Global distribution modelling of a conspicuous Gondwanian soil protist reveals latitudinal dispersal limitation and range contraction in response to climate warming

Author:

Bruni Estelle P.1ORCID,Rusconi Olivia1ORCID,Broennimann Olivier23ORCID,Adde Antoine3ORCID,Jauslin Raphaël4ORCID,Krashevska Valentyna5ORCID,Kosakyan Anush678ORCID,Armynot du Châtelet Eric9ORCID,Alcino João P. B.10ORCID,Beyens Louis11ORCID,Blandenier Quentin112ORCID,Bobrov Anatoly13ORCID,Burdman Luciana114ORCID,Duckert Clément1ORCID,Fernández Leonardo D.1516ORCID,Gomes e Souza Maria Beatriz10ORCID,Heger Thierry J.17ORCID,Koenig Isabelle118ORCID,Lahr Daniel J. G.10ORCID,McKeown Michelle1920ORCID,Meisterfeld Ralf21,Singer David1101722ORCID,Voelcker Eckhard23ORCID,Wilmshurst Janet19ORCID,Wohlhauser Sebastien24ORCID,Wilkinson David M.25,Guisan Antoine23ORCID,Mitchell Edward A. D.1ORCID

Affiliation:

1. Laboratory of Soil Biodiversity University of Neuchâtel Neuchâtel Switzerland

2. Department of Ecology and Evolution University of Lausanne Lausanne Switzerland

3. Institute of Earth Surface Dynamics University of Lausanne Lausanne Switzerland

4. Institute of Statistics University of Neuchâtel Neuchâtel Switzerland

5. J.‐F. Blumenbach Institute of Zoology and Anthropology University of Göttingen Göttingen Germany

6. Institute of Parasitology, Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

7. Department of Life Sciences University of Modena and Reggio Emilia Modena Italy

8. National Biodiversity Future Center (NBFC) Palermo Italy

9. Université de Lille, CNRS, Université du Littoral Côte d'Opale, UMR 8187 – LOG – Laboratoire d'Océanologie et de Géosciences Lille France

10. Department of Zoology, Institute of Biosciences University of São Paulo São Paulo Brazil

11. Department of Biology ECOSPHERE, University of Antwerp Antwerpen Belgium

12. Department of Biological Sciences Mississippi State University Mississippi State Mississippi USA

13. Faculty of Soil Science Lomonosov Moscow State University Moscow Russia

14. Center for Conservation and Sustainable Development Missouri Botanical Garden St. Louis Missouri USA

15. Centro de Investigación en Recursos Naturales y Sustentabilidad (CIRENYS) Universidad Bernardo O'Higgins Santiago Chile

16. Centro de Investigación de Estudios Avanzados del Maule Universidad Católica del Maule Talca Chile

17. Soil Science and Environment Group, Changins HES‐SO University of Applied Sciences and Arts Western Switzerland Nyon Switzerland

18. Unité d'Hygiène, Prévention et Contrôle de l'infection (HPCI), Service des Maladies Infectieuses Lausanne University Hospital – CHUV Lausanne Switzerland

19. Manaaki Whenua‐Landcare Research Long Term Ecology Laboratory Lincoln New Zealand

20. School of Biological, Earth and Environmental Sciences (BEES) University College Cork (UCC) Cork Ireland

21. Department of General Biology and General Zoology Institut für Biologie II Aachen Germany

22. UMR CNRS 6112 LPG‐BIAF Angers University Angers France

23. Penard Labs Cape Town South Africa

24. Association Vahatra Antananarivo Madagascar

25. Life and Environmental Sciences, Joseph Banks Laboratories University of Lincoln Lincoln UK

Abstract

AbstractAimThe diversity and distribution of soil microorganisms and their potential for long‐distance dispersal (LDD) are poorly documented, making the threats posed by climate change difficult to assess. If microorganisms do not disperse globally, regional endemism may develop and extinction may occur due to environmental changes. Here, we addressed this question using the testate amoeba Apodera vas, a morphologically conspicuous model soil microorganism in microbial biogeography, commonly found in peatlands and forests mainly of former Gondwana. We first documented its distribution. We next assessed whether its distribution could be explained by dispersal (i.e. matching its climatic niche) or vicariance (i.e. palaeogeography), based on the magnitude of potential range expansions or contractions in response to past and on‐going climatic changes. Last, we wanted to assess the likelihood of cryptic diversity and its potential threat from climate and land‐use changes (e.g. due to limited LDD).LocationDocumented records: Southern Hemisphere and intertropical zone; modelling: Global.MethodsWe first built an updated global distribution map of A. vas using 401 validated georeferenced records. We next used these data to develop a climatic niche model to predict its past (LGM, i.e. 21 ± 3 ka BP; PMIP3 IPSL‐CM5A‐LR), present and future (IPSL‐CMP6A‐LR predictions for 2071–2100, SSP3 and 5) potential distributions in responses to climate, by relating the species occurrences to climatic and topographic predictors. We then used these predictions to test our hypotheses (dispersal/vicariance, cryptic diversity, future threat from LDD limitation).ResultsOur models show that favourable climatic conditions for A. vas currently exist in the British Isles, an especially well‐studied region for testate amoebae where this species has never been found. This demonstrates a lack of interhemispheric LDD, congruent with the palaeogeography (vicariance) hypothesis. Longitudinal LDD is, however, confirmed by the presence of A. vas in isolated and geologically young peri‐Antarctic islands. Potential distribution maps for past, current and future climates show favourable climatic conditions existing on parts of all southern continents, with shifts to higher land from LGM to current in the tropics and a strong range contraction from current to future (global warming IPSL‐CM6A‐LR scenario for 2071–2100, SSP3.70 and SSP5.85) with favourable conditions developing on the Antarctic Peninsula.Main ConclusionsThis study illustrates the value of climate niche models for research on microbial diversity and biogeography, along with exploring the role played by historical factors and dispersal limitation in shaping microbial biogeography. We assess the discrepancy between latitudinal and longitudinal LDD for A. vas, which is possibly due to contrast in wind patterns and/or likelihood of transport by birds. Our models also suggest that climate change may lead to regional extinction of terrestrial microscopic organisms, thus illustrating the pertinence of including microorganisms in biodiversity conservation research and actions.

Funder

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Publisher

Wiley

Subject

Ecology, Evolution, Behavior and Systematics

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