{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T18:33:02Z","timestamp":1787164382893,"version":"build-2736575974"},"reference-count":92,"publisher":"Oxford University Press (OUP)","issue":"11","license":[{"start":{"date-parts":[[2020,6,10]],"date-time":"2020-06-10T00:00:00Z","timestamp":1591747200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"Genomics of Species Diversification"},{"name":"ERC-CoG PANDA"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,11,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>In standard models of molecular evolution, DNA sequences evolve through asynchronous substitutions according to Poisson processes with a constant rate (called the molecular clock) or a rate that can vary (relaxed clock). However, DNA sequences can also undergo episodes of fast divergence that will appear as synchronous substitutions affecting several sites simultaneously at the macroevolutionary timescale. Here, we develop a model, which we call the Relaxed Clock with Spikes model, combining basal, clock-like molecular substitutions with episodes of fast divergence called spikes arising at speciation events. Given a multiple sequence alignment and its time-calibrated species phylogeny, our model is able to detect speciation events (including hidden ones) cooccurring with spike events and to estimate the probability and amplitude of these spikes on the phylogeny. We identify the conditions under which spikes can be distinguished from the natural variance of the clock-like component of molecular substitutions and from variations of the clock. We apply the method to genes underlying snake venom proteins and identify several spikes at gene-specific locations in the phylogeny. This work should pave the way for analyses relying on whole genomes to inform on modes of species diversification.<\/jats:p>","DOI":"10.1093\/molbev\/msaa144","type":"journal-article","created":{"date-parts":[[2020,6,4]],"date-time":"2020-06-04T15:10:26Z","timestamp":1591283426000},"page":"3308-3323","source":"Crossref","is-referenced-by-count":25,"title":["Model-Based Inference of Punctuated Molecular Evolution"],"prefix":"10.1093","volume":"37","author":[{"given":"Marc","family":"Manceau","sequence":"first","affiliation":[{"name":"Center for Interdisciplinary Research in Biology (CIRB), Coll\u00e8ge de France, CNRS UMR 7241, INSERM U 1050, PSL Research University, Paris, France"},{"name":"IBENS, Ecole Normale Sup\u00e9rieure, UMR 8197 CNRS, Paris, France"},{"name":"DBSSE, ETH Z\u00fcrich, Basel, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julie","family":"Marin","sequence":"additional","affiliation":[{"name":"Center for Interdisciplinary Research in Biology (CIRB), Coll\u00e8ge de France, CNRS UMR 7241, INSERM U 1050, PSL Research University, Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H\u00e9l\u00e8ne","family":"Morlon","sequence":"additional","affiliation":[{"name":"IBENS, Ecole Normale Sup\u00e9rieure, UMR 8197 CNRS, Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amaury","family":"Lambert","sequence":"additional","affiliation":[{"name":"Center for Interdisciplinary Research in Biology (CIRB), Coll\u00e8ge de France, CNRS UMR 7241, INSERM U 1050, PSL Research University, Paris, France"},{"name":"Laboratoire de Probabilit\u00e9s, Statistique et Mod\u00e9lisation (LPSM), Sorbonne Universit\u00e9, CNRS UMR 8001, Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,6,10]]},"reference":[{"issue":"1","key":"2020112015462959100_msaa144-B1","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1093\/sysbio\/syv065","article-title":"Quantifying age-dependent extinction from species phylogenies","volume":"65","author":"Alexander","year":"2016","journal-title":"Syst Biol"},{"issue":"1","key":"2020112015462959100_msaa144-B2","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1146\/annurev.es.15.110184.001025","article-title":"Genetic revolutions, founder effects, and speciation","volume":"15","author":"Barton","year":"1984","journal-title":"Annu Rev Ecol Syst"},{"issue":"9","key":"2020112015462959100_msaa144-B3","doi-asserted-by":"crossref","first-page":"1964","DOI":"10.1093\/molbev\/msz125","article-title":"Many options, few solutions: over 60 million years snakes converged on a few optimal venom 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Trans R Soc Lond B Biol Sci"},{"issue":"11","key":"2020112015462959100_msaa144-B61","doi-asserted-by":"crossref","first-page":"7173","DOI":"10.1074\/jbc.272.11.7173","article-title":"Localization of structural elements of bee venom phospholipase A2 involved in N-type receptor binding and neurotoxicity","volume":"272","author":"Nicolas","year":"1997","journal-title":"J Biol Chem"},{"issue":"1","key":"2020112015462959100_msaa144-B62","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1146\/annurev.ecolsys.28.1.195","article-title":"Haldane\u2019s rule","volume":"28","author":"Orr","year":"1997","journal-title":"Annu Rev Ecol Syst"},{"issue":"1","key":"2020112015462959100_msaa144-B63","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1534\/genetics.104.029231","article-title":"Inferring the mode of speciation from genomic data: a study of the great 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