Cenozoichistoryofthetropicalmarinebiodiversityhotspot
The region with the highest marine biodiversity on our planet is known asthe Coral
Triangle or Indo-Australian Archipelago (IAA)1,2. Its enormous biodiversity has long
attracted the interest of biologists; however, the detailed evolutionary history
of theIAA biodiversity hotspot remains poorly understood3. Here we present a
high-resolution reconstruction of the Cenozoic diversity history of theIAAby inferring speciation–extinction dynamics using a comprehensive fossil dataset. We found that theIAA has exhibited a unidirectional diversification trend since about 25 million years ago, following a roughly logistic increase until a diversity plateau beginning about
2.6 million years ago. The growth of diversity was primarily controlled by diversity
dependency and habitat size, and also facilitated by the alleviation of thermal stress
after 13.9 million years ago. Distinct net diversification peaks were recorded at about
25, 20, 16, 12 and 5 million years ago, which were probably related to major tectonic
events in addition to climate transitions. Key biogeographic processes had far-reaching effects on theIAAdiversity as shown by the long-term waning oftheTethyandescendants versus the waxing of cosmopolitan andIAA taxa. Finally, it seems that the absence of major extinctionsand the Cenozoic cooling have been essential in making theIAA the richest marine biodiversity hotspot on Earth.
It is unclear how the global centre of marine biodiversity, theIAA, has
developed, and why its biodiversity is disproportionally high com-
pared to that of other tropical regions. These are key uncertainties in
organismal biology. We have gradually gained abetter understanding
of global-scale diversity dynamics throughout the Cenozoic4,5, revealing
complex waxing and waning of diversity related to climatic and other
environmental changes. However, regionally resolved Cenozoic diver-
sity trends remain poorly understood owing to the scarcity of historical
data and their compilation. This is particularly true for the tropics in
deeper time, making the origins of high biodiversity an enigma6 –8. The
current knowledge of the fossil record suggests that the locations of
peak diversity (that is, biodiversity hotspots) shifted throughout the
Cenozoic from the western Tethys during the Eocene to the Arabian
Peninsula during the late Eocene–Oligocene, before being established
atthe current location of theIAAin Southeast Asia in the early Miocene:
the process known asthe hopping hotspots model3,9. Plate tectonics is
postulated to be the ultimate driver of this process by regulating the
broad-scale availability and configuration of shallow-marine habitats
with successive continent collisions9. Each hop of the biodiversity hot-
spots from the ancient location to the new one was probably under-
pinned by considerable speciation and extinction events, but also could
be associated with the palaeobiogeographic shifts of some component
taxa tracking suitable habitats3. However, the detailed Cenozoic history
of theIAA hotspot remains elusive as explicated below. Better under-
standing the deep-time origin, evolution and maintenance of this most
diverse place in the marine realm is crucial for macroevolutionary and
macroecological studies and provides a solid theoretical framework
for conservation efforts.
As one of the most conspicuous biogeographic and biodiversity
patterns today, the IAA hotspot is characterized by an exceptional
concentration of coastal benthic species, whereas pelagic groups show
widespread distributions without a distinguished centre of diversity2,10.
Historical evidence from benthic taxonomic groups has advanced
our understanding of tropical diversification yet suffers from various
limitations. Recent molecular studies on coralsand reef fishes revealed
their biogeographic and evolutionary history to build theIAA hotspot,
1School of Biological Sciences, Area of Ecology and Biodiversity, The University of Hong Kong, Hong Kong, Hong Kong SAR. 2Swire Institute of Marine Science, The University of Hong Kong, Hong Kong, Hong Kong SAR. 3Institute for Climate and Carbon Neutrality, The University of Hong Kong, Hong Kong, Hong Kong SAR. 4Musketeers Foundation Institute of Data Science,
The University of Hong Kong, Hong Kong, Hong Kong SAR. 5Bonner Institut für Organismische Biologie, Paläontologie, Universität Bonn, Bonn, Germany. 6State Key Laboratory of Marine
Pollution, City University of Hong Kong, Hong Kong, Hong Kong SAR. 7CNRS, Institut des Sciences de l’Evolution de Montpellier, Université de Montpellier, Montpellier, France. 8Department of Geosciences, Princeton University, Princeton, NJ, USA. 9National Institute of Geological Sciences, University of the Philippines, Diliman, Quezon City, The Philippines. 10Marine Geological Survey, Mines and Geosciences Bureau, Quezon City, The Philippines. 11Department of Geological Engineering, Faculty of Mineral Technology, Institute Teknologi Nasional Yogyakarta,
Yogyakarta, Indonesia. 12Department of Geoscience, Interdisciplinary Graduate School of Science and Engineering, Shimane University, Matsue, Japan. 13Division of Earth Science,
Graduate School of Sciences and Technology for Innovation, Yamaguchi University, Yamaguchi, Japan. 14Paleontological Research Institution, Ithaca, NY, USA. 15Department of Earth and Atmospheric Sciences, Cornell University, New York, NY, USA. 16Naturalis Biodiversity Center, Leiden, The Netherlands. 17IBED, University of Amsterdam, Amsterdam, The Netherlands.
18National Museum of Nature and Science, Department of Geology and Paleontology, Tsukuba, Japan. 19These authors contributed equally: Skye Yunshu Tian, Moriaki Yasuhara, Fabien L.
Condamine. ✉e-mail: skyeystian@gmail.com; moriakiyasuhara@gmail.com