Discovery of genetically distinct, sympatric coral lineages with temporal but not gametic reproductive isolation

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Abstract

Coral species abundance and biodiversity estimates are typically based on colony macromorphology. However, such measurements often underestimate the true diversity within coral communities because morphology does not necessarily reflect behavioral or genetic divergence. We previously reported on the unusual spawning behavior of the southern Caribbean population of the brain coral Diploria labyrinthiformis (Linnaeus, 1758), which spawns in both spring and autumn. Here, using data collected from 2013 to 2021, we show that the D. labyrinthiformis population in Curaçao is comprised of two behaviorally- and genetically distinct lineages, with 93% of colonies spawning exclusively in one season or the other. The two lineages could not be distinguished based on macromorphological differences or depth but represented clearly distinct genetic clusters (FST = 0.098) based on genome-wide sequencing. We tested for prezygotic and postzygotic gametic barriers between these two lineages by fertilizing eggs released in spring 2019 with sperm collected and cryopreserved in autumn 2018. Fertilization was successful and the resulting larvae developed normally, thus eliminating gametic incompatibility or early life postzygotic barriers as explanations for the divergence between these groups. Using observations from 19 other Caribbean localities, we confirmed the co-occurrence of discrete spring- and autumn-spawning populations in several locations across a range of latitudes. Thus, we show that seasonal, temporal reproductive isolation (allochrony), but not gametic reproductive isolation, is a strong barrier to gene flow in sympatric lineages of this critically endangered reef-building coral. More broadly, our findings underscore the role of allochrony as a mechanism capable of driving genetic divergence among cryptic, sympatric coral species.
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Discovery of genetically distinct, sympatric coral lineages with temporal but not gametic reproductive isolation | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL Molecular Ecology This is a preprint and has not been peer reviewed. Data may be preliminary. 7 April 2025 V1 Latest version Share on Discovery of genetically distinct, sympatric coral lineages with temporal but not gametic reproductive isolation Authors : Valérie Chamberland 0000-0002-1211-6575 [email protected] , Matias Gómez-Corrales 0000-0002-8604-1553 , Kristen Marhaver , Pim Bongaerts , Kelly Latijnhouwers , Diana Vergara-Flórez , Skylar Snowden , Juan Sánchez 0000-0001-7149-8369 , and Mark Vermeij Authors Info & Affiliations https://doi.org/10.22541/au.174405291.13722277/v1 Published Molecular Ecology Version of record Peer review timeline 624 views 224 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract Coral species abundance and biodiversity estimates are typically based on colony macromorphology. However, such measurements often underestimate the true diversity within coral communities because morphology does not necessarily reflect behavioral or genetic divergence. We previously reported on the unusual spawning behavior of the southern Caribbean population of the brain coral Diploria labyrinthiformis (Linnaeus, 1758), which spawns in both spring and autumn. Here, using data collected from 2013 to 2021, we show that the D. labyrinthiformis population in Curaçao is comprised of two behaviorally- and genetically distinct lineages, with 93% of colonies spawning exclusively in one season or the other. The two lineages could not be distinguished based on macromorphological differences or depth but represented clearly distinct genetic clusters (FST = 0.098) based on genome-wide sequencing. We tested for prezygotic and postzygotic gametic barriers between these two lineages by fertilizing eggs released in spring 2019 with sperm collected and cryopreserved in autumn 2018. Fertilization was successful and the resulting larvae developed normally, thus eliminating gametic incompatibility or early life postzygotic barriers as explanations for the divergence between these groups. Using observations from 19 other Caribbean localities, we confirmed the co-occurrence of discrete spring- and autumn-spawning populations in several locations across a range of latitudes. Thus, we show that seasonal, temporal reproductive isolation (allochrony), but not gametic reproductive isolation, is a strong barrier to gene flow in sympatric lineages of this critically endangered reef-building coral. More broadly, our findings underscore the role of allochrony as a mechanism capable of driving genetic divergence among cryptic, sympatric coral species. Supplementary Material File (chamberland et al 2025 dlab reproductive isolation_manuscript.docx) Download 8.85 MB Information & Authors Information Version history V1 Version 1 07 April 2025 Peer review timeline Published Molecular Ecology Version of Record 13 Oct 2025 Published Copyright This work is licensed under a Non Exclusive No Reuse License. Collection Molecular Ecology Keywords coral spawning cryptic species diploria labyrinthiformis prezygotic and postzygotic barriers seasonal allochrony sympatric speciation Authors Affiliations Valérie Chamberland 0000-0002-1211-6575 [email protected] SECORE International View all articles by this author Matias Gómez-Corrales 0000-0002-8604-1553 Nova Southeastern University View all articles by this author Kristen Marhaver CARMABI Foundation View all articles by this author Pim Bongaerts The University of Queensland School of Biological Sciences View all articles by this author Kelly Latijnhouwers SECORE International View all articles by this author Diana Vergara-Flórez Universidad de los Andes Facultad de Ciencias View all articles by this author Skylar Snowden Virginia Aquarium and Marine Science Center View all articles by this author Juan Sánchez 0000-0001-7149-8369 Universidad de los Andes Facultad de Ciencias View all articles by this author Mark Vermeij CARMABI Foundation View all articles by this author Metrics & Citations Metrics Article Usage 624 views 224 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Valérie Chamberland, Matias Gómez-Corrales, Kristen Marhaver, et al. Discovery of genetically distinct, sympatric coral lineages with temporal but not gametic reproductive isolation. Authorea . 07 April 2025. DOI: https://doi.org/10.22541/au.174405291.13722277/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu . Format Please select one from the list RIS (ProCite, Reference Manager) EndNote BibTex Medlars RefWorks Direct import Tips for downloading citations document.getElementById('citMgrHelpLink').addEventListener('click', function() { popupHelp(this.href); return false; }); $(".js__slcInclude").on("change", function(e){ if ($(this).val() == 'refworks') $('#direct').prop("checked", false); $('#direct').prop("disabled", ($(this).val() == 'refworks')); }); Cited by Shelby E. Gantt, Carsten G. B. Grupstra, Hannah E. Aichelman, Aden Nagree, Ally Swank, Jeric Da-Anoy, Peter M. Buston, Sarah W. Davies, Sex ratios and gamete production vary across cryptic coral lineages and thermal environments, Coral Reefs, 45 , 2, (665-682), (2025). https://doi.org/10.1007/s00338-025-02786-8 Crossref Loading... View Options View options PDF View PDF Figures Tables Media Share Share Share article link Copy Link Copied! Copying failed. 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