Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

Jelmer W. Poelstra, Jordi Salmona, George P. Tiley, Dominik Schüßler, Marina B. Blanco, Jean B. Andriambeloson, Olivier Bouchez, C. Ryan Campbell, Paul D. Etter, Paul A. Hohenlohe, Kelsie E. Hunnicutt, Amaia Iribar, Eric A. Johnson, Peter M. Kappeler, Peter A. Larsen, Sophie Manzi, JosÉ M. Ralison, Blanchard Randrianambinina, Rodin M. Rasoloarison, David W. RasolofosonAmanda R. Stahlke, David W. Weisrock, Rachel C. Williams, LounÈs Chikhi, Edward E. Louis, Ute Radespiel, Anne D. Yoder

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported - a result that is particularly striking when using the genealogical discordance index (gdi). Nonsister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.

Original languageEnglish (US)
Pages (from-to)203-218
Number of pages16
JournalSystematic Biology
Volume70
Issue number2
DOIs
StatePublished - Feb 10 2021

Bibliographical note

Funding Information:
This work was funded by the Bauer Foundation and the Zempelin Foundation of the "Deutsches Stiftungszentrum" [T237/22985/2012/kg and T0214/32083/2018/sm to DS.], Duke Lemur Center/SAVA Conservation research funds to MBB, the School of Animal Biology at The University of Western Australia to AM, the Funda??o para a Ci?ncia e a Tecnologia, Portugal [PTDC/BIABEC/ 100176/2008, PTDC/BIA-BIC/4476/2012, and SFRH/BD/64875/2009], the Groupement de Recherche International (GDRI) Biodiversit? et d?veloppement durable-Madagascar, the Laboratoire d'Excellence (LABEX) TULIP (ANR-10-LABX-41) and CEBA (ANR- 10-LABX-25-01, the Instituto Gulbenkian de Ci?ncia, Portugal to LC and JS, the ERA-NET BiodivERsA project: INFRAGECO (Inference, Fragmentation, Genomics, and Conservation, ANR-16-EBI3-0014 & FCT-Biodiversa/0003/2015) the LIA BEEG-B (Laboratoire International Associ? - Bioinformatics, Ecology, Evolution, Genomics and Behaviour, CNRS) to L.C. and J.S. Further financial support came from the Institute of Zoology, University of Veterinary Medicine Hannover and UR acknowledges the longterm support of the late Elke Zimmermann for her research activities on Madagascar. The genomic data were generated with funds from NSF DEB-1354610 to ADY and DWW and from the EDB Lab to JS ADY also gratefully acknowledges support from the John Simon Guggenheim Memorial Foundation, the Alexander von Humboldt Foundation, and the Duke Tropical Conservation Initiative. EELJ would like to acknowledge support from the Ahmanson Foundation for the data generation. This work was performed in collaboration with the GeT core facility, Toulouse, France (http://get.genotoul.fr), and was supported by France G?nomique National infrastructure, funded as part of "Investissement d'avenir" program managed by Agence Nationale pour la Recherche (contract ANR-10-INBS- 09). J.S., U.R., and L.C. also gratefully acknowledge support from the Get-Plage sequencing and Genotoul bioinformatics (BioinfoGenotoul) platforms Toulouse Midi-Pyrenees. This is DLC publication #1459.

Publisher Copyright:
© 2020 The Author(s).

Keywords

  • Cryptic species
  • effective population size
  • microendemism
  • multispecies coalescent
  • speciation
  • species delimitation

PubMed: MeSH publication types

  • Journal Article

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