperm component represents 95% of the whole flora, 10 650 species (84% endemic) distributed in 1621 genera (19% endemic) (Callmander et al., 2011). Madagascar has been designated one of the most important biodiversity hotspots, mainly because of the unprecedented rate of deforestation that threatens the survival of its biodiversity and therefore the sustainability of its ecosystems (Myers et al., 2000). The island retains < 10% of its natural habitats compared with their original extent before the arrival of the first humans about 2000 years ago (Goodman & Benstead, 2005; for a description of vegetation types, the factors which threaten them and their conservation importance, see Moat & Smith, 2007).

During the last two centuries, botanists have focused mainly on providing a taxonomic framework, and little is known about the evolutionary processes involved in shaping the extant Madagascan flora. The main barrier preventing a better understanding of these processes is the limited availability of well-supported molecular phylogenetic inferences that have been dated using robust calibrations from the fossil record. In this article, we provide a first step towards achieving this aim by reviewing the current state of knowledge of the endemic angiosperm genera. According to Callmander et al. (2011) and the Catalogue of the Vascular Plants of Madagascar (Madagascar Catalogue, 2012), there are 310 endemic genera of angiosperms in Madagascar (c. 19% of the generic diversity), comprising 1227 species (11.5% of the species richness) (Table 1). In these genera, one-third have only one species, but there are a few genera with > 20 species (e.g. Aspidostemon Rohwer & H.G.Richt., Lauraceae, with 31 species; Fig.  1A). We focus on these taxa because the current taxonomic and phylogenetic knowledge of the Madagascan angiosperm flora remains limited. Only species-level phylogenetic trees will allow a more accurate estimation of the number of colonization events to Madagascar by species of more widespread genera. For instance, results from the species-rich genera Pandanus Parkinson (Pandanaceae; Buerki et al., 2012a) and Impatiens L. (Balsaminaceae; Yuan et al., 2004) involved one and several events of colonization to the island, respectively. Therefore, by focusing on the endemic genera, we maximize the chances of addressing these issues using only monophyletic plant radiations. To infer the biogeographical affinities of this element of the flora with other areas, only the genera already included in a phylogenetic framework and retrieved as monophyletic will be considered further. In this review, we also propose a worldwide stratified biogeographical model, based on palaeogeographical evidence, that will prove fundamental to infer the spatio-temporal history of the Madagascan flora. Finally, the implications of past climate change on the origin of these elements of the flora are discussed in depth based on palaeobotanical evidence and divergence time estimation data.

figure

Figure 1. A, Comparison of species richness per genus between the Madagascan endemic genera (in grey) and the whole angiosperm flora on this island (in black). There are some nonendemic genera that were not included in this plot because of a lack of taxonomic knowledge leading to unreliable species richness estimations. The y axis was log transformed. See Table 1 for data on the Madagascan endemic genera and the Catalogue of the Vascular Plants of Madagascar (Madagascar Catalogue, 2012) for the other genera. The names of the genera containing the maximum number of species per category are also displayed. B, Phylogenetic positions of the endemic Madagascan genera following the Angiosperm Phylogeny Group (APG) III system (APG III, 2009). The number of families per order is also provided in parentheses, as well as the endemic families (including Didiereaceae).

Download figure to PowerPoint

Table 1. List of the Madagascan endemic genera of angiosperms based on the Catalogue of the Vascular Plants of Madagascar (Madagascar Catalogue, 2012). Abbreviations of the biogeographical areas: (A) Madagascar; (A′) the Seychelles archipelago, Mascarenes and Comoros; (B) India (including Sri Lanka); (C) mainland Africa; (D) Australia, New Guinea, New Caledonia and New Zealand; (E) South-East Asia and the Pacific islands; (F) Eurasia; (G) South America (Fig. 4). The species richness per genus refers to estimates performed by the Catalogue of the Vascular Plants of Madagascar's team. When several genera were clustered together in the phylogeny, we also scored the distribution of their sister lineage (see Araceae family below for an example). We also provide indications of when the phylogenetic status of the endemic genus was dubious and required further investigation (in this case, the genus was not included for the biogeographical inference). Finally, when a clade had a large range of distribution and included several genera, we did not provide the names of all the taxa
OrderFamilyGenusN speciesSister lineage(s)Reference(s)
TaxaDistribution
AlismatalesAraceaeArophyton7Carlephyton, ColletogyneACabrera et al. (2008)
AraceaeCarlephyton3ColletogyneACabrera et al. (2008)
AraceaeColletogyne1CarlephytonACabrera et al. (2008)
AraceaeArophyton + Carlephyton + Colletogyne TyphonodorumAA′CCabrera et al. (2008)
ApialesApiaceaeAndriana3PseudocarumACNicolas & Plunkett (2009)
ApiaceaeAnisopoda1
ApiaceaeBillburttia2African lineages of Peucedanum (all new genera)CMagee et al. (2009)
ApiaceaeCannaboides2
ApiaceaePhellolophium2CryptotaeniaCSpalik & Downie (2007)
ApiaceaePseudocannaboides1
ApiaceaeTana1
TorricelliaceaeMelanophylla7AralidiumEPlunkett et al. (1996)
ArecalesArecaceaeBeccariophoenix2Jubaeopsis, Voanioala, Jubaea, Butia, Parajubaea, Cocos, Attalea, Allagoptera, Syagrus, LytocaryumACDEGBaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeBismarckia1SatranalaABaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeLemurophoenix1Marojejya, DypsisAA′CBaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeMarojejya2DypsisAA′CBaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeMasoala2Taxa distributed in the Old WorldAA′BDEFBaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeSatranala1BismarkiaABaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeTahina1KerriodoxaEDransfield et al. (2008)
ArecaceaeVoanioala1Jubaea, Butia, Parajubaea, Cocos, Attalea, Allagoptera, Syagrus, LytocaryumDEGBaker et al. (2009); Baker and Couvreur (in press)
ArecaceaeBismarckia + Satranala Hyphaene, MedemiaBC
AsparagalesAsparagaceaeHerreriopsis1
OrchidaceaeAmbrella1
OrchidaceaeCymbidiella3CyrtopodiumGvan den Berg et al. (2002)
OrchidaceaeErasanthe1
OrchidaceaeEulophiella6
OrchidaceaeGrammangis2
OrchidaceaeImerinaea1Anguloa, Maxillaria, Adipe, Paphina, Houlettia, TrevoriaAA′CDEGGorniak et al. (2010)
OrchidaceaeLemurorchis1JumelleaAA′CCarlsward et al. (2006)
OrchidaceaeMegalorchis1
OrchidaceaeParalophia2
OrchidaceaePhysoceras10
OrchidaceaeTylostigma8
AsteralesAsteraceaeApodocephala10
AsteraceaeCatatia2
AsteraceaeCentauropsis8Hilliardiella, Polydora, VernoniaCKeeley et al. (2007)
AsteraceaeCloiselia4Dicoma, Pasaccardoa, MaclediumCOrtiz (2006)
AsteraceaeColobanthera1
AsteraceaeDecastylocarpus1
AsteraceaeDiaphractanthus1
AsteraceaeExomiocarpon1
AsteraceaeGladiopappus1
AsteraceaeGrangeopsis1
AsteraceaeHumeocline1
AsteraceaeIo1HubertiaAA′Pelser et al. (2010)
AsteraceaeMadagaster6A pantropical cladeAA′CDEGKaraman-Castro & Urbatsch (2009)
AsteraceaeOliganthes10
AsteraceaePsiadiella1
AsteraceaeRochonia4
AsteraceaeStenocline2
AsteraceaeSyncephalum5
AsteraceaeVernoniopsis3
CampanulaceaeDialypetalum5LobeliaAA′CDEFGTank & Donoghue (2010)
CanellalesCanellaceaeCinnamosma11WarburgiaCMarquinez et al. (2009)
WinteraceaeTakhtajania1Tasmania, Drimis, Zygogynum, PseudowinteraCDEGMarquinez et al. (2009)
CaryophyllalesAmaranthaceaeHenonia1
AsteropeiaceaeAsteropeia8PhysenaABrockington et al. (2009)
BarbeuiaceaeBarbeuia1Sampling not completeCuenoud et al. (2002)
DidiereaceaeAlluaudia6AlluaudiopsisAArakaki et al. (2011)
DidiereaceaeAlluaudiopsis2AlluaudiaAArakaki et al. (2011)
DidiereaceaeDecarya1Alluaudia, AlluaudiopsisAArakaki et al. (2011)
DidiereaceaeDidierea2Alluaudia, Alluaudiopsis, DecaryaAArakaki et al. (2011)
DidiereaceaeAlluaudia + Alluaudiopsis + Decarya + Didierea CalyptrothecaC
PhysenaceaePhysena2AsteropeiaABrockington et al. (2009)
TalinaceaeTalinella12Talinum triangulareGApplequist & Wallace (2001)
CelastralesCelastraceaeBrexiella5
CelastraceaeEvonymopsis1
CelastraceaeHartogiopsis1PleurostyliaBCDESimmons et al. (2012)
CelastraceaePolycardia12BrexiaAA′CSimmons et al. (2012)
CelastraceaePtelidium2
CelastraceaeSalvadoropsis1
CommelinalesCommelinaceaePseudoparis2
CommelinaceaeRhopalephora1AneilemaCGEvans et al. (2003)
CucurbitalesCucurbitaceaeAmpelosycios5Tricyclandra, Odosicyos (but genus may not be monophyletic)ACKocyan et al. (2007)
CucurbitaceaeLemurosicyos1Solena, BorneosicyosBEFKocyan et al. (2007)
CucurbitaceaeSeyrigia6TrochomeriopsisAKocyan et al. (2007)
CucurbitaceaeTrochomeriopsis1SeyrigiaAKocyan et al. (2007)
CucurbitaceaeSeyrigia + Trochomeriopsis Sister Coniandreae (excl. Dendrosicyos)AA′BCDE
CucurbitaceaeXerosicyos6SiolmatraGKocyan et al. (2007)
EricalesSapotaceaeCapurodendron25LecomtedoxaCAnderberg & Swenson (2003); Smedmark & Anderberg (2007)
SapotaceaeFaucherea11Part of clade 2 in a polytomyAnderberg & Swenson (2003)
SapotaceaeTsebona1
FabalesFabaceaeAlantsilodendron9Nested within DichrostachysABCDHughes et al. (2003)
FabaceaeBaudouinia6EligmocarpusABruneau et al. (2001, 2001,2008)
FabaceaeBrandzeia1DanielliaCBruneau et al. (2001, 2001,2008)
FabaceaeBrenierea1Bauhinia clade s.s.AA′BCDEFGSinou et al. (2009)
FabaceaeChadsia9MunduleaABCHu et al. (2002)
FabaceaeColvillea1Delonix, LemuropisumABCBruneau et al. (2001, 2001,2008)
FabaceaeDisynstemon1IndigofereaeAA′BCDEGSchrire et al. (2009)
FabaceaeDupuya2
FabaceaeEligmocarpus1BaudouiniaABruneau et al. (2001, 2001,2008)
FabaceaeLemurodendron1
FabaceaeLemuropisum1DelonixBCBruneau et al. (2001, 2001,2008)
FabaceaeMendoravia1KoompassiaDEBruneau et al. (2001, 2001,2008)
FabaceaeNeoapaloxylon3Not provided in the manuscriptFougere-Danezan et al. (2007)
FabaceaeNeoharmsia2Not provided in the manuscriptEdwards & Hawkins (2007)
FabaceaeOrmocarpopsis6OrmocarpumABCDELavin et al. (2001)
FabaceaePeltiera2J. N. Labat & M. Lavin (unpubl. data)
FabaceaePhylloxylon7IndigofereaeAA′BCDEGSchrire et al. (2009)
FabaceaePongamiopsis3NeodunniaHu et al. (2002)
FabaceaePyranthus6
FabaceaeSakoanala2
FabaceaeSylvichadsia4FordiaBEFSchrire et al. (2009)
FabaceaeTetrapterocarpon2Acrocarpus (but weak relationship)BEBruneau et al. (2001, 2001,2008)
FabaceaeBaudouinia + Eligmocarpus Sister to Dialiinae (excl. Poeppigia)ABCDEG
GentianalesApocynaceaeBaroniella9PentopetiaAA′Ionta & Judd (2007)
ApocynaceaeCalyptranthera10
ApocynaceaeCraspidospermum1MelodinusBDESimoes et al. (2007)
ApocynaceaeCryptostegia2CamptocarpusAA′Ionta & Judd (2007)
ApocynaceaeIschnolepis1Cryptostegia, CamptocarpusAA′Ionta & Judd (2007)
ApocynaceaePlectaneia3Pteralyxia, AlyxiaBDELivshultz et al. (2007)
ApocynaceaeSecamonopsis2Secamone, PervillaeaACLahaye et al. (2005)
ApocynaceaeStapelianthus6B. Gravendeel et al. (unpubl. data)
ApocynaceaeStephanostegia2
ApocynaceaeStephanotis5Used as outgroup taxonWanntorp et al. (2011)
GentianaceaeGentianothamnus1TachiadenusAKissling (2007); Kissling et al. (2009)
GentianaceaeKlackenbergia2OrnichiaAKissling (2007); Kissling et al. (2009)
GentianaceaeOrnichia3KlackenbergiaAKissling (2007); Kissling et al. (2009)
GentianaceaeTachiadenus11GentianothamnusAKissling (2007); Kissling et al. (2009)
GentianaceaeGentianothamnus + Klackenbergia + Ornichia + Tachiadenus ExacumABCDE
RubiaceaeAmphistemon2ThamnoldenlandiaAGroeninckx et al. (2010a)
RubiaceaeAstiella1PhialiphoraAGroeninckx et al. (2010b)
RubiaceaeBreonia20Gyrostipula, JanotiaAA′Bremer & Eriksson (2009); Manns & Bremer (2010)
RubiaceaeCanephora5PolysphaeriaAA′CDavis et al. (2007)
RubiaceaeCarphalea6Used as outgroup taxonGroeninckx et al. (2009a)
RubiaceaeChapelieria2
RubiaceaeFlagenium6
RubiaceaeGallienia1
RubiaceaeGomphocalyx1Phylohydrax, GomphocalyxACGroeninckx et al. (2010a)
RubiaceaeHomollea3
RubiaceaeHomolliella1
RubiaceaeJanotia1GyrostipulaAA′Bremer & Eriksson (2009); Manns & Bremer (2010)
RubiaceaeJovetia1
RubiaceaeLandiopsis1Kainulainen et al., unpublished data
RubiaceaeLathraeocarpa2Phylohydrax, GomphocalyxACGroeninckx et al. (2009b)
RubiaceaeLemyrea4
RubiaceaeMantalania3
RubiaceaeNematostylis1RazafimandimbisoniaAKainulainen et al. (2009)
RubiaceaeParacorynanthe2HymenodictyonBCEFBremer & Eriksson (2009); Manns & Bremer (2010)
RubiaceaePayera10Schismatoclada (but both genera are polyphyletic)Kruger et al. (2012)
RubiaceaePhialiphora2AstiellaAGroeninckx et al. (2010b)
RubiaceaePseudomantalania1
RubiaceaePyragra2
RubiaceaeRazafimandimbisonia5NematostylisAKainulainen et al. (2009)
RubiaceaeRobbrechtia2Embedded in a polytomyBremer & Eriksson (2009)
RubiaceaeSaldinia21Phylogenetic position not provided in studyBremer & Eriksson (2009); Rydin et al. (2008)
RubiaceaeSchismatoclada19DanaisAA′CBremer & Eriksson (2009); Rydin et al. (2008)
RubiaceaeSchizenterospermum4
RubiaceaeThamnoldenlandia1AmphistemonAGroeninckx et al. (2010a)
RubiaceaeAmphistemon + Thamnoldenlandia + Astiella + Phialiphora Houstonia, Stenaria, Oldenlandia, ArcytophyllumG
RubiaceaeNematostylis + Razafimandimbisonia1AlbertaC
LamialesAcanthaceaeAmbongia1
AcanthaceaeBenoicanthus2
AcanthaceaeBoutonia1
AcanthaceaeCamarotea2LeandriellaAMcDade et al. (2008)
AcanthaceaeCelerina1
AcanthaceaeDanguya1
AcanthaceaeDolichostachys1
AcanthaceaeForcipella6Leandriella, CamaroteaAMcDade et al. (2008)
AcanthaceaeIonacanthus1
AcanthaceaeLasiocladus7Barleria, CrabbeaACMcDade et al. (2008)
AcanthaceaeLeandriella2CamaroteaAMcDade et al., (2008)
AcanthaceaeMelittacanthus1
AcanthaceaePericalypta1
AcanthaceaePodorungia4
AcanthaceaePopulina2
AcanthaceaePseudodicliptera4
AcanthaceaePseudoruellia1
AcanthaceaeRitonia4
AcanthaceaeSphacanthus2
AcanthaceaeVavara1
AcanthaceaeVindasia1
AcanthaceaeZygoruellia1
AcanthaceaeCamarotea + Forcipella + Leandriella2ChlamydacanthusAC
BignoniaceaePerichlaena1
BignoniaceaePhylloctenium9
LamiaceaeAdelosa1
 LamiaceaeCapitanopsis3DauphineaAPaton et al. (2004)
LamiaceaeDauphinea1CapitanopsisAPaton et al. (2004)
LamiaceaeMadlabium1
LamiaceaeCapitanopsis + Dauphinea AeollanthusC
OrobanchaceaeLeucosalpa3E. Fischer et al. (unpubl. data)
OrobanchaceaePseudomelasma1
OrobanchaceaeRadamaea5E. Fischer et al. (unpubl. data)
OrobanchaceaeRhaphispermum1
OrobanchaceaeSieversandreas1E. Fischer et al. (unpubl. data)
OrobanchaceaeTetraspidium1
PedaliaceaeUncarina14Used as outgroup taxonJobson & Albert (2002)
PlantaginaceaeHydrotriche4The taxon sampling is not appropriateSchaferhoff et al. (2010)
ScrophulariaceaeAndroya1MyoporumDOxelman et al. (1999)
ScrophulariaceaeBarthlottia1The taxon sampling is not appropriateSchaferhoff et al. (2010)
ScrophulariaceaeRanopisoa1
LauralesHernandiaceaeHazomalania1IlligeraABCEMichalak et al. (2010)
LauraceaeAspidostemon31Beilschmiedia, Endiandra, Potameia, CryptocaryaAA′BCDEFGChanderbali et al. (2001)
LauraceaePotameia29Beilschmiedia (might need to be included in this genus)AA′BCDEFGChanderbali et al. (2001)
MonimiaceaeDecarydendron4Tambourissa, EphippiandraAA′Renner et al. (2010)
MonimiaceaeEphippiandra7Nested within TambourissaAA′Renner et al. (2010)
MagnolialesAnnonaceaeAmbavia4Cleistopholis, Mezzettia, TetrameranthusCDEChatrou et al. (2012); Pirie and Doyle (2012)
AnnonaceaeFenerivia10Weak relationship, but sister to MaasiaESaunders et al. (2011)
MyristicaceaeBrochoneura5MauloutchiaADoyle et al. (2004); Sauquet et al. (2003)
MyristicaceaeDoyleanthus2
MyristicaceaeHaematodendron1BicuibaGSauquet et al. (2003)
MyristicaceaeMauloutchia9BrochoneuraADoyle et al. (2004); Sauquet et al. (2003)
MyristicaceaeBrochoneura + Mauloutchia CephalosphaeraC
MalpighialesAchariaceaeProckiopsis3
EuphorbiaceaeAmyrea11Agrostistachys, PseudagrostistachysBDEWurdack et al. (2005)
EuphorbiaceaeAnomostachys1
EuphorbiaceaeBenoistia3
EuphorbiaceaeBossera1
EuphorbiaceaeCladogelonium1SuregadaAA′BCDEWurdack et al. (2005)
EuphorbiaceaeClaoxylopsis3
EuphorbiaceaeConosapium2
EuphorbiaceaeParapantadenia1
EuphorbiaceaeRadcliffea1
HypericaceaeEliea1CratoxylumBEWurdack & Davis (2009)
MalpighiaceaeDigoniopterys1Rhynchophora, Madagasikaria, MicrosteiraADavis and Anderson (2010)
MalpighiaceaeMadagasikaria1Rhynchophora (might need to be merged with the former)ADavis and Anderson (2010)
MalpighiaceaeMicrosteira28Rhynchophora, MadagasikariaADavis and Anderson (2010)
MalpighiaceaeRhynchophora3MadagasikariaADavis and Anderson (2010)
MalpighiaceaeDigoniopteris + Rhynchophora + Madagasikaria + Microsteira Triaspis + CaucanthusC
PassifloraceaeArboa4MathurinaA′Thulin et al. (2012)
 PhyllanthaceaeBlotia5PetalodiscusACWurdack et al. (2004)
PhyllanthaceaeLeptonema2Hieronyma, Martretia, ApodiscusCGWurdack et al. (2004)
PicrodendraceaeStachyandra4
PicrodendraceaeVoatamalo2
PodostemaceaeEndocaulos1ThelethylaxAKoi et al. (2012)
PodostemaceaePaleodicraeia1
PodostemaceaeThelethylax2EndocaulosAKoi et al. (2012)
PodostemaceaeEndocaulos + Thelethylax Sister to an Asian and Australian cladeDE
RhizophoraceaeMacarisia4CassipoureaABCEGSchwarzbach and Ricklefs (2000)
SalicaceaeBembicia2M. Alford (unpubl. data)
SalicaceaeCalantica10M. Alford (unpubl. data)
SalicaceaeTisonia21M. Alford (unpubl. data)
TrigoniaceaeHumbertiodendron1
MalvalesBixaceaeDiegodendron1BixaGFay et al. (1998)
MalvaceaeAndringitra6Helmiopsiella, Hemiopsis, EriolaenaABEFSkema (2012)
MalvaceaeHelicteropsis1Hibiscus grandidieri, Jumelleanthus (some incongruence between the nuclear and plastid data)Koopman and Baum (2008)
MalvaceaeHelmiopsiella4EriolaenaBEFSkema (2012)
MalvaceaeHelmiopsis10Helmiopsiella, EriolaenaABEFSkema (2012)
MalvaceaeHumbertiella6Kosteletzkya, PerrierophytumAKoopman and Baum (2008)
MalvaceaeJumelleanthus1Hibiscus grandidieri, Helicteropsis (some incongruence between the nuclear and plastid data)Koopman and Baum (2008)
MalvaceaeMacrostelia3Australian Hibiscus spp.Koopman and Baum (2008)
MalvaceaeMegistostegium3Humbertiella, Kosteletzkya, PerrierophytumAKoopman and Baum (2008)
MalvaceaeParamelhania1TrochetiopsisCBayer et al. (1999)
MalvaceaePerrierophytum9Malagsy species of KosteletzkyaKoopman and Baum (2008)
MalvaceaePseudocorchorus6
SarcolaenaceaeEremolaena2
SarcolaenaceaeLeptolaena8SarcolaenaADucousso et al. (2004)
SarcolaenaceaeMediusella2
SarcolaenaceaePentachlaena3
SarcolaenaceaePerrierodendron5
SarcolaenaceaeRhodolaena7
SarcolaenaceaeSarcolaena14LeptolaenaADucousso et al. (2004)
SarcolaenaceaeSchizolaena20
SarcolaenaceaeXerochlamys8
SarcolaenaceaeXyloolaena5
Sarcolaenaceae  DipterocarpaceaeBE
SphaerosepalaceaeDialyceras3Used as outgroup taxonvan der Bank et al. (2002)
SphaerosepalaceaeRhopalocarpus17Not a good taxon samplingAlverson et al. (1998)
ThymelaeaceaeAtemnosiphon1
MyrtalesLythraceaeCapuronia1GalpiniaCGraham et al. (2005)
LythraceaeKoehneria1WoodfordiaABCEFGraham et al. (2005)
MelastomataceaeAmphorocalyx5
MelastomataceaeDionycha3
MelastomataceaeRousseauxia17
PoalesCyperaceaeTrichoschoenus1
PoaceaeCamusiella2
PoaceaeCathariostachys2DecaryochloaAClark et al. (2007)
PoaceaeChasechloa3
PoaceaeCyphochlaena2OplismenusAA′BCDEFGMorrone et al. (2012)
PoaceaeDecaryella1
PoaceaeDecaryochloa1CathariostachysClark et al. (2007)
PoaceaeHitchcockella1
PoaceaeLecomtella1
PoaceaeNeostapfiella3
PoaceaePerrierbambus2Valiha, Decaryochloa, CathariostachysAClark et al. (2007)
PoaceaePseudolasiacis3
PoaceaeSchizostachyum2CephalostachyumBCEFClark et al. (2007)
PoaceaeSirochloa1Perrierbambus, Hickelia, Valiha, Decaryochloa, CathariostachysACClark et al. (2007)
PoaceaeToliara1
PoaceaeValiha3Decaryochloa, CathariostachysAClark et al. (2007)
PoaceaeViguierella1
PoaceaeYvesia1Salariato et al. (2010)
ProtealesProteaceaeDilobeia2Beaupreopsis, CenarrhenesDSauquet et al. (2009)
ProteaceaeMalagasia1CatalepidiaDMast et al. (2008)
RanunculalesMenispermaceaeBurasaia6OrthogyniumAHoot et al. (2009); Wang et al. (2012)
MenispermaceaeOrthogynium1BurasaiaAHoot et al. (2009); Wang et al. (2012)
MenispermaceaeRhaptonema7StrychnopsisAHoot et al. (2009); Wang et al. (2012)
MenispermaceaeSpirospermum2StrychnopsisAWang et al. (2012)
MenispermaceaeStrychnopsis1RhaptonemaAHoot et al. (2009); Wang et al. (2012)
MenispermaceaeBurasaia + Orthogynium Dioscoreophyllum, Jateorhiza, Tinospora, Rhigiocarya, Kolobopetalum, Chasmanthera, Leptoterantha, Syntriandrium, OdontocaryaBCDEG
MenispermaceaeRhaptonema + Strychnopsis + Spirospermum Cyclea, Cissampelos, Perichasma, StephaniaAA′BCDEFG
RosalesRhamnaceaeBathiorhamnus7Doerpfeldia, AmpelozizyphusGRichardson et al. (2000)
SantalalesAptandraceaePhanerodiscus3Anacolosa, CathedraACEMalecot & Nickrent (2008)
BalanophoraceaeDitepalanthus1
LoranthaceaeSocratina2VanwykiaCVidal–Russell & Nickrent (2008)
SantalaceaePilgerina1Staufferia, Scleropyrum, OkoubakaABCDERogers et al. (2008)
SantalaceaeStaufferia1Scleropyrum, OkoubakaBCDERogers et al. (2008)
SapindalesAnacardiaceaeAbrahamia15Micronychia, Rhus, ProtorhusACPell (2004); Pell et al. (2008)
AnacardiaceaeFaguetia1TrichoscyphaCPell (2004); Pell et al. (2008)
AnacardiaceaeMicronychia9Micronychia, Rhus, ProtorhusACPell (2004); Pell et al. (2008)
AnacardiaceaePoupartiopsis1Weak support, but sister to South American species of AntrocaryonGMitchell et al. (2006)
BurseraceaeAmbilobea1A pantropical cladeAA′BCDEGThulin et al. (2008)
MeliaceaeAstrotrichilia16A pantropical cladeAA′BCDEGMuellner et al. (2003, 2003,2006)
MeliaceaeCalodecaryia2Humbertioturraea, TurraeaABCDEMuellner et al. (2003, 2003,2006)
MeliaceaeCapuronianthus2LovoaCMuellner et al. (2003, 2003,2006)
MeliaceaeHumbertioturraea11TurraeaABCDEMuellner et al. (2003, 2003,2006)
MeliaceaeNeobeguea3Toona, Cedrela, Swietenia, Khaya, Carapa, Lovoa, CapuronianthusACDEFMuellner et al. (2003, 2003,2006)
MeliaceaeQuivisianthe2EkebergiaACMuellner et al. (2003, 2003,2006)
RutaceaeCedrelopsis8PtaeroxylonCAppelhans et al. (2012); Razafimandimbison et al. (2010)
SapindaceaeBeguea7MacphersoniaAA′CBuerki et al. (2010, 2010,2011a)
SapindaceaeChouxia6PseudopterisABuerki et al. (2010)
SapindaceaeConchopetalum2GereauaABuerki et al. (2010, 2010,2011a)
SapindaceaeGereaua1ConchopetalumABuerki et al. (2010, 2010,2011a)
SapindaceaePlagioscyphus10PappeaCBuerki et al. (2010, 2010,2011a)
SapindaceaePseudopteris3ChouxiaABuerki et al. (2010)
SapindaceaeTina25MolinaeaAA′Buerki et al. (2011a, b)
SapindaceaeTsingya1
SapindaceaeChouxia + Pseudopteris + Gereaua + Conchopetalum Macphersonia, BegueaAA′C
SimaroubaceaePerriera2GymnostemonCAppelhans et al. (2012); Clayton et al. (2007)
SaxifragalesCrassulaceaePerrierosedum1
SolanalesConvolvulaceaeCardiochlamys2Poranopsis, CordisepalumEStefanovic et al. (2002)
ConvolvulaceaeHumbertia1Most early lineage within the familyAA′BCDEFGStefanovic et al. (2002)
ConvolvulaceaeRapona1DipteropeltisCStefanovic et al. (2002)
MontiniaceaeKaliphora1N. F. Refulio-Rodriguez & R. G. Olmstead (unpubl. data)
SolanaceaeTsoala1MetternichiaGOlmstead et al. (2008)
ZingiberalesStreliziaceaeRavenala1Phenakospermum, StreliziaCGCron et al. (2012)

Material and Methods and Preliminary Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

For this review, the list of the 310 endemic Madagascan genera was compiled based on the Catalogue of the Vascular Plants of Madagascar (Madagascar Catalogue, 2012). At the generic level, the phylogenetic position of the endemic Madagascan genera appears to be well distributed over the Angiosperm Phylogeny Group (APG) phylogenetic tree (in 28 of the 63 orders; APG III, 2009; Fig. 1B). The five orders with the highest generic diversity are Gentianales (43 genera), Lamiales (39 genera), Malpighiales (28 genera), Fabales (22 genera) and Sapindales (21 genera) (see Table 1 for more details). The endemic families Asteropeiaceae and Physenaceae and the endemic subfamily Didiereoideae (Didiereaceae) belong to Caryophyllales, whereas Sarcolaenaceae and Sphaerosepalaceae are included in Malvales (Fig. 1B). With the exception of Didiereaceae (Arakaki et al., 2011), the understanding of phylogenetic relationships in these families remains limited and further work is needed (Fig. 1B; Table 1). Phylogenetic information for 184 endemic genera was compiled by querying the GenBank database (last accessed 26 October 2012), and DNA sequences for ten additional genera that were not included in any published phylogenetic studies (Table 1) were found. In most of the studies considered, the main aim of the analysis of the Madagascan endemic genera was to support systematic work (i.e. generic and species circumscriptions and the assessment of the position and monophyly of a particular genus). Consequently, there are very few studies investigating the spatio-temporal histories of these taxa (but see, for example, Renner et al., 2010, Monimiaceae; Wikström et al., 2010, Rubiaceae; however, the latter study lacks a dating framework), and data on divergence time estimates are also scarce; we have compiled this type of data for only 67 genera.

If the taxon sampling used in a particular study to infer phylogenetic relationships was judged to be adequate (i.e. sampling covering the whole distribution of the family, reasonable phylogenetic resolution and a monophyletic genus), the distribution of the sister lineage was scored using area circumscriptions defined as follows: (A) Madagascar region (including Madagascar, the Seychelles archipelago, Mascarenes and Comoros); (B) India (including Sri Lanka); (C) mainland Africa; (D) Australia, New Guinea, New Caledonia and New Zealand; (E) South-East Asia and the Pacific islands; (F) Eurasia; (G) South America; and (H) North America. This area circumscription was used to propose a new worldwide biogeographical model (adapted from Buerki et al., 2011a; see below) to constrain ancestral area reconstructions based on palaeogeography. To assess the biogeographical affinities of the Madagascan endemic genera with the other regions, we further split area A into two subareas: (A) Madagascar and (A′) Mascarenes, Comoros and Seychelles. Data on the distribution of the genera were retrieved either from the source publication (see Table 1) or from the general literature (e.g. Schatz, 2001; Mabberley, 2008). Biogeographical affinities of the Madagascan genera with the other areas were assessed by assigning a score of 1.0 to the area in which the sister lineage was found. This value of 1.0 was divided by the number of areas in which a sister lineage was found if the latter had a widespread distribution (i.e. found in more than one area). This scoring scheme differed from that used by Yoder & Nowak (2006), which assigned a score of 1.0 to all areas. By the application of this approach, we minimized the effect of widespread taxa on the estimations of affinities between areas. In addition to scoring the distribution of the sister lineage, we also reported the name of its component(s) (Table 1). Based on this matrix, the distribution of the Madagascan sister lineages was assessed (as percentages). This biogeographical approach does not allow for the assessment of dispersal directionality, but quantifies affinities between floras/areas. The examination of the symmetry (or asymmetry) of dispersals between areas through time can only be inferred using biogeographical methods (see Buerki et al., 2011a). If available, we recorded the stem age of the endemic Madagascan genera and the age of the node subtending it. We have recorded these two ages because, without inferring the biogeographical scenario (and taking extinction into account), it remains difficult to estimate the time of dispersal of the lineage to the island. In addition, as further discussed below, many endemic Madagascan genera tend to share a common ancestor (i.e. they form clades), and therefore this approach provided a conservative estimate of the colonization of the whole lineage on the island. Finally, as a first attempt to investigate the effect of ecology on the evolutionary history of the Madagascan endemics, genera were assigned to one of three habitat types: (1) humid forest (including mountain forest); (2) dry forest; and (3) spiny bush (Moat & Smith, 2007).

A Biogeographical Model with Comments on the Establishment of Biomes

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

In this section, we focus on the assessment of the influence of abiotic factors in shaping the current Madagascan flora, based on palaeogeographical and palaeoclimatic evidence (Figs 2, 3). We also propose a worldwide stratified biogeographical model (adapted from Buerki et al., 2011a) to investigate the spatio-temporal history of the Madagascan flora. The model is subdivided into four time slices as follows: (1) Early to Late Cretaceous (145–80 Mya); (2) Late Cretaceous to early Palaeocene (80.0–61.7 Mya); (3) middle Palaeocene to late Eocene (61.7–33.9 Mya); and (4) early Oligocene (33.9 Mya) to present (Figs 2, 3). The area circumscriptions used in this model are as described above. In the model, the Madagascan satellite islands are included in area A (mainly because of their relatively recent origin), but we refer to them separately when relevant. With the exception of the granitic Seychelles (estimated to have originated c. 85 Mya; Braithwaite, 1984), the other islands originated from the late Miocene onwards (Warren et al., 2010; Fig. 2). In cases in which biogeographical reconstructions are to be inferred on taxa originating during this period (i.e. late Miocene onwards) and exhibiting high species richness in the region, the model could be modified by the addition of a fifth time slice. This would reflect the successive emergence of these islands and their implications in connecting areas, especially in the Quaternary (see Warren et al., 2010). The biogeographical model described here will prove to be useful to constrain ancestral area reconstructions according to palaeogeographical evidence, using software such as Lagrange (Ree & Smith, 2008), and will be applicable to all plants. We describe below the rationale behind the proposed time slice delimitation.

figure

Figure 2. A, Palaeogeographical history of Madagascar showing the establishment of bioclimates and biomes (see text for more details). B, The five major bioclimates (Cornet, 1974, adapted by Schatz, 2000) in Madagascar and an elevation profile.

Download figure to PowerPoint

figure

Figure 3. Stratified worldwide biogeographical model adapted from Buerki et al. (2011a). The model is subdivided into four time slices. Abbreviations of the biogeographical areas: (A) Madagascar region (including Madagascar, the Seychelles archipelago, Mascarenes and Comoros); (B) India (including Sri Lanka); (C) mainland Africa; (D) Australia, New Guinea, New Caledonia and New Zealand; (E) South-East Asia and the Pacific islands; (F) Eurasia; (G) South America; and (H) North America. The full lines refer to dispersal probabilities of unity in the model, whereas broken lines refer to probabilities of 0.5 (for more details, see Buerki et al., 2011a).

Download figure to PowerPoint

Time slice 1 (Early to Late Cretaceous, Figs 2, 3A)

During this period, Pangaea was subdivided into two distinct continents isolated by the Tethyan Seaway: Laurasia and Gondwana (see Buerki et al., 2011a and references cited therein). Movements between Laurasian and Gondwanan landmasses were practically impossible at that time, but dispersal across all areas within these landmasses was possible. South-East Asia (area E) did not come into existence until the early Palaeocene (60 Mya), and thus this area was not included in time slice 1 (for more details, see Metcalfe, 1998). During this period, Madagascar had already separated from Africa as a result of continental drift, but remained in close proximity to India (forming the Indo/Madagascan subcontinent) until the Late Cretaceous (Figs 2, 3A). At that point, the Indo/Madagascan subcontinent broke apart and India started to drift north-eastwards towards the Eurasian plate, but dispersals between these two areas might have remained possible via the Seychelles archipelago (Braithwaite, 1984; Fig. 3). During its northern migration, the position of India greatly influenced the rainfall regime on Madagascar by blocking the moisture coming from the east in the Proto-Indian Ocean (Yoder & Nowak, 2006). There is also a growing body of evidence suggesting possible dispersals between Madagascar and South America via Antarctica until about 80 Mya, despite the fact that these regions were not in direct contact (see Fig. 2; Yoder & Nowak, 2006). Based on this evidence, it is now widely accepted that vicariance-mediated speciation was the main biogeographical process that shaped the Madagascan flora prior to 80 Mya, whereas dispersal-mediated speciation became predominant from this point onwards (Fig. 2).

Time slice 2 (Late Cretaceous to early Palaeocene, Figs 2, 3B)

Gondwanan landmasses, despite ongoing fragmentation during this period, remained in contact until the early Palaeocene, with the exception of South America and Africa as a result of the expansion of the South Atlantic Ocean (Buerki et al., 2011a; Fig. 3B). In the case of Madagascar, India, Africa and Australia, this connection was mediated by the Kerguelen Plateau (and Antarctica), acting as a land bridge between these areas until the end of the Cretaceous (see Sanmartin & Ronquist, 2004 and references cited therein). Likewise, South America, Australia, New Zealand and New Caledonia remained connected with Antarctica until the Late Cretaceous (65–60 Mya), when New Zealand and New Caledonia drifted away from West Antarctica, breaking land connections with Australia and South America (Sanmartin & Ronquist, 2004). Finally, proto-South-East Asia (the south-east part of the Malaysian peninsula and south-west Borneo) was in place in the Late Cretaceous–early Palaeocene (see Fig. 2 in Metcalfe, 1998), such that dispersal between Eurasia and this part of South-East Asia was possible (Fig. 3B; see Buerki et al., 2011a).

Time slice 3 (middle Palaeocene to late Eocene; Figs 2, 3C)

During the Palaeocene, India mediated dispersals between proto-South-East Asia, Madagascar and Africa, whilst drifting rapidly northwards, heading for an imminent collision with Eurasia. Several studies have discussed the similarities between the Madagascan and Indian floras by invoking a direct pathway of dispersal via islands in the Indian Ocean (e.g. Schatz, 1995); the continental dispersal route via Arabia–Socotra (Africa) was largely neglected, but it is now modelled here. This route was inferred by Yuan et al. (2005) to explain the current distribution of Exacum L. (Gentianaceae). Also during this period, Africa and Madagascar started a northward migration towards the equator (which created a path of dispersal between Gondwanan and Laurasian landmasses), leaving the subtropical and arid belt at 30° latitude (Wells, 2003; Fig. 2). This northward migration greatly influenced the vegetation on Madagascar, causing a shift from a dry/arid to a more humid environment (Wells, 2003; Fig. 2). Before it drifted north, Madagascar had a much drier climate because of its geographical position and the limited amount of moisture reaching the island from the Proto-Indian Ocean (Fig. 2; Yoder & Nowak, 2006 and references cited therein). According to Wells (2003), the conjunction of these abiotic factors resulted in the emergence of arid forests all over Madagascar that were similar in nature to the extant spiny bush vegetation (referred to as the subarid bioclimate by Cornet, 1974) currently confined to the southern part of the island (Fig. 2). The dramatic shift in rainfall regime that took place during the Eocene and onwards led to the gradual replacement of the arid forests by three main bioclimate types from the humid biome (Fig. 2; Wells, 2003). These three ecotypes are the product of the orographic processes that led to the current Madagascan topography, which includes a steep eastward-facing slope on the eastern coast (ranging from sea level to c. 1500 m) and a more gentle slope that gradually descends to sea level on the western coast (Fig. 2B; Cornet, 1974).

Time slice 4 (early Oligocene to present; Figs 2, 3D)

During this phase, climatic conditions on Earth shifted and there was a change from a relatively ice-free world to one with glacial conditions in polar regions, characterized by the presence of substantial ice sheets (Bowen, 2007). This glaciation resulted in a drastic drop in sea level (leading to the emergence of islands between Madagascar and India that could have acted as stepping stones for dispersal; Warren et al., 2010), induced drought in southern regions (especially in Africa and Australia; Bowen, 2007) and a subsequent reduction in the width of the tropical belt (see Morley, 2003). In the same time span, the collision of the Australian and Eurasian plates resulted in intensive volcanic activity (Buerki et al., 2011a and references cited therein) and created most of the islands in South-East Asia (e.g. Sumatra, part of Borneo, Celebes, the Inner Banda Arc). These climatic and geological events (especially the emergence of South-East Asia) opened up new pathways of dispersal, allowing plants to colonize various parts of the world, including Madagascar. After the Miocene climatic optimum (Zachos et al., 2001), a second drought period was recorded, persisting until the Pleistocene, and this correlated with the establishment of several deserts, C4 grasslands and the radiation of major succulent lineages (see Micheels, Eronen & Mosbrugger, 2009; Arakaki et al., 2011 and references cited therein).

This period also coincided with the establishment of the Mediterranean climate in the Cape region (South Africa; Buerki et al., 2012b and references cited therein), which replaced a continuous subtropical humid forest shared between this region, Madagascar, Antarctica and South America (Coetzee & Muller, 1984). For instance, Nilsson, Coetzee & Grafstrom (1996) described fossil pollen grains from this region assigned to an extinct species of Sarcolaenaceae that is morphologically similar to extant species of the family currently viewed as endemic to Madagascar. This pattern suggests a wider distribution for this family before the middle Miocene, followed by extinctions driven by climate change in the region. This example is unlikely to be unique (for a discussion of New Caledonia, see, for example, Pillon, 2012) and, consequently, further palaeobotanical studies (with particular focus on the eastern coast of Africa) are critically needed to understand the biogeographical history of the Madagascan flora. Parametric biogeographical methods would need to be amended to take into account the distribution of fossil taxa. This need is well exemplified in the case of Sarcolaenaceae, where current biogeographical methods would infer Madagascar as the cradle of this family, which would be clearly ruled out if the fossil record were to be taken into account. Finally, the use of such new methods, together with the biogeographical model presented here, would allow the inference of more accurate and realistic dispersal routes.

Sometime during the Miocene onwards, the establishment of the equatorial and west wind drift currents allowed a certain level of reconnection between previously isolated Gondwanan areas via long-distance dispersal (Fig. 3D; Buerki et al., 2011a). During the late Miocene (c. 8 Mya), an onset of heavy seasonal rains was initiated, especially in the north-western Sambirano region in Madagascar, as a result of the establishment of the Indian monsoons (Fig. 2; Yoder & Nowak, 2006). This onset of heavy rain was advocated to be the cause of the expansion of the humid forest in the Sambirano region (Yoder & Nowak, 2006). Finally, the Comoros and Mascarene islands originated during the late Miocene and might have facilitated dispersals between Madagascar and Africa (via the Comoros) and Madagascar and India (Mascarenes and Seychelles) (Warren et al., 2010; Fig. 2).

Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

Biogeographical affinities of the endemic Madagascan genera

The biogeographical patterns and divergence time estimates retrieved here are displayed in Figures 4 and 5. A lack of information on the biogeography and palaeobotany of each group has prevented what was initially intended, namely the combination of these data to infer the main routes of dispersal through time, based on palaeogeography. Consequently, we only discuss biogeographical affinities between areas and investigate the impact of past climate change on the origin of Madagascan endemic genera.

figure

Figure 4. Biogeographical affinities of the Madagascan endemic genera (in percentages). See text for details related to the compilation of the data used here and in Table 1. The pie chart in the inset refers to the occurrence of sister lineages in the Mascarenes (M), Comoros (C) and the Seychelles (S) based on sister lineages occurring in a maximum of three areas (see text). The biogeographical affinities of some widespread genera (15% of cases) remain unclear.

Download figure to PowerPoint

figure

Figure 5. Plot of the tempo of origin of the 67 endemic Madagascan genera for which divergence time estimates are available. For each genus, the ages of its stem and the node subtending it are displayed as intervals (see text for more details). The estimations of climatic oscillations through time are displayed based on the variation of 18O concentration (Zachos et al., 2001) and major abiotic events (see text for more details). Data for Fabaceae are based on unpublished data from a study of phylogenetic diversity patterns in the family in Madagascar (S. Buerki et al., unpubl. data). For Rubiaceae, the only age estimates available were at the tribal level; these values overestimate the actual age of the genera (see Table 1). The distribution of the genera in the main vegetation types is also provided.

Download figure to PowerPoint

As demonstrated previously (e.g. Yoder & Nowak, 2006), the Madagascan endemic genera share extensive biogeographical affinities with African taxa (22.4%; Fig. 4). This affinity could easily be explained by the close geographical proximity of these areas through time, and agrees with past (Leroy, 1978) and current (Gautier et al., 2012) floristic views. This floristic similarity was even higher before the establishment of the Mediterranean climate in the Cape region (during the middle Miocene; Coetzee & Muller, 1984), as demonstrated by the discovery of fossils of Sarcolaenaceae in this region. The strong connections between the Madagascan, South-East Asian (9.1%; see Schatz, 1995) and Indian (6.2%; Warren et al., 2010) biota are also confirmed by our data (Fig. 4). In this context, India could have acted as a land bridge, but further dated inferences are required to assess this hypothesis. In addition, further data will also be crucial to investigate the importance of the African continental route of dispersal connecting Madagascar with India and, to some extent, South-East Asia via Arabia and Socotra (see above; Figs 3, 4). Finally, in the Madagascar region, the Mascarenes exhibit the highest biogeographical affinity with Madagascar (58.3%), followed by the Comoros (37.5%) and Seychelles (4.1%) (Fig. 4). These figures were compiled by considering sister lineages restricted to a maximum of three areas (most of the time, these areas were Africa, Madagascar and one of these islands). It should be noted, however, that the relationship between the Madagascan, Mascarene and Comoros floras is most certainly underestimated by this analysis, as it is limited to genera endemic to Madagascar. Indeed, these satellite islands share a lot of diversity with Madagascar, such as Didymeles Thouars (Buxaceae; Schatz, 2001) and Oncostemum A.Juss. (Primulaceae; Bone et al., 2012) with the Comoros, Molinaea Comm. ex Juss. (Sapindaceae; Buerki et al., 2011b) with the Mascarenes and Martellidendron (Pic. Serm.) Callm. & Chassot (Pandanaceae; Callmander et al., 2003; Buerki et al., 2012a) with the granitic Seychelles. In addition, to further demonstrate the affinities between these floras, Wikström et al. (2010) inferred the origin of almost all the taxa of Rubiaceae found in these satellite islands to be Madagascar. Further studies focusing on the biogeography and tempo of diversification of the Madagascan flora will need to consider these additional genera [for an example on Psiadia Jacq. (Asteraceae), see Strijk et al., 2012], but, for the moment, the information required to undertake such a task is not available.

Tempo of origin of the Madagascan endemic genera

With the exception of Hazomalania Capuron (Hernandiaceae) and Dilobeia Thouars (Proteaceae), which originated during the Cretaceous, the current data suggest that the endemic Madagascan genera originated from the middle Eocene/Oligocene onwards, with most of the genera appearing in the Miocene (Fig. 5). These results confirm the current trend in ruling out the importance of the Gondwanan break-up on shaping the current Madagascan flora (as proposed by Leroy, 1978). One of the only genera that might have been sufficiently old (> 80 Mya; Fig. 2) to have been influenced by vicariance speciation triggered by the break-up of Gondwana is Takhtajania Baranova & J.-F. Leroy (Winteraceae; c. 120 Mya; Marquinez et al., 2009; Table 1). In this context, this element of the flora (i.e. the endemic genera) was mainly shaped by dispersal events and relatively recent climate change. However, we would like to draw attention to the importance of putative extinction events in the assemblage of the current species distributions and the subsequent interpretations that arise from them. Extinction events could lead to the loss of the signature of vicariance, thus favouring dispersal as an explanation for current distributions and, consequently, increase the assignment of endemism (e.g. the case of Sarcolaenaceae; see above). Further studies inferring spatio-temporal histories of the endemic Madagascan lineages, based on the fossil record, to calibrate molecular phylogenetic trees and provide evidence of past distributions are crucial to provide more accurate estimates for the dispersal routes (Figs 2-5).

Strong phylogenetic clustering of the Madagascan endemic genera

One of the particular features of the Madagascan endemic genera is their high level of phylogenetic clustering in families (i.e. genera generally form monophyletic clades confined to the island), low species richness per genus and frequent occurrence of narrow endemics (Madagascar Catalogue, 2012; Table 1; Fig. 1A). The data compiled here show that 26% of the endemic genera have sister lineages that are also restricted to the island (Fig. 4). Based on this evidence, these taxa can be: (1) simply an artefact of taxonomic over-splitting; (2) relicts of extinct lineages resulting, for instance, from abrupt mass extinctions induced by climate change on Madagascar and elsewhere, and therefore creating the observed genetic and morphological discontinuities; or (3) the result of recent ‘rapid’ radiations potentially caused by, for example, co-evolutionary processes and/or abrupt climate change that cleared or created new niches for colonization. In the latter case, the observed pattern resulted from a rapid geographical or phenological barrier and speciation is ongoing. To address these lines of investigation fully, we need robustly dated phylogenetic trees based on almost complete taxon sampling (at least at the generic level) and knowledge of the fossil record. Below, we assess the importance of each of these factors in explaining the current distribution and diversity of the endemic genera.

Recently, phylogenetic inferences have suggested cases of taxonomic over-splitting in the Madagascan flora, particularly in Acanthaceae, in which several endemic genera have been shown to be nested in more widespread genera (e.g. Conocalyx Benoist, clustered in the Afro-Madagascan genus Isoglossa Oerst.; Kiel et al., 2006). However, there are also cases in which phylogenetic studies have supported the description of Madagascan endemic genera segregated from more widely distributed genera (e.g. Andringitra Skema segregated from Dombeya Lam., Malvaceae; Skema, 2012). Consequently, taxonomic over-splitting is not a satisfactory explanation to account for the pattern observed in Madagascan endemic genera, and so, although it may have an effect, it must be ruled out as a general explanation.

We have already shown the role played by extinction during the middle Miocene in explaining the apparent endemism of Sarcolaenaceae (see above). This is one of many potentially similar pieces of evidence supporting the option that this process could have been one of the main driving forces involved in shaping current Madagascan diversity. Additional fossil data are necessary to fully assess this situation. The African and Madagascan family Didiereaceae potentially provides another example in which extinction events could have led to the current diversity. The family is estimated to have originated sometime during the Eocene, but the 11 species assigned to four genera forming the Madagascan clade only diversified during the middle Miocene (Arakaki et al., 2011; Fig. 5). This long temporal interval between the stem and crown ages for this group is putatively indicative of extinction events in Madagascar (and, to some extent, in Africa, see Fig. 3) caused by the contraction of the subarid biome from the Eocene onwards as a result of the northward drift of Madagascar (Figs 2, 5). The time of origin of the Madagascan Didiereaceae coincides with the same aridification events that led to the establishment of deserts, C4 grasslands, the radiation of succulent plant lineages and the establishment of the Mediterranean climate in the Cape region (see Micheels et al., 2009; Arakaki et al., 2011; Buerki et al., 2012b and references cited therein; Fig. 5). Although this biome was under contraction, this period of aridification could have mimicked the former climatic conditions of the end of the Cretaceous and triggered the emergence of these taxa. Finally, this period is also synchronous with the origin of other major elements of the spiny bush flora of southern Madagascar, such as the Fabaceae, Malvaceae and Meliaceae (Fig. 5). In this case, the subarid biome could have served as a second geographical centre of diversification for these plants, as they were better adapted to dry ecosystems.

Finally, preliminary results of DNA-based divergence time estimates showed that most of the examined genera originated recently (Fig. 5). Most of these genera have few species, with the exception of Tina Schult. (Sapindaceae) which contains c. 25 species (Table 1). This genus originated and diversified in the last ten million years (Buerki et al., 2011a, b), most probably in response to the onset of heavy seasonal rains as a result of the establishment of the Indian monsoons (Figs 1, 5), and has successfully colonized the humid forests (from the eastern coast to the highlands, with a high species richness in the Sambirano region) and also diversified into the drier areas of the island. Further investigations are required to confirm this hypothesis and test it over a set of taxa widely represented in the Sambirano region. The implications of the last glaciation on the Madagascan flora also deserve to be investigated, especially with regard to the preliminary results suggesting the origin of several endemic lineages during this period (Fig. 5).

Conclusion and Perspectives

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

Although we have been able to gather data for 184 endemic genera, there is still a long way to go to sample all the genera endemic to the Madagascan flora and to obtain extensive spatial and temporal information. The network of DNA and tissue banks (particularly those housed at the Royal Botanic Gardens, Kew, and Missouri Botanical Garden, which have important Madagascar programmes) could support the completion of this task, but extensive fieldwork in target areas will also need to be conducted. Such a task will also require sampling in areas with the strongest biogeographical links with Madagascar (particularly Africa, India and South-East Asia, as shown here) to obtain robust phylogenetic frameworks and reliable timescales at the species level for as many groups as possible. These dated phylogenetic trees will subsequently be employed to perform biogeographical analyses using the model presented here. This work will be instrumental in allowing the evaluation of the hypotheses presented in this review, especially the effect of climate change on the diversification of the Madagascan flora as a whole.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References

We are grateful to two anonymous reviewers and the editor (Mike Fay) for their valuable comments that greatly contributed to the improvement of the manuscript. Financial support to SB was provided by the Marie-Curie Intra-European Fellowship (CRADLE; no. 253866). Financial support to MWC and PBP was provided by grants from the US National Science Foundation (0743355) and the Andrew W. Mellon Foundation.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods and Preliminary Results
  5. A Biogeographical Model with Comments on the Establishment of Biomes
  6. Biogeography and Temporal Framework of the Endemic Madagascan Generic Flora
  7. Conclusion and Perspectives
  8. Acknowledgements
  9. References
  • Alverson WS, Karol KG, Baum DA, Chase MW, Swensen SM, McCourt R, Sytsma KJ. 1998. Circumscription of the Malvales and relationships to other Rosidae: evidence from rbcL sequence data. American Journal of Botany 85: 876887.
  • Anderberg AA, Swenson U. 2003. Evolutionary lineages in Sapotaceae (Ericales): a cladistic analysis based on ndhF sequence data. International Journal of Plant Sciences 164: 763773.
  • APG III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105121.
  • Appelhans MS, Kessler PJA, Smets E, Razafimandimbison SG, Janssens SB. 2012. Age and historical biogeography of the pantropically distributed Spathelioideae (Rutaceae, Sapindales). Journal of Biogeography 39: 12351250.
  • Applequist WL, Wallace RS. 2001. Phylogeny of the portulacaceous cohort based on ndhF sequence data. Systematic Botany 26: 406419.
  • Arakaki M, Christin PA, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences of the United States of America 108: 83798384.
  • Baker WJ, Couvreur TLP. in press. Global biogeography and diversification of palms sheds light on the evolution of tropical lineages. Part 1: historical biogeography. Journal of Biogeography. doi: 10.1111/j.1365-2699.2012.02795.x
  • Baker WJ, Savolainen V, Asmussen-Lange CB, Chase MW, Dransfield J, Forest F, Harley MM, Uhl NW, Wilkinson M. 2009. Complete generic-level phylogenetic analyses of palms (Arecaceae) with comparisons of supertree and supermatrix approaches. Systematic Biology 58: 240256.
  • van der Bank M, Fay MF, Chase MW. 2002. Molecular phylogenetics of Thymelaeaceae with particular reference to African and Australian genera. Taxon 51: 329339.
  • Bayer C, Fay MF, De Bruijn PY, Savolainen V, Morton CM, Kubitzki K, Alverson WS, Chase MW. 1999. Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: a combined analysis of plastid atpB and rbcL DNA sequences. Botanical Journal of the Linnean Society 129: 267303.
  • van den Berg C, Ryan A, Cribb PJ, Chase MW. 2002. Molecular phylogenetics of Cymbidium (Orchidaceae: Maxillarieae) sequence data from internal transcribed spacers (ITS) of nuclear ribosomal DNA and plastid matK. Lindleyana 17: 102111.
  • Bone RE, Strijk JS, Fritsch PW, Buerki S, Strasberg D, Thebaud C, Hodkinson TR. 2012. Phylogenetic inference of Badula (Primulaceae), a rare and threatened genus endemic to the Mascarene Archipelago. Botanical Journal of the Linnean Society 169: 284296.
  • Bowen GJ. 2007. Palaeoclimate – when the world turned cold. Nature 445: 607608.
  • Braithwaite CJR. 1984. Geology of the Seychelles. In: Stoddart DR , ed. Biogeography and ecology of the Seychelles Islands. The Hague: Junk, 1738.
  • Bremer B, Eriksson T. 2009. Time tree of the Rubiaceae: phylogeny and dating the family, subfamilies, and tribes. International Journal of Plant Sciences 170: 766793.
  • Brockington SF, Alexandre R, Ramdial J, Moore MJ, Crawley S, Dhingra A, Hilu K, Soltis DE, Soltis PS. 2009. Phylogeny of the Caryophyllales sensu lato: revisiting hypotheses on pollination biology and perianth differentiation in the core Caryophyllales. International Journal of Plant Sciences 170: 627643.
  • Bruneau A, Forest F, Herendeen PS, Klitgaard BB, Lewis GP. 2001. Phylogenetic relationships in the Caesalpinioideae (Leguminosae) as inferred from chloroplast trnL intron sequences. Systematic Botany 26: 487514.
  • Bruneau A, Mercure M, Lewis GP, Herendeen PS. 2008. Phylogenetic patterns and diversification in the caesalpinioid legumes. Botany-Botanique 86: 697718.
  • Buerki S, Callmander MW, Devey DS, Chappell L, Gallaher T, Munzinger J, Haevermans T, Forest F. 2012a. Straightening out the screw-pines: a first step in understanding phylogenetic relationships within Pandanaceae. Taxon 61: 10101020.
  • Buerki S, Forest F, Alvarez N, Nylander JAA, Arrigo N, Sanmartin I. 2011a. An evaluation of new parsimony-based versus parametric inference methods in biogeography: a case study using the globally distributed plant family Sapindaceae. Journal of Biogeography 38: 531550.
  • Buerki S, Jose S, Yadav SR, Goldblatt P, Manning JC, Forest F. 2012b. Contrasting biogeographic and diversification patterns in two Mediterranean-type ecosystems. PloS ONE 7: e39377.
  • Buerki S, Lowry PP, Andriambololonera S, Phillipson PB, Vary L, Callmander MW. 2011b. How to kill two genera with one tree: clarifying generic circumscriptions in an endemic Madagascan clade of Sapindaceae. Botanical Journal of the Linnean Society 165: 223234.
  • Buerki S, Lowry PP, Phillipson PB, Callmander MW. 2010. Molecular phylogenetic and morphological evidence supports recognition of Gereaua, a new endemic genus of Sapindaceae from Madagascar. Systematic Botany 35: 172180.
  • Cabrera LI, Salazar GA, Chase MW, Mayo SJ, Bogner J, Davila P. 2008. Phylogenetic relationships of aroids and duckweeds (Araceae) inferred from coding and noncoding plastid DNA. American Journal of Botany 95: 11531165.
  • Callmander MW, Chassot P, Küpfer P, Lowry PP. 2003. Recognition of Martellidendron, a new genus of Pandanaceae, and its biogeographic implications. Taxon 52: 747762.
  • Callmander MW, Phillipson PB, Schatz GE, Andriambololonera S, Rabarimanarivo M, Rakotonirina N, Raharimampionona J, Chatelain C, Gautier L, Lowry PP. 2011. The endemic and non-endemic vascular flora of Madagascar updated. Plant Ecology and Evolution 144: 121125.
  • Carlsward BS, Whitten WM, Williams NH, Bytebier B. 2006. Molecular phylogenetics of Vandeae (Orchidaceae) and the evolution of leaflessness. American Journal of Botany 93: 770786.
  • Chanderbali AS, van der Werff H, Renner SS. 2001. Phylogeny and historical biogeography of Lauraceae: evidence from the chloroplast and nuclear genomes. Annals of the Missouri Botanical Garden 88: 104134.
  • Chatrou LW, Pirie MD, Erkens RHJ, Couvreur TLP, Neubig KM, Abbott JR, Mols JB, Maas JW, Saunders RMK, Chase MW. 2012. A new subfamilial and tribal classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. Botanical Journal of the Linnean Society 169: 540.
  • Clark LG, Dransfield S, Triplett J, Sanchez-Ken JG. 2007. Phylogenetic relationships among the one-flowered, determinate genera of Bambuseae (Poaceae: Bambusoideae). Aliso 23: 315332.
  • Clayton JW, Fernando ES, Soltis PS, Soltis DE. 2007. Molecular phylogeny of the tree-of-heaven family (Simaroubaceae) based on chloroplast and nuclear markers. International Journal of Plant Sciences 168: 13251339.
  • Coetzee JA, Muller J. 1984. The phytogeographic significance of some extinct Gondwana pollen types from the Tertiary of the southwestern Cape (South Africa). Annals of the Missouri Botanical Garden 71: 10881099.
  • Cornet A. 1974. Essai de cartographie bioclimatique à Madagascar. Notice explicative. Paris: ORSTOM, 155.
  • Cron GV, Pirone C, Bartlett M, Kress WJ, Specht C. 2012. Phylogenetic relationships and evolution in the Strelitziaceae (Zingiberales). Systematic Botany 37: 606619.
  • Cuenoud P, Savolainen V, Chatrou LW, Powell M, Grayer RJ, Chase MW. 2002. Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. American Journal of Botany 89: 132144.
  • Davis AP, Chester M, Maurin O, Fay MF. 2007. Searching for the relatives of Coffea (Rubiaceae, Ixoroideae): the circumscription and phylogeny of Coffeeae based on plastid sequence data and morphology. American Journal of Botany 94: 313329.
  • Davis CC, Anderson WR. 2010. A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. American Journal of Botany 97: 20312048.
  • Doyle JA, Sauquet H, Scharaschkin T, Le Thomas A. 2004. Phylogeny, molecular and fossil dating, and biogeographic history of Annonaceae and Myristicaceae (Magnoliales). International Journal of Plant Sciences 165: S55S67.
  • Dransfield J, Rakotoarinivo M, Baker WJ, Bayton RP, Fisher JB, Horn JW, Leroy B, Metz X. 2008. A new coryphoid palm genus from Madagascar. Botanical Journal of the Linnean Society 156: 7991.
  • Ducousso M, Bena G, Bourgeois C, Buyck B, Eyssartier G, Vincelette M, Rabevohitra R, Randrihasipara L, Dreyfus B, Prin Y. 2004. The last common ancestor of Sarcolaenaceae and Asian dipterocarp trees was ectomycorrhizal before the India–Madagascar separation, about 88 million years ago. Molecular Ecology 13: 231236.
  • Edwards D, Hawkins JA. 2007. Are Cape floral clades the same age? Contemporaneous origins of two lineages in the genistoids s.l. (Fabaceae). Molecular Phylogenetics and Evolution 45: 952970.
  • Evans TM, Sytsma KJ, Faden RB, Givnish TJ. 2003. Phylogenetic relationships in the Commelinaceae: II. A cladistic analysis of rbcL sequences and morphology. Systematic Botany 28: 270292.
  • Fay MF, Bayer C, Alverson WS, de Bruijn AY, Chase MW. 1998. Plastid rbcL sequence data indicate a close affinity between Diegodendron and Bixa. Taxon 47: 4350.
  • Fougere-Danezan M, Maumont S, Bruneau A. 2007. Relationships among resin-producing Detarieae s.l. (Leguminosae) as inferred by molecular data. Systematic Botany 32: 748761.
  • Gautier L, Chatelain C, Callmander MW, Phillipson PB. 2012. Richness, similarity and specificity of Madagascar flora compared with sub-Saharan Africa. Plant Ecology and Evolution 145: 5564.
  • Goodman SM, Benstead JP. 2005. Updated estimates of biotic diversity and endemism for Madagascar. Oryx 39: 7377.
  • Gorniak M, Paun O, Chase MW. 2010. Phylogenetic relationships within Orchidaceae based on a low-copy nuclear coding gene, Xdh: congruence with organellar and nuclear ribosomal DNA results. Molecular Phylogenetics and Evolution 56: 784795.
  • Graham SA, Hall J, Sytsma K, Shi SH. 2005. Phylogenetic analysis of the Lythraceae based on four gene regions and morphology. International Journal of Plant Sciences 166: 9951017.
  • Groeninckx I, De Block P, Rakotonasolo F, Smets E, Dessein S. 2009b. Rediscovery of Madagascan Lathraeocarpa allows determination of its taxonomic position within Rubiaceae. Taxon 58: 209226.
  • Groeninckx I, De Block P, Robbrecht E, Smets EE, Dessein S. 2010a. Amphistemon and Thamnoldenlandia, two new genera of Rubiaceae (Spermacoceae) endemic to Madagascar. Botanical Journal of the Linnean Society 163: 447472.
  • Groeninckx I, Briggs M, Davis A, De Block P, Robbrecht E, Smets E, Dessein S. 2010b. A new herbaceous genus endemic to Madagascar: Phialiphora (Spermacoceae, Rubiaceae). Taxon 59: 18151829.
  • Groeninckx I, Dessein S, Ochoterena H, Person C, Motley TJ, Karehed J, Bremer B, Huysmans S, Smets E. 2009a. Phylogeny of the herbaceous tribe Spermacoceae (Rubiaceae) based on plastid DNA data. Annals of the Missouri Botanical Garden 96: 109132.
  • Hoot SB, Zautke H, Harris DJ, Crane PR, Neves SS. 2009. Phylogenetic patterns in Menispermaceae based on multiple chloroplast sequence data. Systematic Botany 34: 4456.
  • Hu JM, Lavin M, Wojciechowski MF, Sanderson MJ. 2002. Phylogenetic analysis of nuclear ribosomal ITS/5.8S sequences in the tribe Millettieae (Fabaceae): Poecilanthe–Cyclolobium, the core Millettieae, and the Callerya group. Systematic Botany 27: 722733.
  • Hughes CE, Bailey CD, Krosnick S, Luckow MA. 2003. Relationships among genera of the informal Dichrostachys and Leucaena groups (Mimosoideae) inferred from nuclear ribosomal ITS sequences. In: Klitgaard B , Bruneau A , eds. Advances in legume systematics, Part 10. Higher level systematics. Kew: Kew Publishing, 221238.
  • Ionta GM, Judd WS. 2007. Phylogenetic relationships in Periplocoideae (Apocynaceae s.l.) and insights into the origin of pollinia. Annals of the Missouri Botanical Garden 94: 360375.
  • Jobson RW, Albert VA. 2002. Molecular rates parallel diversification contrasts between carnivorous plant sister lineages. Cladistics 18: 127136.
  • Kainulainen K, Mouly A, Khodabandeh A, Bremer B. 2009. Molecular phylogenetic analysis of the tribe Alberteae (Rubiaceae), with description of a new genus, Razafimandimbisonia. Taxon 58: 757768.
  • Karaman-Castro V, Urbatsch LE. 2009. Phylogeny of Hinterhubera group and related genera (Hinterhuberinae: Astereae) based on the nrDNA ITS and ETS sequences. Systematic Botany 34: 805817.
  • Keeley SC, Forsman ZH, Chan R. 2007. A phylogeny of the ‘evil tribe’ (Vernonieae: Compositae) reveals Old/New World long distance dispersal: support from separate and combined congruent datasets (trnL-F, ndhF, ITS). Molecular Phylogenetics and Evolution 44: 89103.
  • Kiel CA, McDade LA, Daniel TF, Champluvier D. 2006. Phylogenetic delimitation of Isoglossinae (Acanthaceae: Justicieae) and relationships among constituent genera. Taxon 55: 683694.
  • Kissling J. 2007. Phylogenetics of tribe Exaceae (Gentianaceae) based on molecular, morphological and karyological data, with special emphasis on the genus Sebaea. DPhil Thesis, University of Neuchatel.
  • Kissling J, Yuan YM, Kupfer P, Mansion G. 2009. The polyphyletic genus Sebaea (Gentianaceae): a step forward in understanding the morphological and karyological evolution of the Exaceae. Molecular Phylogenetics and Evolution 53: 734748.
  • Kocyan A, Zhang LB, Schaefer H, Renner SS. 2007. A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Molecular Phylogenetics and Evolution 44: 553577.
  • Koi S, Kita Y, Hirayama Y, Rutishauser R, Huber KA, Kato M. 2012. Molecular phylogenetic analysis of Podostemaceae: implications for taxonomy of major groups. Botanical Journal of the Linnean Society 169: 461492.
  • Koopman MM, Baum DA. 2008. Phylogeny and biogeography of tribe Hibisceae (Malvaceae) on Madagascar. Systematic Botany 33: 364374.
  • Kruger A, Razafimandimbison SG, Bremer B. 2012. Molecular phylogeny of the tribe Danaideae (Rubiaceae: Rubioideae): another example of out-of-Madagascar dispersal. Taxon 61: 629636.
  • Lahaye R, Civeyrel L, Speck T, Rowe NP. 2005. Evolution of shrub-like growth forms in the lianoid subfamily Secamonoideae (Apocynaceae s.l.) of Madagascar: phylogeny, biomechanics, and development. American Journal of Botany 92: 13811396.
  • Lavin M, Pennington RT, Klitgaard BB, Sprent JI, de Lima HC, Gasson PE. 2001. The dalbergioid legumes (Fabaceae): delimitation of a pantropical monophyletic clade. American Journal of Botany 88: 503533.
  • Leroy JF. 1978. Composition, origin, and affinities of the Madagascan vascular flora. Annals of the Missouri Botanical Garden 65: 535589.
  • Livshultz T, Middleton DJ, Endress ME, Williams JK. 2007. Phylogeny of Apocynoideae and the APSA clade (Apocynaceae s.l.). Annals of the Missouri Botanical Garden 94: 324359.
  • Mabberley DJ. 2008. Mabberley's plant-book a portable dictionary of plants, their classifications, and uses. Seattle, WA: University of Washington Botanic Gardens.
  • Madagascar Catalogue. 2012. Catalogue of the Vascular Plants of Madagascar. St Louis, MO: Missouri Botanical Garden; Antananarivo, Madagascar: Missouri Botanical Garden, Madagascar Research and Conservation Program. Available at: http://www.efloras.org/madagascar. [Accessed August 2012].
  • Magee AR, van Wyk BE, Tilney PM, Sales F, Hedge I, Downie SR. 2009. Billburttia, a new genus of Apiaceae (tribe Apieae) endemic to Madagascar. Plant Systematics and Evolution 283: 237245.
  • Malecot V, Nickrent DL. 2008. Molecular phylogenetic relationships of Olacaceae and related Santalales. Systematic Botany 33: 97106.
  • Manns U, Bremer B. 2010. Towards a better understanding of intertribal relationships and stable tribal delimitations within Cinchonoideae s.s. (Rubiaceae). Molecular Phylogenetics and Evolution 56: 2139.
  • Marquinez X, Lohmann LG, Salatino MLF, Salatino A, Gonzalez F. 2009. Generic relationships and dating of lineages in Winteraceae based on nuclear (ITS) and plastid (rps16 and psbA-trnH) sequence data. Molecular Phylogenetics and Evolution 53: 435449.
  • Mast AR, Willis CL, Jones EH, Downs KM, Weston PH. 2008. A smaller Macadamia from a more vagile tribe: inference of phylogenetic relationships, divergence times, and diaspore evolution in Macadamia and relatives (tribe Macadamieae; Proteaceae). American Journal of Botany 95: 843870.
  • McDade LA, Daniel TF, Kiel CA. 2008. Toward a comprehensive understanding of phylogenetic relationships among lineages of Acanthaceae s.l. (Lamiales). American Journal of Botany 95: 11361152.
  • Metcalfe I. 1998. Paleozoic and Mesozoic geological evolution of the SE Asia region: multidisciplinary constraints and implications for biogeography. In: Halle R , Holloway JD , eds. Biogeography and geological evolution of SE Asia. Leiden: Backhuys Publisher, 2541.
  • Michalak I, Zhang LB, Renner SS. 2010. Trans-Atlantic, trans-Pacific and trans-Indian Ocean dispersal in the small Gondwanan Laurales family Hernandiaceae. Journal of Biogeography 37: 12141226.
  • Micheels A, Eronen J, Mosbrugger V. 2009. The Late Miocene climate response to a modern Sahara desert. Global and Planetary Change 67: 193204.
  • Mitchell JD, Daly DC, Pell SK, Randrianasolo A. 2006. Poupartiopsis gen. nov and its context in Anacardiaceae classification. Systematic Botany 31: 337348.
  • Moat J, Smith P. 2007. Atlas of the vegetation of Madagascar. Kew: Kew Publishing.
  • Morley RJ. 2003. Interplate dispersal paths for megathermal angiosperms. Perspectives in Plant Ecology, Evolution and Systematics 6: 520.
  • Morrone O, Aagesen L, Scataglini MA, Salariato DL, Denham SS, Chemisquy MA, Sede SM, Giussani LM, Kellogg EA, Zuloaga FO. 2012. Phylogeny of the Paniceae (Poaceae: Panicoideae): integrating plastid DNA sequences and morphology into a new classification. Cladistics 28: 333356.
  • Muellner AN, Samuel R, Johnson SA, Cheek M, Pennington TD, Chase MW. 2003. Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences. American Journal of Botany 90: 471480.
  • Muellner AN, Savolainen V, Samuel R, Chase MW. 2006. The mahogany family ‘out-of-Africa’: divergence time estimation, global biogeographic patterns inferred from plastid rbcL DNA sequences, extant, and fossil distribution of diversity. Molecular Phylogenetics and Evolution 40: 236250.
  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853858.
  • Nicolas AN, Plunkett GM. 2009. The demise of subfamily Hydrocotyloideae (Apiaceae) and the re-alignment of its genera across the entire order Apiales. Molecular Phylogenetics and Evolution 53: 134151.
  • Nilsson S, Coetzee J, Grafstrom E. 1996. On the origin of the Sarcolaenaceae with reference to pollen morphological evidence. Grana 35: 321334.
  • Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM. 2008. A molecular phylogeny of the Solanaceae. Taxon 57: 11591181.
  • Ortiz S. 2006. Systematics of Cloiselia (Asteraceae, Mutisieae s.l.), a reinstated Madagascan genus. Systematic Botany 31: 421431.
  • Oxelman B, Backlund M, Bremer B. 1999. Relationships of the Buddlejaceae s.l.: investigated using parsimony jackknife and branch support analysis of chloroplast ndhF and rbcL sequence data. Systematic Botany 24: 164182.
  • Paton AJ, Springate D, Suddee S, Otieno D, Grayer RJ, Harley MM, Willis F, Simmonds MSJ, Powell MP, Savolainen V. 2004. Phylogeny and evolution of basils and allies (Ocimeae, Labiatae) based on three plastid DNA regions. Molecular Phylogenetics and Evolution 31: 277299.
  • Pell SK. 2004. Molecular systematics of the cashew family (Anacardiaceae). DPhil Thesis, Louisiana State University, Baton Rouge, LA.
  • Pell SK, Mitchell JD, Lowry PP, Randrianasolo A, Urbatsch LE. 2008. Phylogenetic split of Malagasy and African taxa of Protorhus and Rhus (Anacardiaceae) based on cpDNA trnL-trnF and nrDNA ETS and ITS sequence data. Systematic Botany 33: 375383.
  • Pelser PB, Kennedy AH, Tepe EJ, Shidler JB, Nordenstam B, Kadereit JW, Watson LE. 2010. Patterns and causes of incongruence between plastid and nuclear Senecioneae (Asteraceae) phylogenies. American Journal of Botany 97: 856873.
  • Perrier de la Bâthie H. 1936. Biogéographie des plantes de Madagascar. Paris: Société d'Éditions Géographiques, Maritimes et Coloniales.
  • Pillon Y. 2012. Time and tempo of diversification in the flora of New Caledonia. Botanical Journal of the Linnean Society 170: 288298.
  • Pirie MD, Doyle JA. 2012. Dating clades with fossils and molecules: the case of Annonaceae. Botanical Journal of the Linnean Society 169: 84116.
  • Plunkett GM, Soltis DE, Soltis PS. 1996. Higher level relationships of Apiales (Apiaceae and Araliaceae) based on phylogenetic analysis of rbcL sequences. American Journal of Botany 83: 499515.
  • Razafimandimbison SG, Appelhans MS, Rabarison H, Haevermans T, Rakotondrafara A, Rakotonandrasana SR, Ratsimbason M, Labat JN, Kessler PJA, Smets E, Cruaud C, Couloux A, Randrianarivelojosia M. 2010. Implications of a molecular phylogenetic study of the Malagasy genus Cedrelopsis and its relatives (Ptaeroxylaceae). Molecular Phylogenetics and Evolution 57: 258265.
  • Ree RH, Smith SA. 2008. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 414.
  • Renner SS, Strijk JS, Strasberg D, Thebaud C. 2010. Biogeography of the Monimiaceae (Laurales): a role for East Gondwana and long-distance dispersal, but not West Gondwana. Journal of Biogeography 37: 12271238.
  • Richardson JE, Fay MF, Cronk QCB, Bowman D, Chase MW. 2000. A phylogenetic analysis of Rhamnaceae using rbcL and trnL-F plastid DNA sequences. American Journal of Botany 87: 13091324.
  • Rogers ZS, Nickrent DL, Malecot V. 2008. Staufferia and Pilgerina: two new endemic monotypic arborescent genera of Santalaceae from Madagascar. Annals of the Missouri Botanical Garden 95: 391404.
  • Rydin C, Razafimandimbison SG, Bremer B. 2008. Rare and enigmatic genera (Dunnia, Schizocolea, Colletoecema), sisters to species-rich clades: phylogeny and aspects of conservation biology in the coffee family. Molecular Phylogenetics and Evolution 48: 7483.
  • Salariato DL, Zuloaga FO, Giussani LM, Morrone O. 2010. Molecular phylogeny of the subtribe Melinidinae (Poaceae: Panicoideae: Paniceae) and evolutionary trends in the homogenization of inflorescences. Molecular Phylogenetics and Evolution 56: 355369.
  • Sanmartin I, Ronquist F. 2004. Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53: 216243.
  • Saunders RMK, Su YCF, Xue B. 2011. Phylogenetic affinities of Polyalthia species (Annonaceae) with columellar-sulcate pollen: enlarging the Madagascan endemic genus Fenerivia. Taxon 60: 14071416.
  • Sauquet H, Doyle JA, Scharaschkin T, Borsch T, Hilu KW, Chatrou LW, Le Thomas A. 2003. Phylogenetic analysis of Magnoliales and Myristicaceae based on multiple data sets: implications for character evolution. Botanical Journal of the Linnean Society 142: 125186.
  • Sauquet H, Weston PH, Barker NP, Anderson CL, Cantrill DJ, Savolainen V. 2009. Using fossils and molecular data to reveal the origins of the Cape proteas (subfamily Proteoideae). Molecular Phylogenetics and Evolution 51: 3143.
  • Schaferhoff B, Fleischmann A, Fischer E, Albach DC, Borsch T, Heubl G, Muller KF. 2010. Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences. BMC Evolutionary Biology 10: 352.
  • Schatz GE. 1995. Malagasy/Indo-Malesian phytogeographic connections. In: Lourenço WR , ed. Biogéographie de Madagascar. Paris: ORSTOM, 7383.
  • Schatz GE. 2000. Endemism in the Malagasy tree flora. In: Lourenço WR , Goodman SM , eds. Diversity and Endemism in Madagascar. Paris: Mémoires de la Société de Biogéographie, 19.
  • Schatz GE. 2001. Generic tree flora of Madagascar. Kew: Royal Botanic Gardens; St Louis: Missouri Botanical Garden.
  • Schrire BD, Lavin M, Barker NP, Forest F. 2009. Phylogeny of the tribe Indigofereae (Leguminosae–Papilionoideae): geographically structured more in succulent-rich and temperate settings than in grass-rich environments. American Journal of Botany 96: 816852.
  • Schwarzbach AE, Ricklefs RE. 2000. Systematic affinities of Rhizophoraceae and Anisophylleaceae, and intergeneric relationships within Rhizophoraceae, based on chloroplast DNA, nuclear ribosomal DNA, and morphology. American Journal of Botany 87: 547564.
  • Simmons MP, Bacon CD, Cappa JJ, McKenna MJ. 2012. Phylogeny of Celastraceae subfamilies Cassinoideae and Tripterygioideae inferred from morphological characters and nuclear and plastid loci. Systematic Botany 37: 456467.
  • Simoes AO, Livshultz T, Conti E, Endress ME. 2007. Phylogeny and systematics of the Rauvolfioideae (Apocynaceae) based on molecular and morphological evidence. Annals of the Missouri Botanical Garden 94: 268297.
  • Sinou C, Forest F, Lewis GP, Bruneau A. 2009. The genus Bauhinia s.l. (Leguminosae): a phylogeny based on the plastid trnL-trnF region. Botany-Botanique 87: 947960.
  • Skema C. 2012. Toward a new circumscription of Dombeya (Malvales: Dombeyaceae): a molecular phylogenetic and morphological study of Dombeya of Madagascar and a new segregate genus, Andringitra. Taxon 61: 612628.
  • Smedmark JEE, Anderberg AA. 2007. Boreotropical migration explains hybridization between geographically distant lineages in the pantropical clade Sideroxyleae (Sapotaceae). American Journal of Botany 94: 14911505.
  • Spalik K, Downie SR. 2007. Intercontinental disjunctions in Cryptotaenia (Apiaceae, Oenantheae): an appraisal using molecular data. Journal of Biogeography 34: 20392054.
  • Stefanovic S, Krueger L, Olmstead RG. 2002. Monophyly of the Convolvulaceae and circumscription of their major lineages based on DNA sequences of multiple chloroplast loci. American Journal of Botany 89: 15101522.
  • Strijk JS, Noyes RD, Strasberg D, Cruaud C, Gavory F, Chase MW, Abbott RJ, Thébaud C. 2012. In and out of Madagascar: dispersal to peripheral islands, insular speciation and diversification of Indian Ocean daisy trees (Psiadia, Asteraceae). PLoS ONE 7: e42932.
  • Tank DC, Donoghue MJ. 2010. Phylogeny and phylogenetic nomenclature of the Campanulidae based on an expanded sample of genes and taxa. Systematic Botany 35: 425441.
  • Thulin M, Beier BA, Razafimandimbison SG, Banks HI. 2008. Ambilobea, a new genus from Madagascar, the position of Aucoumea, and comments on the tribal classification of the frankincense and myrrh family (Burseraceae). Nordic Journal of Botany 26: 218229.
  • Thulin M, Razafimandimbison SG, Chafe P, Heidari N, Kool A, Shore JS. 2012. Phylogeny of the Turneraceae clade (Passifloraceae s.l.): trans-Atlantic disjunctions and two new genera in Africa. Taxon 61: 308323.
  • Vidal-Russell R, Nickrent DL. 2008. Evolutionary relationships in the showy mistletoe family (Loranthaceae). American Journal of Botany 95: 10151029.
  • Wang W, Ortiz RD, Jacques FMB, Xiang XG, Li HL, Lin L, Li RQ, Liu Y, Soltis PS, Soltis DE, Chen ZD. 2012. Menispermaceae and the diversification of tropical rainforests near the Cretaceous–Paleogene boundary. New Phytologist 195: 470478.
  • Wanntorp L, Gotthardt K, Muellner AN. 2011. Revisiting the wax plants (Hoya, Marsdenieae, Apocynaceae): phylogenetic tree using the matK gene and psbA-trnH intergenic spacer. Taxon 60: 414.
  • Warren BH, Strasberg D, Bruggemann JH, Prys-Jones RP, Thebaud C. 2010. Why does the biota of the Madagascar region have such a strong Asiatic flavour? Cladistics 26: 526538.
  • Wells NA. 2003. Some hypotheses on the Mesozoic and Cenozoic paleoenvironmental history of Madagascar. In: Goodman SM , Benstead JP , eds. The natural history of Madagascar. Chicago, IL: University of Chicago Press, 1634.
  • Wikström N, Avino M, Razafimandimbison SG, Bremer B. 2010. Historical biogeography of the coffee family (Rubiaceae, Gentianales) in Madagascar: case studies from the tribes Knoxieae, Naucleeae, Paederieae and Vanguerieae. Journal of Biogeography 37: 10941113.
  • Wurdack KJ, Davis CC. 2009. Malpighiaceae phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. American Journal of Botany 96: 15511570.
  • Wurdack KJ, Hoffmann P, Chase MW. 2005. Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid rbcL and trnL-F DNA sequences. American Journal of Botany 92: 13971420.
  • Wurdack KJ, Hoffmann P, Samuel R, De Bruijn A, Van der Bank M, Chase MW. 2004. Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid rbcL DNA sequences. American Journal of Botany 91: 18821900.
  • Yoder AD, Nowak MD. 2006. Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annual Review of Ecology Evolution and Systematics 37: 405431.
  • Yuan YM, Song Y, Geuten K, Rahelivololona E, Wohlhauser S, Fischer E, Smets E, Kupfer P. 2004. Phylogeny and biogeography of Balsaminaceae inferred from ITS sequences. Taxon 53: 391403.
  • Yuan YM, Wohlhauser S, Moller M, Klackenberg J, Callmander MW, Kupfer P. 2005. Phylogeny and biogeography of Exacum (Gentianaceae): a disjunctive distribution in the Indian Ocean Basin resulted from long distance dispersal and extensive radiation. Systematic Biology 54: 2134.
  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292: 686693.