Ecology and morphology of mouse lemurs ( Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species Dominik Schüßler, Marina Blanco, Jordi Salmona, Jelmer Poelstra, Jean Andriambeloson, Alex Miller, Blanchard Randrianambinina, David Rasolofoson, Jasmin Mantilla-contreras, Lounès Chikhi, et al. To cite this version: Dominik Schüßler, Marina Blanco, Jordi Salmona, Jelmer Poelstra, Jean Andriambeloson, et al.. Ecology and morphology of mouse lemurs ( Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species. American Journal of Primatology, Wiley, 2020, 82 (9), pp.e23180. 10.1002/ajp.23180. hal-03026869 HAL Id: hal-03026869 https://hal.archives-ouvertes.fr/hal-03026869 Submitted on 5 Jan 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. American Journal of Primatology Ecology and morphology of mouse lemurs (Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species Journal: American Journal of Primatology Manuscript ID AJP-20-0048.R1 Wiley - Manuscript type:ForResearch Peer Article Review Date Submitted by the n/a Author: Complete List of Authors: Schüßler, Dominik; University of Hildesheim, Institute of Biology and Chemistry Blanco, Marina; Duke Lemur Center; Duke University, Department of Biology Salmona, Jordi; Laboratoire Evolution & Diversité Biologique, UMR 5174 CNRS – Université Paul Sabatier Poelstra, Jelmer; Duke University, Department of Biology Andriambeloson, Jean-Basile; University of Antananarivo, Department of Zoology and Animal Biodiversity Miller, Alex; Instituto Gulbenkian de Ciencia, Population and Conservation Genetics Group Randrianambinina, Blanchard; Groupe d’Etude et de Recherche sur les Primates de Madagascar (GERP); University of Mahajanga, Faculté des Sciences Rasolofoson, David; Groupe d’Etude et de Recherche sur les Primates de Madagascar (GERP) Mantilla-Contreras, Jasmin; University of Hildesheim, Institute of Biology and Chemistry Chikhi, Lounès; Instituto Gulbenkian de Ciênca, ; Laboratoire Evolution & Diversité Biologique, UMR 5174 CNRS – Université Paul Sabatier, Lewis, Edward; Omaha’s Henry Doorly Zoo and Aquarium, Grewcock Center for Conservation and Research Yoder, Anne; Duke University, Department of Biology Radespiel, Ute; University of Veterinary Medicine, Institute of Zoology Indicate which taxonomic group was the subject of your Prosimians study (select all that apply or type another option):: Keywords: evolution, cryptic species, phenotype, habitat use, sympatry John Wiley & Sons Page 1 of 66 American Journal of Primatology 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 For Peer Review 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 John Wiley & Sons American Journal of Primatology Page 2 of 66 Schüßler et al. page 1 1 2 3 4 5 1 Ecology and morphology of mouse lemurs (Microcebus spp.) in 6 7 2 a hotspot of microendemism in northeastern Madagascar, with 8 9 10 3 the description of a new species 11 12 13 4 14 15 16 5 Authors: 17 18 19 6 Dominik Schüßler1#, Marina B. Blanco2,3#, Jordi Salmona4, Jelmer Poelstra3, 20 21 7 Jean B. AndriambelosonFor5, Alex Peer Miller6, BlanchardReview Randrianambinina7,8, David 22 23 7 1 4,6 24 8 W. Rasolofoson , Jasmin Mantilla-Contreras , Lounès Chikhi , Edward E. 25 26 9 Louis Jr.9, Anne D. Yoder3, Ute Radespiel10* 27 28 29 10 30 31 32 11 Affiliations: 33 34 35 12 1: Research Group Ecology and Environmental Education, Institute of Biology 36 37 13 and Chemistry, University of Hildesheim, Universitaetsplatz 1, 31141 38 39 14 Hildesheim, Germany 40 41 42 15 2: Duke Lemur Center, Duke University, Durham, NC 27705, USA 43 44 45 16 3: Department of Biology, Duke University, Durham, NC 27708, USA 46 47 48 17 4: CNRS, Université Paul Sabatier, IRD, UMR5174 EDB (Laboratoire Évolution 49 50 51 18 & Diversité 11 Biologique), 118 route de Narbonne, 31062 Toulouse, France 52 53 5 54 19 : Zoology and Animal Biodiversity, University of Antananarivo, Antananarivo 55 56 20 101, Madagascar 57 58 59 60 John Wiley & Sons Page 3 of 66 American Journal of Primatology Schüßler et al. page 2 1 2 3 4 21 6: Instituto Gulbenkian de Ciência, Rua da Quinta Grande, 6, 2780-156 Oeiras, 5 6 7 22 Portugal 8 9 7 10 23 : Groupe d’Etude et de Recherche sur les Primates de Madagascar (GERP), 11 12 24 BP 779, Antananarivo 101, Madagascar 13 14 15 25 8: Faculté des Sciences, University of Mahajanga, Mahajanga, Madagascar 16 17 18 26 9: Grewcock Center for Conservation and Research, Omaha’s Henry Doorly 19 20 27 Zoo and Aquarium, Omaha, NE 21 For Peer Review 22 23 28 10: Institute of Zoology, University of Veterinary Medicine Hannover, Buenteweg 24 25 29 17, 30559 Hannover, Germany 26 27 28 30 29 30 31 31 32 32 Short title: 33 34 35 33 A new species of mouse lemur 36 37 38 34 39 40 41 35 42 43 44 36 Corresponding author: 45 46 47 37 *Ute Radespiel, Institute of Zoology, University of Veterinary Medicine 48 49 Hannover, Buenteweg 17, 30559 Hannover, Germany; email: 50 38 51 52 39 [email protected] 53 54 55 40 56 57 58 41 #: should be considered as shared first authors 59 60 John Wiley & Sons American Journal of Primatology Page 4 of 66 Schüßler et al. page 3 1 2 3 4 42 Abstract 5 6 7 43 Delimitation of cryptic species is increasingly based on genetic analyses but the 8 9 10 44 integration of distributional, morphological, behavioral and ecological data offers 11 12 45 unique complementary insights into species diversification. We surveyed 13 14 46 communities of nocturnal mouse lemurs (Microcebus spp.) in five different sites 15 16 17 47 of northeastern Madagascar, measuring a variety of morphological parameters 18 19 48 and assessing reproductive states for 123 individuals belonging to five different 20 21 49 lineages. We documentedFor two Peer different Reviewnon-sister lineages occurring in 22 23 50 sympatry in two areas. In both cases, sympatric species pairs consisted of a 24 25 26 51 locally restricted (M. macarthurii or M. sp. #3) and a more widespread lineage 27 28 52 (M. mittermeieri or M. lehilahytsara). Estimated Extents of Occurrence (EOO) of 29 30 53 these lineages differed remarkably with 560 and 1,500 km² versus 9,250 and 31 32 33 54 50,700 km², respectively. Morphometric analyses distinguished unambiguously 34 35 55 between sympatric species and detected more subtle but significant differences 36 37 56 among sister lineages. Tail length and body size were most informative in this 38 39 40 57 regard. Reproductive schedules were highly variable among lineages, most 41 42 58 likely impacted by phylogenetic relatedness and environmental variables. While 43 44 59 sympatric species pairs differed in their reproductive timing (M. sp. #3 / M. 45 46 60 lehilahytsara and M. macarthurii / M. mittermeieri), warmer lowland rainforests 47 48 49 61 were associated with a less seasonal reproductive schedule for M. mittermeieri 50 51 62 and M. lehilahytsara compared to populations occurring in montane forests. 52 53 63 Distributional, morphological and ecological data gathered in this study support 54 55 56 64 the results of genomic species delimitation analyses conducted in a companion 57 58 65 study, which identified one lineage, M. sp. #3, as meriting formal description as 59 60 66 a new species. Consequently, a formal species description is included. John Wiley & Sons Page 5 of 66 American Journal of Primatology Schüßler et al. page 4 1 2 3 4 67 Worryingly, our data also show that geographically restricted populations of M. 5 6 7 68 sp. #3 and its sister species (M. macarthurii) are at high risk of local and 8 9 69 perhaps permanent extinction from both deforestation and habitat 10 11 70 fragmentation. 12 13 14 71 15 16 17 72 Research highlights 18 19 20 73 Two pairs of Microcebus species occur in partial sympatry 21 For Peer Review 22 23 74 Morphological distinctiveness supports genomic species delimitation in 24 25 75 cryptic lemurs 26 27 76 High plasticity in reproductive schedules in a lineage of habitat 28 29 30 77 generalists detected 31 32 33 78 34 35 36 79 Keywords: evolution, cryptic species, phenotype, habitat use, sympatry, 37 38 80 conservation 39 40 41 81 42 43 44 82 1. Introduction 45 46 47 83 Madagascar is one of the world’s prime biodiversity hotspots and its endemic 48 49 84 group of primates, the lemurs (Primates; Lemuriformes), are flagships for 50 51 85 species conservation (Myers, Mittermeier, Mittermeier, Da Fonseca & Kent, 52 53 54 86 2000). More than 100 species of lemurs are recognized today making up about 55 56 87 one fifth of all living primate species on earth (Estrada et al., 2017). However, 57 58 88 the full extent of lemur species diversity is not yet fully known as several regions 59 60 John Wiley & Sons American Journal of Primatology Page 6 of 66 Schüßler et al. page 5 1 2 3 4 89 in Madagascar are still poorly studied. Intensified biological inventories during 5 6 7 90 recent years have indeed resulted in a considerable rise in lemur species 8 9 91 numbers.