Ancient DNA is preserved in fish fossils from tropical lake sediments

Moritz Muschick*, Eliane Jemmi, Nicholas Lengacher, Stephanie Hänsch, Nathan Wales, Mary A. Kishe, Salome Mwaiko, Jorunn Dieleman, Mark Alexander Lever, Walter Salzburger, Dirk Verschuren, Ole Seehausen

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Tropical freshwater lakes are well known for their high biodiversity, and particularly the East African Great Lakes are renowned for their adaptive radiation of cichlid fishes. While comparative phylogenetic analyses of extant species flocks have revealed patterns and processes of their diversification, little is known about evolutionary trajectories within lineages, the impacts of environmental drivers, or the scope and nature of now-extinct diversity. Time-structured palaeodata from geologically young fossil records, such as fossil counts and particularly ancient DNA (aDNA) data, would help fill this large knowledge gap. High ambient temperatures can be detrimental to the preservation of DNA, but refined methodology now allows data generation even from very poorly preserved samples. Here, we show for the first time that fish fossils from tropical lake sediments yield endogenous aDNA. Despite generally low endogenous content and high sample dropout, the application of high-throughput sequencing and, in some cases, sequence capture allowed taxonomic assignment and phylogenetic placement of 17% of analysed fish fossils to family or tribe level, including remains which are up to 2700 years old or weigh less than 1 mg. The relationship between aDNA degradation and the thermal age of samples is similar to that described for terrestrial samples from cold environments when adjusted for elevated temperature. Success rates and aDNA preservation differed between the investigated lakes Chala, Kivu and Victoria, possibly caused by differences in bottom water oxygenation. Our study demonstrates that the sediment records of tropical lakes can preserve genetic information on rapidly diversifying fish taxa over time scales of millennia.

Original languageEnglish
Number of pages19
JournalMolecular Ecology
DOIs
Publication statusPublished - 13 Oct 2023

Bibliographical note

© 2023 The Authors.

Funding Information:
We thank the Tanzania Fisheries Research Institute (TAFIRI) for their collaboration on sediment coring in Lake Victoria. The Continental Scientific Drilling Facility at the University of Minnesota (USA) provided additional samples and core scanning data from Lake Kivu and Lake Victoria, and Pascal Isumbisho Mwapu (Institut Supérieur Pédagogique de la Gombe, Rwanda) and Martin Schmid (EAWAG, Switzerland) provided sample Kivu 4. The Genetic Diversity Centre at ETH Zürich, the Functional Genomics Centre Zürich and the University of Bern Next Generation Sequencing platform provided laboratory and HPC access and/or sequencing support. Silvia Bollhalder and Caroline Welte from the ETH Zürich Radiocarbon facility dated samples from Lake Kivu. Petra Boltshauser‐Kaltenrieder, Willi Tanner, Sandra Brügger, Alexander Bolland, Edwin Sombe, Harith Kalima, Boaz Jumbe, Toto Mohammed, Daniel Bwathondi, Daniel Chacha and Hamisi Ramadhani are gratefully acknowledged for their participation in the 2018 Lake Victoria coring campaign. We further thank the following colleagues for discussions on palaeolimnology, ancient DNA analysis, cichlid genomics, sediment chronology or project design: Andy Cohen, Tom Gilbert, Mikkel Winther Pedersen, Binia de Cahsan, Nare Ngoepe, Yunuén Temoltzin‐Loranca, Giulia Wienhues, Leighton King, Martin Grosjean, Blake Matthews, Willy Tinner, Barbara Bramanti, Nils Christian Stenseth, Jim Russell, Marie‐Theres Gansauge, Marcel Häsler, Curt Stager, José Granado, Angela Schlumbaum, Michael Hofreiter, Ludovic Orlando, Robert Hecky, Christine Lane, Joana Meier, David Marques, Pooja Singh, Andy Foote, Logan Kistler and the Seehausen group at the University of Bern and EAWAG. We further thank three anonymous reviewers and the handling editor, whose comments helped to improve the manuscript. This study was funded through the SNSF Sinergia grant CRSII5_183566 to OS. Coring in Lake Victoria was financed by a grant from the Strategy pool of the Faculty of Natural Sciences of the University of Bern to OS, the Institute of Plant Sciences of the University of Bern and the Department of Fish Ecology & Evolution at EAWAG. Lake Chala samples were extracted from cores collected by the Challacea project, jointly funded by the Research Foundation of Flanders (FWO, Belgium), the Danish National Research Council, the Deutsche Forschungsgemeinschaft (DFG, Germany) and the Dutch Research Council (NWO, The Netherlands) through the European Science Foundation's EuroCLIMATE programme. The collection of core KIVU12‐10A was supported by MacArthur Foundation Grant 11‐97251‐000‐INP to R. Hecky. The Centre for Ecology and Evolutionary Synthesis (CEES) at the University of Oslo provided laboratory access, consumables, sequencing and travel support to MM in the initial phase of the project. SH was supported by the ERC Advanced Grant ‘MedPlag’ (Grant No. 324249) to Barbara Bramanti. Open access funding provided by Universitat Bern.

Keywords

  • adaptive radiation
  • cichlid fish
  • conservation
  • diversification
  • evolution
  • palaeogenetics

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