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Diversification of Gastropods Reflects Drainage Evolution in Africa Anna Mahulu, Björn Stelbrink, Bert Van Bocxlaer, Frank Riedel, Christian Albrecht

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Diversification of Gastropods Reflects Drainage Evolution in Africa Anna Mahulu, Björn Stelbrink, Bert Van Bocxlaer, Frank Riedel, Christian Albrecht Going with the flow? Diversification of gastropods reflects drainage evolution in Africa Anna Mahulu, Björn Stelbrink, Bert van Bocxlaer, Frank Riedel, Christian Albrecht To cite this version: Anna Mahulu, Björn Stelbrink, Bert van Bocxlaer, Frank Riedel, Christian Albrecht. Going with the flow? Diversification of gastropods reflects drainage evolution in Africa. Journal of Biogeography, Wiley, 2021, 48 (7), pp.1579-1593. 10.1111/jbi.14096. hal-03320817 HAL Id: hal-03320817 https://hal.archives-ouvertes.fr/hal-03320817 Submitted on 16 Aug 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Received: 16 November 2020 | Revised: 22 January 2021 | Accepted: 1 February 2021 DOI: 10.1111/jbi.14096 RESEARCH ARTICLE Going with the flow? Diversification of gastropods reflects drainage evolution in Africa Anna Mahulu1 | Björn Stelbrink1,2 | Bert Van Bocxlaer3,4 | Frank Riedel5 | Christian Albrecht1,6 1Department of Animal Ecology and Systematics, Justus Liebig University Abstract Giessen, Giessen, Germany Aim: The roles of geodynamics, climatic variability and landscape evolution in shap- 2Department of Environmental Sciences, Zoological Institute, University of Basel, ing aquatic biodiversity patterns on the African continent remain poorly understood. Basel, Switzerland We studied the geographical origin and phylogenetic relationships of an Afrotropical 3 CNRS, Univ. Lille, UMR 8198 – Evo- Eco- freshwater snail genus to examine the role of drainage evolution on diversification Paleo, Lille, France and range evolution. The relevance of fish provinces in bio- regionalization of inverte- 4Limnology Unit, Department of Biology, Ghent University, Ghent, Belgium brates was explored, as well as the evolution of habitat specificity. 5 Institute of Geological Sciences, Freie Location: Africa including Madagascar. Universität Berlin, Berlin, Germany Taxon: Lanistes (Gastropoda: Ampullariidae). 6Department of Biology, Mbarara University of Science and Technology, Methods: Based on a sampling covering the entire geographical range, we recon- Mbarara, Uganda structed a fossil- calibrated multi- locus molecular phylogeny using maximum likelihood Correspondence and Bayesian inference approaches. After applying species delimitation methods, we Christian Albrecht, Department of Animal estimated ancestral areas and habitats and examined rates of diversification through Ecology and Systematics, Justus Liebig University Giessen, Heinrich- Buff- Ring 26, time using lineage through time plots. 35392 Giessen, Germany. Results: RAxML and MrBayes analyses resulted in highly congruent topologies and Email: [email protected] giessen.de a strongly supported phylogeny. Our BEAST analysis indicate that Lanistes probably originated in the Eocene about 50 Ma and the most recent common ancestor (MRCA) Funding information CA, BS: Deutsche Forschungsgemeinschaft of all 23 Lanistes OTUs in our study may have inhabited an area including the Central (DFG); CA: SCHR352/9- 1, AL1076/5- 2 African and adjacent Lower Guinean biogeographical regions. A steeper increase in and AL1076/6- 2; BS: STE 2460/2- 1 and STE 2460/3- 1; AM: Deutscher species accumulation from the middle Miocene (c. 15 to 10 Ma), followed by a de- Akademischer Austauschdienst (DAAD); crease towards the present was found. Sympatry and jump dispersal were the com- BVB: Postdoctoral Fellowship BEL 1154574 STP of the Alexander von mon cladogenetic events and only a single anagenetic dispersal event was detected. Humboldt Foundation, grant FEDER- The biogeographical analyses further suggest that Madagascar was colonized from ERC- EVORAD by the French National Centre for Scientific Research and the East Africa and that the Zambezi River was colonized at least twice independently. European Union through the European Seven species are confined to rivers and three live exclusively in lakes. The estimation Fund for Regional Development (FEDER) in the Region Hauts- de- France, and of ancestral habitats suggested that the MRCA of all Lanistes probably evolved in a fieldwork support by the Fonds voor riverine habitat. Wetenschappelijk Onderzoek Vlaanderen, the Belgian Federal Directorate General Main conclusions: The diversification of Lanistes started in the Eocene and occurred for Development Cooperation and the at a constant pace apart from a possible climate- related increase in the Miocene. This Belgian Science Policy. Equal contribution: Björn Stelbrink and Christian Albrecht. This is an open access article under the terms of the Creative Commons Attribution- NonCommercial- NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non- commercial and no modifications or adaptations are made. © 2021 The Authors. Journal of Biogeography published by John Wiley & Sons Ltd. Journal of Biogeography. 2021;48:1579–1593. wileyonlinelibrary.com/journal/jbi | 1579 1580 | MAHULU ET al. study highlights the significance of temporal geographical isolation of river systems and subsequent reconnection in clade diversification and of jump dispersal in range evolution. More comparative analyses across various taxa are needed to obtain a bet- ter understanding of African freshwater biodiversity. KEYWORDS Ampullariidae, biogeography, dispersal, East African Rift System, fossil record, molluscs, radiation, river basin 1 | INTRODUCTION such as rapids and falls, inter- basin dispersal and, in rare cases, trans- oceanic dispersal as well as vicariance to have been involved (see, Africa is renowned for its terrestrial megafauna and biodiver- e.g. Daniels et al., 2015). Despite the potential of phylogenetic, bio- sity hotspots in rainforest and savannah (e.g. Myers et al., 2000). geographical and phylogeographical studies for the reconstruction Freshwater life is, however, also very diverse with, among others, of landscape/drainage evolution, there is a significant bias towards >3000 species of fishes (Lévêque et al., 2008), and diverse inverte- studies on lakes rather than river systems. This bias is in part caused brates such as crabs, dragonflies and molluscs (Holland et al., 2012). not only by the attractiveness of spectacular species radiations in This freshwater biodiversity is assumed to have largely arisen be- the tectonic lakes but also the practical advantages of studying evo- cause of the very heterogeneous landscape and especially a hydro- lutionary processes in a comparatively small, insular system as op- scape in which a mosaic of old and young rivers as well as lakes and posed to vast drainages. Most of the few continental- scale studies extensive wetlands exists at various spatial scales (Thieme et al., on the evolution of aquatic biodiversity are based on fish such as 2005). haplochromine cichlids (e.g. Schwarzer et al., 2009), squeaker cat- The current complexity of African aquatic ecosystems and their fish (Synodontis spp.; Day et al., 2013) and spiny eels (Mastacembelus faunas partly traces back to the breakup of Gondwana (Moore & spp.; Day et al., 2017). Consequently, biogeographical regions are Larkin, 2001). However, the recent biodiversity represents an as- mainly delineated based on diversity patterns in fish (Lévêque et al., semblage of species that originated on Gondwana, complemented 2008). Given that most fish are highly mobile and may disperse over by Cenozoic colonizers from Asia. Geological processes including large distances, against the flow, across barriers or via short- term dome formation and the rifting that created the East African Rift connections during wetter conditions, dispersal patterns may differ System (EARS) played a pivotal role in shaping the continent and drastically from those in most invertebrates. In addition, fish trans- its aquatic ecosystems (Ring et al., 2018; Salzburger et al., 2014). locations by humans may obscure biogeographical patterns (e.g. Van Rifting gave rise to large lakes such as Lakes Tanganyika and Malawi Steenberge et al., 2020). Biogeographical studies of less mobile in- and modified the course and hydrographic connectivity of ancient vertebrates may allow reconstruction of hydrographic connectivity river systems such as the Congo River (Stankiewicz & de Wit, 2006). of drainages through time more reliably. However, beyond a detailed However, the roles of rifting in shaping aquatic communities and bio- study on the crab family Potamonautidae (Daniels et al., 2015), which diversity patterns over time are still largely unexplored. revealed historical drainage connectivity and transoceanic dispersal Apart from geodynamics, climatic variability has also impacted since the Eocene, invertebrate studies (Ortiz- Sepulveda et al., 2020; terrestrial and aquatic biodiversity patterns profoundly (e.g. Lyons Schultheiß et al., 2014) are usually not at a fully continental scale, or et al., 2015). Aquatic ecosystems might have been particularly im- not framed in an explicit biogeographical context (Jørgensen et al. pacted by Plio- Pleistocene climatic shifts (deMenocal, 2004), which 2008). Taxa endemic
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