Ecological and anthropogenic effects on the genomic diversity of lemurs in Madagascar

Joseph D. Orkin*, Lukas F. K. Kuderna, Núria Hermosilla-Albala, Claudia Fontsere, Megan L. Aylward, Mareike C. Janiak, Nicole Andriaholinirina, Patricia Balaresque, Mary E. Blair, Jean Luc Fausser, Ivo Glynne Gut, Marta Gut, Matthew W. Hahn, R. Alan Harris, Julie E. Horvath, Christine Keyser, Andrew C. Kitchener, Minh D. Le, Esther Lizano, Stefan MerkerTilo Nadler, George H. Perry, Clément J. Rabarivola, Linett Rasmussen, Muthuswamy Raveendran, Christian Roos, Dong Dong Wu, Alphonse Zaramody, Guojie Zhang, Dietmar Zinner, Luca Pozzi, Jeffrey Rogers, Kyle Kai-How Farh, Tomas Marques Bonet

*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Abstract

Ecological variation and anthropogenic landscape modification have had key roles in the diversification and extinction of mammals in Madagascar. Lemurs represent a radiation with more than 100 species, constituting roughly one-fifth of the primate order. Almost all species of lemurs are threatened with extinction, but little is known about their genetic diversity and demographic history. Here, we analyse high-coverage genome-wide resequencing data from 162 unique individuals comprising 50 species of Lemuriformes, including multiple individuals from most species. Genomic diversity varies widely across the infraorder and yet is broadly consistent among individuals within species. We show widespread introgression in multiple genera and generally high levels of genomic diversity likely resulting from allele sharing that occurred during periods of connectivity and fragmentation during climatic shifts. We find distinct patterns of demographic history in lemurs across the ecogeographic regions of Madagascar within the last million years. Within the past 2,000 years, lemurs underwent major declines in effective population size that corresponded to the timing of human population expansion in Madagascar. In multiple regions of the island, we identified chronological trajectories of inbreeding that are consistent across genera and species, suggesting localized effects of human activity. Our results show how the extraordinary diversity of these long-neglected, endangered primates has been influenced by ecological and anthropogenic factors.
OriginalsprogEngelsk
Artikelnummer70
TidsskriftNature Ecology and Evolution
Vol/bind9
Sider (fra-til)42–56
Antal sider15
ISSN2397-334X
DOI
StatusUdgivet - 2025

Bibliografisk note

Funding Information:
We acknowledge the Duke Lemur Center and the European Association of Zoos and Aquaria (EAZA) Biobank for collecting primate samples. This is Duke Lemur Center publication no. 1593. We thank D. Pierron for access to the Malagasy human population data. J.D.O. was supported by the \u2018La Caixa\u2019 Foundation (ID 100010434) and the European Union\u2019s Horizon 2020 research and innovation programme under Marie Sk\u0142odowska-Curie grant agreement no. 847648 (LCF/BQ/PI20/11760004) and the Natural Sciences and Engineering Research Council of Canada (RGPIN-2023-04399, DGECR-2023-00272). Nous remercions le Conseil de recherches en sciences naturelles et en g\u00E9nie du Canada (CRSNG) de son soutien. T.M.B. is supported by funding from the European Research Council (ERC) under the European Union\u2019s Horizon 2020 research and innovation programme (grant agreement no. 864203), PID2021-126004NB-100 (MICIIN/FEDER, UE) and Secretaria d\u2019Universitats i Recerca and CERCA Programme del Departament d\u2019Economia i Coneixement de la Generalitat de Catalunya (GRC 2021 SGR 00177). L.F.K.K. was supported by an EMBO STF 8286. M.C.J. was supported by the Natural Environment Research Council (NE/T000341/1). This research was supported by the National Science Foundation to L.P. (BCS 1926105) and M.E.B. (BCS 1926215). P.B. was supported by the Mission pour les Initiatives Transverses et Interdisciplinaires (MITI) from the Centre National de la Recherche Scientifique (DEFI X-LiFE grant \u2018unknown living branches\u2019). The research reported in this article was funded by the Vietnamese Ministry of Science and Technology\u2019s Program 562 (grant no. \u0110T\u0110L.CN-64/19) to M.D.L. This project also received internal support from the Baylor College of Medicine. This research was enabled in part by support provided by Calcul Quebec ( www.calculquebec.ca ) and the Digital Research Alliance of Canada ( https://alliancecan.ca ).

Publisher Copyright:
© The Author(s), under exclusive licence to Springer Nature Limited 2024.

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