{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,13]],"date-time":"2026-06-13T20:16:59Z","timestamp":1781381819349,"version":"3.54.1"},"reference-count":90,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2023,11,2]],"date-time":"2023-11-02T00:00:00Z","timestamp":1698883200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010665","name":"H2020 Marie Sk\u0142odowska-Curie Actions","doi-asserted-by":"publisher","award":["641456"],"award-info":[{"award-number":["641456"]}],"id":[{"id":"10.13039\/100010665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Recurrent polyploidization occurred in the evolutionary history of most Eukaryota. However, how neopolyploid detriment (sterility, gigantism, gene dosage imbalances) has been overcome and even been bridged to evolutionary advantage (gene network diversification, mass radiation, range expansion) is largely unknown, particularly for animals. We used the parasitoid wasp <jats:italic>Nasonia vitripennis<\/jats:italic>, a rare insect system with heritable polyploidy, to begin addressing this knowledge gap. In Hymenoptera the sexes have different ploidies (haploid males, diploid females) and neopolyploids (diploid males, triploid females) occur for various species. Although such polyploids are usually sterile, those of <jats:italic>N<\/jats:italic>. <jats:italic>vitripennis<\/jats:italic> are reproductively capable and can even establish stable polyploid lines. To assess the effects of polyploidization, we compared a long-established polyploid line, the Whiting polyploid line (WPL) and a newly generated <jats:italic>transformer<\/jats:italic> knockdown line (tKDL) for fitness traits, absolute gene expression, and cell size and number. WPL polyploids have high male fitness and low female fecundity, while tKDL polyploids have poor male mate competition ability and high fertility. WPL has larger cells and cell number reduction, but the tKDL does not differ in this respect. Expression analyses of two housekeeping genes indicated that gene dosage is linked to sex irrespective of ploidy. Our study suggests that polyploid phenotypic variation may explain why some polyploid lineages thrive and others die out; a commonly proposed but difficult-to-test hypothesis. This documentation of diploid males (tKDL) with impaired competitive mating ability; triploid females with high fitness variation; and hymenopteran sexual dosage compensation (despite the lack of sex chromosomes) all challenges general assumptions on hymenopteran biology. We conclude that polyploidization is dependent on the duplicated genome characteristics and that genomes of different lines are unequally suited to survive diploidization. These results demonstrate the utility of <jats:italic>N<\/jats:italic>. <jats:italic>vitripennis<\/jats:italic> for delineating mechanisms of animal polyploid evolution, analogous to more advanced polyploid plant models.<\/jats:p>","DOI":"10.1371\/journal.pone.0288278","type":"journal-article","created":{"date-parts":[[2023,11,2]],"date-time":"2023-11-02T17:51:19Z","timestamp":1698947479000},"page":"e0288278","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":6,"title":["Effects of polyploidization and their evolutionary implications are revealed by heritable polyploidy in the haplodiploid wasp Nasonia vitripennis"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1392-6203","authenticated-orcid":true,"given":"Kelley","family":"Leung","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Louis","family":"van de Zande","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leo W.","family":"Beukeboom","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,11,2]]},"reference":[{"key":"pone.0288278.ref001","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/S1369-5266(00)00118-7","article-title":"Plant cell-size control: growing by ploidy?","volume":"3","author":"E Kondorosi","year":"2000","journal-title":"Curr Opin Plant Biol"},{"key":"pone.0288278.ref002","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1159\/000351998","article-title":"Polyploidy in animals: effects of gene expression on sex determination, evolution and ecology","volume":"140","author":"B Wertheim","year":"2013","journal-title":"Cytogenet Genome Res"},{"key":"pone.0288278.ref003","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1086\/285130","article-title":"\u201cWhy polyploidy is rarer in animals than in plants\u201d revisited.","volume":"136","author":"HA Orr","year":"1990","journal-title":"Am Nat"},{"key":"pone.0288278.ref004","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1086\/280047","article-title":"Why polyploidy is rarer in animals than in plants","volume":"59","author":"HJ Muller","year":"1925","journal-title":"Am Nat"},{"key":"pone.0288278.ref005","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1038\/nrg1711","article-title":"The advantages and disadvantages of being polyploid","volume":"6","author":"L. 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