Topographic barriers drive the pronounced genetic subdivision of a range-limited fossorial rodent

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Due to their limited dispersal ability, fossorial species with predominantly belowground activity usually show increased levels of population subdivision across relatively small spatial scales. This may be exacerbated in harsh mountain ecosystems, where landscape geomorphology limits species' dispersal ability and leads to small effective population sizes, making species relatively vulnerable to environmental change. To better understand the environmental drivers of species' population subdivision in remote mountain ecosystems, particularly in understudied high-elevation systems in Africa, we studied the giant root-rat (Tachyoryctes macrocephalus), a fossorial rodent confined to the afro-alpine ecosystem of the Bale Mountains in Ethiopia. Using mitochondrial and low-coverage nuclear genomes, we investigated 77 giant root-rat individuals sampled from nine localities across its entire ~1000 km2 range. Our data revealed a distinct division into a northern and southern group, with no signs of gene flow, and higher nuclear genetic diversity in the south. Landscape genetic analyses of the mitochondrial and nuclear genomes indicated that population subdivision was driven by slope and elevation differences of up to 500 m across escarpments separating the north and south, potentially reinforced by glaciation of the south during the Late Pleistocene (~42,000–16,000 years ago). Despite this landscape-scale subdivision between the north and south, weak geographic structuring of sampling localities within regions indicated gene flow across distances of at least 16 km at the local scale, suggesting high, aboveground mobility for relatively long distances. Our study highlights that despite the potential for local-scale gene flow in fossorial species, topographic barriers can result in pronounced genetic subdivision. These factors can reduce genetic variability, which should be considered when developing conservation strategies.

OriginalsprogEngelsk
Artikelnummere17271
TidsskriftMolecular Ecology
Vol/bind33
Udgave nummer5
Antal sider16
ISSN0962-1083
DOI
StatusUdgivet - 2024

Bibliografisk note

Funding Information:
This work was supported by the German Research Council (DFG) in the framework of the joint Ethio-European DFG Research Unit 2358 “The Mountain Exile Hypothesis. How humans benefited from and re-shaped African high-altitude ecosystems during Quaternary climate changes” [FA-925/14-1], [OP-219/10-2] and [SCHA-2085/3-1]. We are grateful to the Ethiopian Wildlife Conservation Authority for providing us with permits to carry out research in Ethiopia. We thank the College of Natural and Computational Sciences (Addis Ababa University), the Department of Plant Biology and Biodiversity Management (Addis Ababa University), the Frankfurt Zoological Society, the Ethiopian Wolf Project, and the Bale Mountains National Park for their cooperation and kind permission to conduct fieldwork. We are thankful to Awol Assefa, Wege Abebe, Mohammed Ahmed Muhammed, and Katinka Thielsen for contributing to the preparation and implementation of the fieldwork. Field work would not have been possible without the assistance of the escort team in sample collection, logistics, and safety guarantee in the field, in particular Usman Abdella, Hamza Ahmed, Mohammed Kadir, Kasim Adem, Hussein Umer, and Sophie Haje. We thank Christian Lampei for input on landscape genetic analyses and Alexander Groos for the input on Late Pleistocene glaciation. The research was also supported by Villum Fonden Young Investigator Programme, grant no 13151 and Independent Research Fund Denmark, Sapere Aude: DFF-Forskningsleder, grant no 9064-00025B to EDL. Last, we thank C. Riginos, A. Angus Davison, and the three reviewers (V. Wishingrad and two anonymous) for their comments, which greatly improved the quality of this manuscript. Open Access funding enabled and organized by Projekt DEAL.

Funding Information:
Benefit sharing: This study was designed as a joint Ethio‐European research collaboration ‘The Mountain Exile Hypothesis’ which was developed by scientists from Germany, Ethiopia, Switzerland, the United Kingdom, and Spain ( https://www.uni‐marburg.de/en/fb19/dfg2358/about‐us ). Genetic samples were collected by German (VMR, LW DGS) and an Ethiopian scientist (AA; all listed as co‐authors) with the help from a local escort team. Sample collection was permitted by the Ethiopian Wildlife Conservation Authority and supported by the Bale Mountain National Park. Our project is committed to international scientific partnerships as can be seen in the international author lists with authors from Denmark, Ethiopia, Czech Republic, and Germany. The research addresses a priority concern, in this case the conservation of the studied organism.

Funding Information:
This work was supported by the German Research Council (DFG) in the framework of the joint Ethio‐European DFG Research Unit 2358 “The Mountain Exile Hypothesis. How humans benefited from and re‐shaped African high‐altitude ecosystems during Quaternary climate changes” [FA‐925/14‐1], [OP‐219/10‐2] and [SCHA‐2085/3‐1]. We are grateful to the Ethiopian Wildlife Conservation Authority for providing us with permits to carry out research in Ethiopia. We thank the College of Natural and Computational Sciences (Addis Ababa University), the Department of Plant Biology and Biodiversity Management (Addis Ababa University), the Frankfurt Zoological Society, the Ethiopian Wolf Project, and the Bale Mountains National Park for their cooperation and kind permission to conduct fieldwork. We are thankful to Awol Assefa, Wege Abebe, Mohammed Ahmed Muhammed, and Katinka Thielsen for contributing to the preparation and implementation of the fieldwork. Field work would not have been possible without the assistance of the escort team in sample collection, logistics, and safety guarantee in the field, in particular Usman Abdella, Hamza Ahmed, Mohammed Kadir, Kasim Adem, Hussein Umer, and Sophie Haje. We thank Christian Lampei for input on landscape genetic analyses and Alexander Groos for the input on Late Pleistocene glaciation. The research was also supported by Villum Fonden Young Investigator Programme, grant no 13151 and Independent Research Fund Denmark, Sapere Aude: DFF‐Forskningsleder, grant no 9064‐00025B to EDL. Last, we thank C. Riginos, A. Angus Davison, and the three reviewers (V. Wishingrad and two anonymous) for their comments, which greatly improved the quality of this manuscript. Open Access funding enabled and organized by Projekt DEAL.

Publisher Copyright:
© 2024 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

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