Ancient DNA elucidates the lost world of western Indian Ocean giant tortoises and reveals a new extinct species from Madagascar - PubMed (original) (raw)

. 2023 Jan 13;9(2):eabq2574.

doi: 10.1126/sciadv.abq2574. Epub 2023 Jan 11.

Eva Graciá 2 3, Jason R Ali 4, Patrick D Campbell 5, Sandra D Chapman 6, V Deepak 1, Flora Ihlow 1, Nour-Eddine Jalil 7 8, Laure Pierre-Huyet 9, Karen E Samonds 10, Miguel Vences 11, Uwe Fritz 1

Affiliations

Ancient DNA elucidates the lost world of western Indian Ocean giant tortoises and reveals a new extinct species from Madagascar

Christian Kehlmaier et al. Sci Adv. 2023.

Abstract

Before humans arrived, giant tortoises occurred on many western Indian Ocean islands. We combined ancient DNA, phylogenetic, ancestral range, and molecular clock analyses with radiocarbon and paleogeographic evidence to decipher their diversity and biogeography. Using a mitogenomic time tree, we propose that the ancestor of the extinct Mascarene tortoises spread from Africa in the Eocene to now-sunken islands northeast of Madagascar. From these islands, the Mascarenes were repeatedly colonized. Another out-of-Africa dispersal (latest Eocene/Oligocene) produced on Madagascar giant, large, and small tortoise species. Two giant and one large species disappeared c. 1000 to 600 years ago, the latter described here as new to science using nuclear and mitochondrial DNA. From Madagascar, the Granitic Seychelles were colonized (Early Pliocene) and from there, repeatedly Aldabra (Late Pleistocene). The Granitic Seychelles populations were eradicated and later reintroduced from Aldabra. Our results underline that integrating ancient DNA data into a multi-evidence framework substantially enhances the knowledge of the past diversity of island faunas.

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Figures

Fig. 1.

Fig. 1.. Placement of extinct Malagasy and Mascarene giant tortoises in the tortoise phylogeny.

The shown maximum likelihood (ML) topology is based on near-complete mitochondrial genomes (15,537 bp) of all genera and species groups of tortoises (Testudinidae). Codes preceding scientific names are DNA Data Bank of Japan (DDJB)/European Nucleotide Archive (ENA)/GenBank accession numbers or museum numbers. Genus names of extinct taxa bear dagger symbols. Numbers at nodes are thorough bootstrap values and posterior probabilities from a Bayesian analysis yielding the same topology. Asterisks indicate maximum support under both approaches. Colored boxes represent different geographic regions. Inset pictures show the past and present diversity of native tortoise species of the western Indian Ocean (extinct species are in gray). Top: Madagascar, from left to right, †Aldabrachelys abrupta, †Al. grandidieri, Pyxis planicauda, P. arachnoides, †Astrochelys rogerbouri n. sp., As. yniphora, and As. radiata. Center: Granitic Seychelles (extinct), Aldabra, Al. gigantea. Bottom: Mascarenes, from left to right, †Cylindraspis indica (Réunion), †C. inepta, †C. triserrata (both Mauritius), †C. vosmaeri, and †C. peltastes (both Rodrigues). Sizes to scale, corresponding to reported maximum SCLs (8). Artwork: Michal Rössler; photo of Al. gigantea: Massimo Delfino.

Fig. 2.

Fig. 2.. Fossil-calibrated time tree for tortoises (Testudinidae).

This analysis is based on the same dataset as that presented in Fig. 1. For each node, estimated mean ages and 95% highest posterior density intervals are shown. Codes preceding scientific names are DDJB/ENA/GenBank accession numbers or museum numbers. Genus names of extinct taxa bear dagger symbols. The red circles indicate fossil calibration points (see detailed explanation in the Supplementary Materials): (A) Hadrianus majusculus, 100.5 to 50.3 Ma ago; (B) Cheirogaster maurini and Gigantochersina ammon, 66.0 to 33.9 Ma ago; (C) Cheirogaster maurini, 47.8 to 33.9 Ma ago; and (D) Chelonoidis hesternus, 33.9 to 11.8 Ma ago. Inset: Aldabrachelys grandidieri, paralectotype (MNHN.F.MAD3502; photo: Nour-Eddine Jalil).

Fig. 3.

Fig. 3.. Tortoise phylogeny based on nuclear DNA sequences, including an extinct Malagasy species (highlighted in red).

The shown ML tree is based on four nuclear loci (HMGB2, _HNF1_α, R35, and TB73; 3047 bp). Sample codes precede taxon names; for accession numbers, see table S3. Numbers at nodes are thorough bootstrap values and posterior probabilities from a Bayesian analysis yielding the same topology. Asterisks indicate maximum support under both approaches. Inset top: Holotype of Astrochelys rogerbouri n. sp. (photo: Uwe Fritz), bottom: As. yniphora (photo: Gerald Kuchling), the sister species of the extinct tortoise.

Fig. 4.

Fig. 4.. Dispersal routes and radiation centers of western Indian Ocean giant tortoises.

Black arrows: Malagasy tortoise radiation, including giant Aldabrachelys; red arrows: Mascarene Cylindraspis radiation. Note that the Cylindraspis lineage evolved and diversified on the now-sunken northern islands of the Réunion hot spot (now submersed Saya de Malha, Nazareth, and Cargados Carajos banks), while Aldabrachelys evolved on Madagascar and later dispersed to the Granitic Seychelles and subsequently to Aldabra. The map shows the key physiographical features of the western Indian Ocean. The base image was created using GeoMapApp (73). The ocean bed down to 120 m is shaded white and corresponds with the lowest lows in global sea level back to 630,000 years ago (74).

Fig. 5.

Fig. 5.. Distribution of extant and extinct tortoise species on Madagascar and western Indian Ocean islands.

Genus names of extinct taxa bear dagger symbols. If not otherwise indicated, genetically unconfirmed subfossil records are mapped (summarized from different sources; see data file S5). Divided or overlapping symbols indicate syntopic occurrences of the respective species. Distribution ranges for extant species are from the IUCN Checklist and Atlas of the Turtles of the World (8); introduced populations are disregarded. For the small Mascarene islands (Réunion, Mauritius, and Rodrigues), only one symbol per Cylindraspis species is shown; all species identifications are genetically supported (21). Native Al. gigantea are today restricted to Aldabra. The map for Pyxis spp. shows two rivers mentioned in the Discussion.

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