{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,31]],"date-time":"2026-08-31T21:23:34Z","timestamp":1788211414065,"version":"build-2803163510"},"reference-count":85,"publisher":"National Academy of Sciences","issue":"32","license":[{"start":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T00:00:00Z","timestamp":1786060800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001655","name":"Deutscher Akademischer Austauschdienst","doi-asserted-by":"publisher","award":["57507871"],"award-info":[{"award-number":["57507871"]}],"id":[{"id":"10.13039\/501100001655","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Landesgraduierten F\u00f6rderung of the State of Baden W\u00fcrttemberg","award":["Stephan Lohmar"],"award-info":[{"award-number":["Stephan Lohmar"]}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["NE 969\/8-1 503320462"],"award-info":[{"award-number":["NE 969\/8-1 503320462"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["KO1895\/28-1 493354423"],"award-info":[{"award-number":["KO1895\/28-1 493354423"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2026,8,11]]},"abstract":"<jats:p>The evolution of life is characterized by major transitions, i.e., the evolution of new targets of selection (e.g., prokaryotes, eukaryotes, multicellular organisms, social insect colonies). They arose when preexisting lower-level units cooperated and gave up the capability to reproduce so that reproductive success is now achieved at the new, joint, higher unit. Currently, increasing confusion exists about major transition in evolution (MTE) that hampers progress in this fundamental research field. Misconceptions partly arose due to inadequate evolutionary reasoning. In addition, pivotal recent work shows considerable diversity in organismality in metazoan and social insect systems that makes clear-cut distinctions of transitions more difficult and that challenges our classical understanding of MTEs. Applying evolutionary reasoning, we develop three categories that all metazoan and social insect systems can be grouped into. The categories are defined by the reproductive potential of altruistic level units and how they can realize it (i.e., via independent reproduction as dispersing propagules or only through reproduction within the higher-level unit). These categories capture the variation in diversity in organismality that is crucial when analyzing potential major transitions, but that was always hard to grasp. This unifying conceptual framework advances our understanding of MTEs. It will enable comparative analyses within as well as across MTEs, to answer fundamental questions about the evolution of life.<\/jats:p>","DOI":"10.1073\/pnas.2530125123","type":"journal-article","created":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T17:46:06Z","timestamp":1786124766000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":1,"title":["A unifying framework for the evolution of metazoa and social insects, two major evolutionary transitions"],"prefix":"10.1073","volume":"123","author":[{"ORCID":"https:\/\/orcid.org\/0009-0001-5590-8353","authenticated-orcid":false,"given":"Stephan","family":"Lohmar","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0245cg223","id-type":"ROR","asserted-by":"publisher"}],"name":"Evolutionary Biology and Ecology, University of Freiburg","place":["Freiburg, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-9251-5077","authenticated-orcid":false,"given":"Julius","family":"Rombach","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0245cg223","id-type":"ROR","asserted-by":"publisher"}],"name":"Evolutionary Biology and Ecology, University of Freiburg","place":["Freiburg, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2059-3531","authenticated-orcid":false,"given":"Louis Allan","family":"Okwaro","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0245cg223","id-type":"ROR","asserted-by":"publisher"}],"name":"Evolutionary Biology and Ecology, University of Freiburg","place":["Freiburg, Germany"]},{"id":[{"id":"https:\/\/ror.org\/02crff812","id-type":"ROR","asserted-by":"publisher"}],"name":"National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse and Medical Faculty, University of Z\u00fcrich","place":["Z\u00fcrich, Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-6446-6982","authenticated-orcid":false,"given":"Wei","family":"Zhou","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0245cg223","id-type":"ROR","asserted-by":"publisher"}],"name":"Evolutionary Biology and Ecology, University of Freiburg","place":["Freiburg, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0494-1428","authenticated-orcid":false,"given":"Volker","family":"Nehring","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0245cg223","id-type":"ROR","asserted-by":"publisher"}],"name":"Evolutionary Biology and Ecology, University of Freiburg","place":["Freiburg, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9577-9376","authenticated-orcid":false,"given":"Judith","family":"Korb","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0245cg223","id-type":"ROR","asserted-by":"publisher"}],"name":"Evolutionary Biology and Ecology, University of Freiburg","place":["Freiburg, Germany"]},{"id":[{"id":"https:\/\/ror.org\/048zcaj52","id-type":"ROR","asserted-by":"publisher"}],"name":"Research Institute for the Environment and Livelihoods, Charles Darwin University","place":["Darwin, Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2026,8,7]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"publisher","DOI":"10.1038\/374227a0"},{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1093\/oso\/9780198502944.001.0001"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature21031"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-ecolsys-110411-160320"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2000.0727"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2120457119"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1093\/oso\/9780198746171.001.0001"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-018-0575-6"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1017\/CBO9780511721953"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-540-75957-7_7"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","DOI":"10.3389\/fevo.2021.732907"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.coisb.2023.100486"},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1420-9101.2008.01681.x"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1093\/jeb\/voaf141"},{"key":"e_1_3_4_15_2","first-page":"149","volume-title":"The Social Biology of Wasps","author":"Gadagkar R.","year":"1991","unstructured":"R. Gadagkar, \u201cBelonogaster, Mischocyttarus, Parapolybia, and independent-founding Ropalidia\u201d in The Social Biology of Wasps, K. G. Ross, R. W. Matthews, Eds. (Cornell University Press, 1991), pp. 149\u2013190."},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-540-75957-7"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2011.2639"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1017\/9781107338319.003"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1017\/9781107338319.005"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","DOI":"10.1093\/acprof:oso\/9780199231157.001.0001"},{"key":"e_1_3_4_21_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-ento-010715-023711"},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2009.0101"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12330"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.3389\/fevo.2022.1109484"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.3389\/fevo.2016.00006"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8312.1991.tb00612.x"},{"key":"e_1_3_4_27_2","first-page":"720","article-title":"South African \u201cfertile-worker bees\u201d","volume":"3","author":"Onions G. W.","year":"1912","unstructured":"G. W. Onions, South African \u201cfertile-worker bees\u201d. Agric. J. Union South Afr. 3, 720\u2013728 (1912).","journal-title":"Agric. J. Union South Afr."},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.1038\/415163a"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00040-008-1023-4"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1111\/evo.14513"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00265-010-1131-9"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1086\/415930"},{"key":"e_1_3_4_33_2","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-417156-5.00003-4"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1017\/9781107338319.006"},{"key":"e_1_3_4_35_2","first-page":"133","article-title":"\u201cSocial organisation and the status of workers in termites\u201d","author":"Roisin Y.","year":"2011","unstructured":"Y. Roisin, J. Korb, \u201cSocial organisation and the status of workers in termites\u201d in Biology of Termites: A Modern Synthesis, D. E. Bignell, Y. Roisin, N. Lo, Eds. (Springer, Netherlands, 2011), pp. 133\u2013164.","journal-title":"Biology of Termites: A Modern Synthesis"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00427-012-0417-5"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1387\/ijdb.180016nf"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.1038\/35050087"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ecolsys.38.091206.095740"},{"key":"e_1_3_4_40_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2008.00150.x"},{"key":"e_1_3_4_41_2","doi-asserted-by":"publisher","DOI":"10.1017\/CBO9780511781360.027"},{"key":"e_1_3_4_42_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-018-0533-3"},{"key":"e_1_3_4_43_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2017.10.010"},{"key":"e_1_3_4_44_2","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a040725"},{"key":"e_1_3_4_45_2","doi-asserted-by":"publisher","DOI":"10.1201\/b21831-4"},{"key":"e_1_3_4_46_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0609708104"},{"key":"e_1_3_4_47_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2023.2466"},{"key":"e_1_3_4_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.gde.2016.07.010"},{"key":"e_1_3_4_49_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro2242"},{"key":"e_1_3_4_50_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2013.05.004"},{"key":"e_1_3_4_51_2","doi-asserted-by":"publisher","DOI":"10.5962\/bhl.title.101564"},{"key":"e_1_3_4_52_2","volume-title":"Ants: Their Structure, Development and Behavior","author":"Wheeler W. M.","year":"1910","unstructured":"W. M. Wheeler, Ants: Their Structure, Development and Behavior (Columbia University Press, 1910)."},{"key":"e_1_3_4_53_2","doi-asserted-by":"publisher","DOI":"10.1186\/2041-9139-4-2"},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1111\/dgd.12211"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2023.1420"},{"key":"e_1_3_4_56_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cois.2025.101401"},{"key":"e_1_3_4_57_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1065507"},{"key":"e_1_3_4_58_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02270971"},{"key":"e_1_3_4_59_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1992.0118"},{"key":"e_1_3_4_60_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jtbi.2012.04.004"},{"key":"e_1_3_4_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/0022-5193(64)90038-4"},{"key":"e_1_3_4_62_2","doi-asserted-by":"publisher","DOI":"10.1016\/0022-5193(64)90039-6"},{"key":"e_1_3_4_63_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro1461"},{"key":"e_1_3_4_64_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ento.51.110104.151003"},{"key":"e_1_3_4_65_2","doi-asserted-by":"publisher","DOI":"10.1111\/brv.70107"},{"key":"e_1_3_4_66_2","doi-asserted-by":"publisher","DOI":"10.1163\/156853988X00340"},{"key":"e_1_3_4_67_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.3003290"},{"key":"e_1_3_4_68_2","doi-asserted-by":"publisher","DOI":"10.1111\/jeb.12566"},{"key":"e_1_3_4_69_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.es.05.110174.001545"},{"key":"e_1_3_4_70_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1156108"},{"key":"e_1_3_4_71_2","doi-asserted-by":"publisher","DOI":"10.1111\/mec.16185"},{"key":"e_1_3_4_72_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cois.2025.101388"},{"key":"e_1_3_4_73_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0014-3820.2002.tb00850.x"},{"key":"e_1_3_4_74_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10682-006-9153-5"},{"key":"e_1_3_4_75_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0907961106"},{"key":"e_1_3_4_76_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1420-9101.2012.02617.x"},{"key":"e_1_3_4_77_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00265-013-1569-7"},{"key":"e_1_3_4_78_2","doi-asserted-by":"publisher","DOI":"10.1111\/mec.12302"},{"key":"e_1_3_4_79_2","first-page":"325","article-title":"Termite polygyny: The ecological dynamics of queen mutualism","volume":"31","author":"Thorne B. L.","year":"1985","unstructured":"B. L. Thorne, Termite polygyny: The ecological dynamics of queen mutualism. Fortschr. Zool. 31, 325\u2013341 (1985).","journal-title":"Fortschr. Zool."},{"key":"e_1_3_4_80_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-294X.2003.2065.x"},{"key":"e_1_3_4_81_2","doi-asserted-by":"publisher","DOI":"10.1111\/mec.12233"},{"key":"e_1_3_4_82_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0701285104"},{"key":"e_1_3_4_83_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2009.0095"},{"key":"e_1_3_4_84_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-540-75957-7_12"},{"key":"e_1_3_4_85_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1050220206"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2530125123","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T17:46:08Z","timestamp":1786124768000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2530125123"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,7]]},"references-count":85,"journal-issue":{"issue":"32","published-print":{"date-parts":[[2026,8,11]]}},"alternative-id":["10.1073\/pnas.2530125123"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2530125123","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,7]]},"assertion":[{"value":"2026-08-07","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2530125123"}}