Integrative taxonomy clarifies the evolution of a cryptic primate clade
Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for c...
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Veröffentlicht in: | Nature ecology & evolution 2025-01, Vol.9 (1), p.57-72 |
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creator | van Elst, Tobias Sgarlata, Gabriele M. Schüßler, Dominik Tiley, George P. Poelstra, Jelmer W. Scheumann, Marina Blanco, Marina B. Aleixo-Pais, Isa G. Rina Evasoa, Mamy Ganzhorn, Jörg U. Goodman, Steven M. Hasiniaina, Alida F. Hending, Daniel Hohenlohe, Paul A. Ibouroi, Mohamed T. Iribar, Amaia Jan, Fabien Kappeler, Peter M. Le Pors, Barbara Manzi, Sophie Olivieri, Gillian Rakotonanahary, Ando N. Rakotondranary, S. Jacques Rakotondravony, Romule Ralison, José M. Ranaivoarisoa, J. Freddy Randrianambinina, Blanchard Rasoloarison, Rodin M. Rasoloharijaona, Solofonirina Rasolondraibe, Emmanuel Teixeira, Helena Zaonarivelo, John R. Louis, Edward E. Yoder, Anne D. Chikhi, Lounès Radespiel, Ute Salmona, Jordi |
description | Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus
Microcebus
, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework.
A spatial taxonomic framework integrating genomic, morphological, ecological, life history and acoustic data is used to clarify the cryptic evolution of the taxonomically controversial mouse lemur complex, with a view to aiding future conservation of this and other similarly cryptic clades. |
doi_str_mv | 10.1038/s41559-024-02547-w |
format | Article |
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Microcebus
, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework.
A spatial taxonomic framework integrating genomic, morphological, ecological, life history and acoustic data is used to clarify the cryptic evolution of the taxonomically controversial mouse lemur complex, with a view to aiding future conservation of this and other similarly cryptic clades.</description><identifier>ISSN: 2397-334X</identifier><identifier>EISSN: 2397-334X</identifier><identifier>DOI: 10.1038/s41559-024-02547-w</identifier><identifier>PMID: 39333396</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/181/2474 ; 631/181/2480 ; 631/208/457 ; 631/601/18 ; Animals ; Best practice ; Biodiversity ; Biological and Physical Anthropology ; Biological Evolution ; Biomedical and Life Sciences ; Biota ; Cheirogaleidae - anatomy & histology ; Cheirogaleidae - classification ; Cheirogaleidae - genetics ; Crypsis ; Ecology ; Endemic species ; Evolutionary Biology ; Evolutionary conservation ; Genetic Speciation ; Geographical variations ; Life history ; Life Sciences ; Madagascar ; Morphology ; Paleontology ; Phylogeny ; Primates ; Speciation ; Species diversity ; Species extinction ; Systematics, Phylogenetics and taxonomy ; Taxonomic revision ; Taxonomy ; Zoology</subject><ispartof>Nature ecology & evolution, 2025-01, Vol.9 (1), p.57-72</ispartof><rights>The Author(s) 2024</rights><rights>2024. 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Freddy</creatorcontrib><creatorcontrib>Randrianambinina, Blanchard</creatorcontrib><creatorcontrib>Rasoloarison, Rodin M.</creatorcontrib><creatorcontrib>Rasoloharijaona, Solofonirina</creatorcontrib><creatorcontrib>Rasolondraibe, Emmanuel</creatorcontrib><creatorcontrib>Teixeira, Helena</creatorcontrib><creatorcontrib>Zaonarivelo, John R.</creatorcontrib><creatorcontrib>Louis, Edward E.</creatorcontrib><creatorcontrib>Yoder, Anne D.</creatorcontrib><creatorcontrib>Chikhi, Lounès</creatorcontrib><creatorcontrib>Radespiel, Ute</creatorcontrib><creatorcontrib>Salmona, Jordi</creatorcontrib><title>Integrative taxonomy clarifies the evolution of a cryptic primate clade</title><title>Nature ecology & evolution</title><addtitle>Nat Ecol Evol</addtitle><addtitle>Nat Ecol Evol</addtitle><description>Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus
Microcebus
, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework.
A spatial taxonomic framework integrating genomic, morphological, ecological, life history and acoustic data is used to clarify the cryptic evolution of the taxonomically controversial mouse lemur complex, with a view to aiding future conservation of this and other similarly cryptic clades.</description><subject>631/181/2474</subject><subject>631/181/2480</subject><subject>631/208/457</subject><subject>631/601/18</subject><subject>Animals</subject><subject>Best practice</subject><subject>Biodiversity</subject><subject>Biological and Physical Anthropology</subject><subject>Biological Evolution</subject><subject>Biomedical and Life Sciences</subject><subject>Biota</subject><subject>Cheirogaleidae - anatomy & histology</subject><subject>Cheirogaleidae - classification</subject><subject>Cheirogaleidae - genetics</subject><subject>Crypsis</subject><subject>Ecology</subject><subject>Endemic species</subject><subject>Evolutionary Biology</subject><subject>Evolutionary conservation</subject><subject>Genetic Speciation</subject><subject>Geographical variations</subject><subject>Life history</subject><subject>Life Sciences</subject><subject>Madagascar</subject><subject>Morphology</subject><subject>Paleontology</subject><subject>Phylogeny</subject><subject>Primates</subject><subject>Speciation</subject><subject>Species diversity</subject><subject>Species extinction</subject><subject>Systematics, Phylogenetics and taxonomy</subject><subject>Taxonomic revision</subject><subject>Taxonomy</subject><subject>Zoology</subject><issn>2397-334X</issn><issn>2397-334X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNp9kc1uEzEUhS0EolXpC7BAI7GBxRRf_8YrVFXQVorEBiR2luPcSVxNxsH2pOTtcTqlLV1gybJlf-fcax9C3gI9A8pnn7IAKU1LmahTCt3eviDHjBvdci5-vnyyPyKnOd9QSkFraZR6TY644XUYdUwur4eCq-RK2GFT3O84xM2-8b1LoQuYm7LGBnexH0uIQxO7xjU-7bcl-GabwsYVPMBLfENeda7PeHq_npAfX798v7hq598ury_O563nhpaWMUn9cjmji0UnhaxC3WmluRIavOJeMZRm0XmhlZMgvVbGGVAKkDMFcsZPyOfJdzsuNrj0OJTkenvXS9rb6IL992YIa7uKOwugmRKKV4ePk8P6me7qfG4PZ7QW12DUDir74b5air9GzMVuQvbY927AOGbLAahmRoCu6Ptn6E0c01D_olKSGyNBHIqzifIp5pywe-gAqD3kaqdcbc3V3uVqb6vo3dM3P0j-plgBPgG5Xg0rTI-1_2P7B95jrZg</recordid><startdate>20250101</startdate><enddate>20250101</enddate><creator>van Elst, Tobias</creator><creator>Sgarlata, Gabriele M.</creator><creator>Schüßler, Dominik</creator><creator>Tiley, George P.</creator><creator>Poelstra, Jelmer W.</creator><creator>Scheumann, Marina</creator><creator>Blanco, Marina B.</creator><creator>Aleixo-Pais, Isa G.</creator><creator>Rina Evasoa, Mamy</creator><creator>Ganzhorn, Jörg U.</creator><creator>Goodman, Steven M.</creator><creator>Hasiniaina, Alida F.</creator><creator>Hending, Daniel</creator><creator>Hohenlohe, Paul A.</creator><creator>Ibouroi, Mohamed T.</creator><creator>Iribar, Amaia</creator><creator>Jan, Fabien</creator><creator>Kappeler, Peter M.</creator><creator>Le Pors, Barbara</creator><creator>Manzi, Sophie</creator><creator>Olivieri, Gillian</creator><creator>Rakotonanahary, Ando N.</creator><creator>Rakotondranary, S. 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Jacques</creatorcontrib><creatorcontrib>Rakotondravony, Romule</creatorcontrib><creatorcontrib>Ralison, José M.</creatorcontrib><creatorcontrib>Ranaivoarisoa, J. Freddy</creatorcontrib><creatorcontrib>Randrianambinina, Blanchard</creatorcontrib><creatorcontrib>Rasoloarison, Rodin M.</creatorcontrib><creatorcontrib>Rasoloharijaona, Solofonirina</creatorcontrib><creatorcontrib>Rasolondraibe, Emmanuel</creatorcontrib><creatorcontrib>Teixeira, Helena</creatorcontrib><creatorcontrib>Zaonarivelo, John R.</creatorcontrib><creatorcontrib>Louis, Edward E.</creatorcontrib><creatorcontrib>Yoder, Anne D.</creatorcontrib><creatorcontrib>Chikhi, Lounès</creatorcontrib><creatorcontrib>Radespiel, Ute</creatorcontrib><creatorcontrib>Salmona, Jordi</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature ecology & evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>van Elst, Tobias</au><au>Sgarlata, Gabriele M.</au><au>Schüßler, Dominik</au><au>Tiley, George P.</au><au>Poelstra, Jelmer W.</au><au>Scheumann, Marina</au><au>Blanco, Marina B.</au><au>Aleixo-Pais, Isa G.</au><au>Rina Evasoa, Mamy</au><au>Ganzhorn, Jörg U.</au><au>Goodman, Steven M.</au><au>Hasiniaina, Alida F.</au><au>Hending, Daniel</au><au>Hohenlohe, Paul A.</au><au>Ibouroi, Mohamed T.</au><au>Iribar, Amaia</au><au>Jan, Fabien</au><au>Kappeler, Peter M.</au><au>Le Pors, Barbara</au><au>Manzi, Sophie</au><au>Olivieri, Gillian</au><au>Rakotonanahary, Ando N.</au><au>Rakotondranary, S. Jacques</au><au>Rakotondravony, Romule</au><au>Ralison, José M.</au><au>Ranaivoarisoa, J. Freddy</au><au>Randrianambinina, Blanchard</au><au>Rasoloarison, Rodin M.</au><au>Rasoloharijaona, Solofonirina</au><au>Rasolondraibe, Emmanuel</au><au>Teixeira, Helena</au><au>Zaonarivelo, John R.</au><au>Louis, Edward E.</au><au>Yoder, Anne D.</au><au>Chikhi, Lounès</au><au>Radespiel, Ute</au><au>Salmona, Jordi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Integrative taxonomy clarifies the evolution of a cryptic primate clade</atitle><jtitle>Nature ecology & evolution</jtitle><stitle>Nat Ecol Evol</stitle><addtitle>Nat Ecol Evol</addtitle><date>2025-01-01</date><risdate>2025</risdate><volume>9</volume><issue>1</issue><spage>57</spage><epage>72</epage><pages>57-72</pages><issn>2397-334X</issn><eissn>2397-334X</eissn><abstract>Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus
Microcebus
, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework.
A spatial taxonomic framework integrating genomic, morphological, ecological, life history and acoustic data is used to clarify the cryptic evolution of the taxonomically controversial mouse lemur complex, with a view to aiding future conservation of this and other similarly cryptic clades.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>39333396</pmid><doi>10.1038/s41559-024-02547-w</doi><tpages>16</tpages><orcidid>https://orcid.org/0009-0008-0716-8507</orcidid><orcidid>https://orcid.org/0000-0002-2601-6938</orcidid><orcidid>https://orcid.org/0000-0002-3514-7462</orcidid><orcidid>https://orcid.org/0000-0002-8779-1700</orcidid><orcidid>https://orcid.org/0000-0003-2934-6622</orcidid><orcidid>https://orcid.org/0000-0002-7616-0161</orcidid><orcidid>https://orcid.org/0000-0003-2730-3688</orcidid><orcidid>https://orcid.org/0000-0003-0053-0207</orcidid><orcidid>https://orcid.org/0009-0003-8538-7389</orcidid><orcidid>https://orcid.org/0000-0001-9032-4575</orcidid><orcidid>https://orcid.org/0000-0002-1950-5805</orcidid><orcidid>https://orcid.org/0000-0001-9318-0570</orcidid><orcidid>https://orcid.org/0000-0001-5885-7988</orcidid><orcidid>https://orcid.org/0000-0003-0609-4354</orcidid><orcidid>https://orcid.org/0000-0002-4091-9500</orcidid><orcidid>https://orcid.org/0000-0002-4801-487X</orcidid><orcidid>https://orcid.org/0000-0002-4115-6453</orcidid><orcidid>https://orcid.org/0000-0002-0814-2404</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 2397-334X |
ispartof | Nature ecology & evolution, 2025-01, Vol.9 (1), p.57-72 |
issn | 2397-334X 2397-334X |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11726463 |
source | MEDLINE; Nature; SpringerLink Journals - AutoHoldings |
subjects | 631/181/2474 631/181/2480 631/208/457 631/601/18 Animals Best practice Biodiversity Biological and Physical Anthropology Biological Evolution Biomedical and Life Sciences Biota Cheirogaleidae - anatomy & histology Cheirogaleidae - classification Cheirogaleidae - genetics Crypsis Ecology Endemic species Evolutionary Biology Evolutionary conservation Genetic Speciation Geographical variations Life history Life Sciences Madagascar Morphology Paleontology Phylogeny Primates Speciation Species diversity Species extinction Systematics, Phylogenetics and taxonomy Taxonomic revision Taxonomy Zoology |
title | Integrative taxonomy clarifies the evolution of a cryptic primate clade |
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