Biogeography of the Sunda Shelf revisited: Insights from Macaranga section Pruinosae (Euphorbiaceae)

The Southeast Asian region of Sundaland is among the world’s major biodiversity hotspots. The region’s biodiversity coupled with its complex and dynamic geographic and climatic histories makes it an ideal region to study the various factors that determine the diversification and distribution patterns of tropical biota. Here we investigate the biogeographic patterns in the partly myrmecophytic Macaranga section Pruinosae to reveal some of the factors that play a role in determining the distribution of biota in Sundaland. We used single nucleotide polymorphisms (SNP) data derived from GBS, a next generation sequencing technique, in maximum likelihood and cluster analyses to determine phylogenetic relationships and population structures within this taxonomic section. Bayesian inference based on secondary calibration points and ancestral area reconstruction analyses were performed to infer spatial–temporal origins of the major lineages in the section. The results from these analyses were further substantiated using nuclear microsatellite data obtained from a broader sample set of two widely distributed species within the section: Macaranga gigantea and Macaranga pruinosa. Phylogenetic and cluster analyses reveal four well-defined, discrete species groups within section Pruinosae, all of which but one originated in Borneo with the crown node dated at 3.58 mya. Biogeographic patterns within the species reveal a biogeographic barrier between east and west Sundaland besides bringing to light the role played by various geological factors, especially the Crocker Range, on Borneo. Patterns also reveal a biogeographic barrier between the Bangka/Belitung islands and Sumatra for ant-free, swamp-adapted species. This study provides evidence that geographic barriers, edaphic conditions, and ecological adaptations are tightly linked and that their mutual interaction determines the diversification and distribution of species.

[1]  T. Salles,et al.  Quaternary landscape dynamics boosted species dispersal across Southeast Asia , 2021, Communications Earth & Environment.

[2]  L. Rüber,et al.  Impact of Pleistocene Eustatic Fluctuations on Evolutionary Dynamics in Southeast Asian Biodiversity Hotspots. , 2021, Systematic biology.

[3]  Komisi Penyelamatan,et al.  International Union for Conservation of Nature , 2021, Permanent Missions to the United Nations, No. 309.

[4]  J. Leonard,et al.  Ancient Divergence Driven by Geographic Isolation and Ecological Adaptation in Forest Dependent Sundaland Tree Squirrels , 2020, Frontiers in Ecology and Evolution.

[5]  L. Husson,et al.  Evidence of Sundaland’s subsidence requires revisiting its biogeography , 2020, Journal of Biogeography.

[6]  Isaac Overcast,et al.  ipyrad: Interactive assembly and analysis of RADseq datasets , 2020, Bioinform..

[7]  Deren A. R. Eaton,et al.  Toytree: A minimalist tree visualization and manipulation library for Python , 2019, Methods in Ecology and Evolution.

[8]  Yan Yu,et al.  RASP 4: ancestral state reconstruction tool for multiple genes and characters. , 2019, Molecular biology and evolution.

[9]  J. Walker GSA Geologic Time Scale v. 5.0 , 2019 .

[10]  A. Harris,et al.  Species Boundaries and Parapatric Speciation in the Complex of Alpine Shrubs, Rosa sericea (Rosaceae), Based on Population Genetics and Ecological Tolerances , 2019, Front. Plant Sci..

[11]  W. Murphy,et al.  Comparative Phylogeography of Forest-Dependent Mammals Reveals Paleo-Forest Corridors throughout Sundaland , 2018, The Journal of heredity.

[12]  Sebastián Duchêne,et al.  BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis , 2018, bioRxiv.

[13]  Fengyuan Li,et al.  Paleocene-Eocene and Plio-Pleistocene sea-level changes as "species pumps" in Southeast Asia: Evidence from Althepus spiders. , 2018, Molecular phylogenetics and evolution.

[14]  M. Suchard,et al.  Posterior summarisation in Bayesian phylogenetics using Tracer , 2022 .

[15]  M. Fujita,et al.  Within‐island diversification underlies parachuting frog (Rhacophorus) species accumulation on the Sunda Shelf , 2018 .

[16]  U. Maschwitz,et al.  On benefits of indirect defence: short- and long-term studies of antiherbivore protection via mutualistic ants , 2001, Oecologia.

[17]  Jesse L. Grismer,et al.  Out of Borneo, again and again: Biogeography of the Stream Toad genus Ansonia Stoliczka (Anura: Bufonidae) and the discovery of the first limestone cave-dwelling species , 2016 .

[18]  R. Bouckaert,et al.  bModelTest: Bayesian phylogenetic site model averaging and model comparison , 2016, bioRxiv.

[19]  U. Maschwitz,et al.  Taxonomic Revision of the Obligate Plant-Ants of the Genus Crematogaster Lund (Hymenoptera: Formicidae: Myrmicinae), Associated with Macaranga Thouars (Euphorbiaceae) on Borneo and the Malay Peninsula , 2016 .

[20]  J. Schenk,et al.  Consequences of Secondary Calibrations on Divergence Time Estimates , 2016, PloS one.

[21]  U. Maschwitz,et al.  Phylogeography of three closely related myrmecophytic pioneer tree species in SE Asia: implications for species delimitation , 2016, Organisms Diversity & Evolution.

[22]  H. Watson Remarks On the Geographical Distribution of British Plants; Chiefly in Connection With Latitude, Elevation, and Climate , 2015 .

[23]  L. Knowles,et al.  Species‐specific responses to island connectivity cycles: refined models for testing phylogeographic concordance across a Mediterranean Pleistocene Aggregate Island Complex , 2015, Molecular ecology.

[24]  S. Renner,et al.  Phylogenetics and molecular clocks reveal the repeated evolution of ant-plants after the late Miocene in Africa and the early Miocene in Australasia and the Neotropics. , 2015, The New phytologist.

[25]  L. Knowles,et al.  Genomic tests of the species‐pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands , 2015, Evolution; international journal of organic evolution.

[26]  J. Leonard,et al.  Phylogeography of vertebrates on the Sunda Shelf: a multi‐species comparison , 2015 .

[27]  N. Matzke,et al.  Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. , 2014, Systematic biology.

[28]  L. Maiorano,et al.  Borneo and Indochina are major evolutionary hotspots for Southeast Asian biodiversity. , 2014, Systematic biology.

[29]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[30]  P. V. Van Welzen,et al.  Dated Phylogenies of the Sister Genera Macaranga and Mallotus (Euphorbiaceae): Congruence in Historical Biogeographic Patterns? , 2014, PloS one.

[31]  B. Fiala,et al.  High gene flow in two thrips-pollinated South-East Asian pioneer trees: genetic diversity and population structure of Macaranga hypoleuca and M. beccariana(Euphorbiaceae) , 2013 .

[32]  Q. Guo,et al.  Global variation in elevational diversity patterns , 2013, Scientific Reports.

[33]  K. Cameron,et al.  Comparative phylogeography of the Smilax hispida group (Smilacaceae) in eastern Asia and North America--implications for allopatric speciation, causes of diversity disparity, and origins of temperate elements in Mexico. , 2013, Molecular phylogenetics and evolution.

[34]  P. Lymberakis,et al.  Phylogenetic position, origin and biogeography of Palearctic and Socotran blind-snakes (Serpentes: Typhlopidae). , 2013, Molecular phylogenetics and evolution.

[35]  C. Specht,et al.  Influence of the geological history of the Trans‐Mexican Volcanic Belt on the diversification of Nolina parviflora (Asparagaceae: Nolinoideae) , 2013 .

[36]  J. Schenk Biogeographical diversification of Mentzelia section Bartonia in western North America , 2013 .

[37]  H. Slabbekoorn,et al.  Ecological speciation along an elevational gradient in a tropical passerine bird? , 2013, Journal of evolutionary biology.

[38]  L. Bernatchez,et al.  Glacial cycles as an allopatric speciation pump in north‐eastern American freshwater fishes , 2013, Molecular ecology.

[39]  Jamie R. Oaks,et al.  Did geckos ride the Palawan raft to the Philippines? , 2012 .

[40]  R. Morley Biotic Evolution and Environmental Change in Southeast Asia: A review of the Cenozoic palaeoclimate history of Southeast Asia , 2012 .

[41]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[42]  Carsten Rahbek,et al.  The patterns and causes of elevational diversity gradients , 2012 .

[43]  David J. Lohman,et al.  Biogeography of the Indo-Australian Archipelago , 2011 .

[44]  Campbell O. Webb,et al.  Soils on exposed Sunda Shelf shaped biogeographic patterns in the equatorial forests of Southeast Asia , 2011, Proceedings of the National Academy of Sciences.

[45]  P. B. Matheny,et al.  DEALING WITH INCOMPLETE TAXON SAMPLING AND DIVERSIFICATION OF A LARGE CLADE OF MUSHROOM‐FORMING FUNGI , 2011, Evolution; international journal of organic evolution.

[46]  Robert J. Elshire,et al.  A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species , 2011, PloS one.

[47]  M. Hasegawa,et al.  A time‐calibrated phylogenetic approach to assessing the phylogeography, colonization history and phenotypic evolution of snakes in the Japanese Izu Islands , 2011 .

[48]  F. Sheldon,et al.  REVISITING WALLACE'S HAUNT: COALESCENT SIMULATIONS AND COMPARATIVE NICHE MODELING REVEAL HISTORICAL MECHANISMS THAT PROMOTED AVIAN POPULATION DIVERGENCE IN THE MALAY ARCHIPELAGO , 2011, Evolution; international journal of organic evolution.

[49]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[50]  D. Woodruff Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity , 2010, Biodiversity and Conservation.

[51]  B. Fiala,et al.  Comparative chloroplast DNA phylogeography of two tropical pioneer trees, Macaranga gigantea and Macaranga pearsonii (Euphorbiaceae) , 2010, Tree Genetics & Genomes.

[52]  Rafe M. Brown,et al.  The role of repeated sea-level fluctuations in the generation of shrew (Soricidae: Crocidura) diversity in the Philippine Archipelago. , 2009, Molecular phylogenetics and evolution.

[53]  W. Clemens The Evolution of Artiodactyls , 2009 .

[54]  M. Stephens,et al.  Inferring weak population structure with the assistance of sample group information , 2009, Molecular ecology resources.

[55]  R. Corlett The Ecology of Tropical East Asia , 2009 .

[56]  C. Cannon,et al.  The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance , 2009, Proceedings of the National Academy of Sciences.

[57]  R. Ricklefs,et al.  Adaptation and diversification on islands , 2009, Nature.

[58]  J. Pritchard,et al.  Documentation for structure software : Version 2 . 3 , 2009 .

[59]  James F. Smith,et al.  Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae) , 2009, Proceedings of the Royal Society B: Biological Sciences.

[60]  P. S. Ashton,et al.  The genus Macaranga : a prodromus , 2008 .

[61]  S. Ho Calibrating molecular estimates of substitution rates and divergence times in birds , 2007 .

[62]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: dominant markers and null alleles , 2007, Molecular ecology notes.

[63]  B. Fiala,et al.  A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridization, vicariance and long‐distance dispersals , 2006, Molecular ecology.

[64]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[65]  C. Hunt,et al.  Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? , 2005 .

[66]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[67]  C. Carpenter The environmental control of plant species density on a Himalayan elevation gradient , 2005 .

[68]  B. Fiala,et al.  AFLP analysis of phylogenetic relationships among myrmecophytic species of Macaranga(Euphorbiaceae) and their allies , 2004, Plant Systematics and Evolution.

[69]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[70]  S. Abbo,et al.  Modified CTAB Procedure for DNA Isolation from Epiphytic Cacti of the Genera Hylocereus and Selenicereus (Cactaceae) , 1999, Plant Molecular Biology Reporter.

[71]  Ju¨rgen Haffer Alternative models of vertebrate speciation in Amazonia: an overview , 1997, Biodiversity & Conservation.

[72]  U. Maschwitz,et al.  Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association , 1994, Oecologia.

[73]  A. Helbig,et al.  Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis , 1989, Oecologia.

[74]  E. Meijaard Mammals of south‐east Asian islands and their Late Pleistocene environments , 2003 .

[75]  T. Brooks,et al.  Habitat Loss and Extinction in the Hotspots of Biodiversity , 2002 .

[76]  L. K. Wang,et al.  EVOLUTION OF MYRMECOPHYTISM IN WESTERN MALESIAN MACARANGA (EUPHORBIACEAE) , 2001, Evolution; international journal of organic evolution.

[77]  U. Maschwitz,et al.  Molecular analysis of phylogenetic relationships among Myrmecophytic macaranga species (Euphorbiaceae). , 2001, Molecular phylogenetics and evolution.

[78]  H. Voris Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations , 2000 .

[79]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[80]  T. Brooks,et al.  Hotspots Revisited: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions , 2000 .

[81]  R. Mittermeier,et al.  Biodiversity hotspots for conservation priorities , 2000, Nature.

[82]  T. Boller,et al.  Reduced Chitinase Activities in Ant Plants of the Genus Macaranga , 1999, Naturwissenschaften.

[83]  U. Maschwitz,et al.  Diversity, evolutionary specialization and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia , 1999 .

[84]  J. Palmer,et al.  Chloroplast DNA variation and the recent radiation of the giant senecios (Asteraceae) on the tall mountains of eastern Africa. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[85]  J. Dodson,et al.  Phylogeographic structure in mitochondrial DNA of a South‐east Asian freshwater fish, Hemibagrus nemurus (Siluroidei; Bagridae) and Pleistocene sea‐level changes on the Sunda shelf , 1995 .

[86]  L. Heaney A synopsis of climatic and vegetational change in Southeast Asia , 1991 .

[87]  W. Bond The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence , 1989 .

[88]  M. Nei Molecular Evolutionary Genetics , 1987 .