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
Hauptverfasser: 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
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container_end_page 72
container_issue 1
container_start_page 57
container_title Nature ecology & evolution
container_volume 9
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
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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. 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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. 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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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c390t-2250cdd80bbf545ade7f76736471c63c62e59bfc476a515c769a91661e3261583</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>631/181/2474</topic><topic>631/181/2480</topic><topic>631/208/457</topic><topic>631/601/18</topic><topic>Animals</topic><topic>Best practice</topic><topic>Biodiversity</topic><topic>Biological and Physical Anthropology</topic><topic>Biological Evolution</topic><topic>Biomedical and Life Sciences</topic><topic>Biota</topic><topic>Cheirogaleidae - anatomy &amp; histology</topic><topic>Cheirogaleidae - classification</topic><topic>Cheirogaleidae - genetics</topic><topic>Crypsis</topic><topic>Ecology</topic><topic>Endemic species</topic><topic>Evolutionary Biology</topic><topic>Evolutionary conservation</topic><topic>Genetic Speciation</topic><topic>Geographical variations</topic><topic>Life history</topic><topic>Life Sciences</topic><topic>Madagascar</topic><topic>Morphology</topic><topic>Paleontology</topic><topic>Phylogeny</topic><topic>Primates</topic><topic>Speciation</topic><topic>Species diversity</topic><topic>Species extinction</topic><topic>Systematics, Phylogenetics and taxonomy</topic><topic>Taxonomic revision</topic><topic>Taxonomy</topic><topic>Zoology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van Elst, Tobias</creatorcontrib><creatorcontrib>Sgarlata, Gabriele M.</creatorcontrib><creatorcontrib>Schüßler, Dominik</creatorcontrib><creatorcontrib>Tiley, George P.</creatorcontrib><creatorcontrib>Poelstra, Jelmer W.</creatorcontrib><creatorcontrib>Scheumann, Marina</creatorcontrib><creatorcontrib>Blanco, Marina B.</creatorcontrib><creatorcontrib>Aleixo-Pais, Isa G.</creatorcontrib><creatorcontrib>Rina Evasoa, Mamy</creatorcontrib><creatorcontrib>Ganzhorn, Jörg U.</creatorcontrib><creatorcontrib>Goodman, Steven M.</creatorcontrib><creatorcontrib>Hasiniaina, Alida F.</creatorcontrib><creatorcontrib>Hending, Daniel</creatorcontrib><creatorcontrib>Hohenlohe, Paul A.</creatorcontrib><creatorcontrib>Ibouroi, Mohamed T.</creatorcontrib><creatorcontrib>Iribar, Amaia</creatorcontrib><creatorcontrib>Jan, Fabien</creatorcontrib><creatorcontrib>Kappeler, Peter M.</creatorcontrib><creatorcontrib>Le Pors, Barbara</creatorcontrib><creatorcontrib>Manzi, Sophie</creatorcontrib><creatorcontrib>Olivieri, Gillian</creatorcontrib><creatorcontrib>Rakotonanahary, Ando N.</creatorcontrib><creatorcontrib>Rakotondranary, S. 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 &amp; 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 &amp; 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>
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issn 2397-334X
2397-334X
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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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