{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,4]],"date-time":"2026-05-04T03:13:22Z","timestamp":1777864402456,"version":"3.51.4"},"reference-count":38,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T00:00:00Z","timestamp":1777507200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    Maternally inherited bacterial endosymbionts such as\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    are common in arthropods. Some serve as reproductive manipulators, favoring the production of infected females in host populations despite possible fitness costs to the host. One such manipulation is feminization, in which the symbiont turns genetic males into functional females. To date, all described cases of feminization occur in host systems that are either female heterogametic (ZW-female\/ZZ-male) or where females are diploid and males are haploid for sex chromosomes (XX-female\/X0-male). Here we test potential fitness costs associated with feminization in the spider\n                    <jats:italic>Mermessus fradeorum<\/jats:italic>\n                    (Linyphiidae), which has a type of XX\/X0 sex determination. In addition to a feminizing\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    , this spider can be co-infected with up to four additional maternally-inherited bacterial endosymbionts. Using a series of increasingly speciose symbiont co-infections, including three containing the feminizing\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    , we measured female fecundity and the proportion of developed versus undeveloped offspring. We found that fitness costs were associated only with the feminizing\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    , but not with any of the other symbionts. Eggmasses infected with this\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    had 16% fewer eggs, and 20% of those eggs failed to develop, compared to only 4% failure in eggmasses from other symbiotypes. We hypothesize that the reduced egg viability results from the production of inviable 00 zygotes by feminized X0 individuals, which can provision X chromosomes to only half of their eggs. These results suggest that fitness costs may be an unavoidable consequence of feminization in hosts with an XX\/X0 sex determination system, potentially limiting the distribution of this reproductive manipulation phenotype.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2026.1798411","type":"journal-article","created":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T05:41:21Z","timestamp":1777527681000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Symbiont-mediated feminization imposes unavoidable host fitness costs"],"prefix":"10.3389","volume":"17","author":[{"given":"Jordyn D.","family":"Robinson","sequence":"first","affiliation":[{"name":"Department of Entomology, Agricultural Science Center North, University of Kentucky","place":["Lexington, KY, United States"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dylan T.","family":"Thorp","sequence":"additional","affiliation":[{"name":"Department of Entomology, Agricultural Science Center North, University of Kentucky","place":["Lexington, KY, United States"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeremy","family":"Van Cleve","sequence":"additional","affiliation":[{"name":"Department of Biology, T.H. Morgan Building, University of Kentucky","place":["Lexington, KY, United States"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jennifer A.","family":"White","sequence":"additional","affiliation":[{"name":"Department of Entomology, Agricultural Science Center North, University of Kentucky","place":["Lexington, KY, United States"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2026,4,30]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"7098","DOI":"10.1128\/AEM.00731-06","article-title":"Multilocus sequence typing system for the endosymbiont Wolbachia pipientis","volume":"72","author":"Baldo","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1787","DOI":"10.1111\/brv.70024","article-title":"Infection dynamics of endosymbionts that manipulate arthropod reproduction","volume":"100","author":"Brenninger","year":"2025","journal-title":"Biol. Rev."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1038\/hdy.2015.2","article-title":"Multiple endosymbiont infections and reproductive manipulations in a Linyphiid spider population","volume":"115","author":"Curry","year":"2015","journal-title":"Heredity"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1007\/s00442-025-05818-w","article-title":"Food availability influences adult body mass variability and reproductive traits in a spider","volume":"207","author":"Dong","year":"2025","journal-title":"Oecologia"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1016\/bs.aiip.2020.03.003","article-title":"The saboteur's tools: common mechanistic themes across manipulative symbioses","volume":"58","author":"Doremus","year":"2020","journal-title":"Adv. Insect Physiol."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"e03276","DOI":"10.1128\/AEM.03276-16","article-title":"Aphid heritable symbiont exploits defensive mutualism","volume":"83","author":"Doremus","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1741-7007-6-27","article-title":"The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone","volume":"6","author":"Duron","year":"2008","journal-title":"BMC Biol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1016\/j.jtbi.2004.06.029","article-title":"Infection dynamics of different Wolbachia-types within one host population","volume":"231","author":"Engelst\u00e4dter","year":"2004","journal-title":"J. Theor. Biol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"e11216","DOI":"10.1002\/ece3.11216","article-title":"Sex ratio distorting microbes exacerbate arthropod extinction risk in variable environments","volume":"14","author":"Fisher","year":"2024","journal-title":"Ecol. Evol."},{"key":"ref10","volume-title":"Biology of Spiders","author":"Foelix","year":"2011"},{"key":"ref11","first-page":"294","article-title":"DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates","volume":"3","author":"Folmer","year":"1994","journal-title":"Mol. Mar. Biol. Biotechnol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"10551","DOI":"10.1038\/s41598-020-67428-1","article-title":"The shutting down of the insulin pathway: a developmental window for Wolbachia load and feminization","volume":"10","author":"Herran","year":"2020","journal-title":"Sci. Rep."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1751","DOI":"10.1098\/rspb.2004.2769","article-title":"Multiple infection with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe","volume":"271","author":"Hiroki","year":"2004","journal-title":"Proc. R. Soc. London, Ser. B"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1098\/rspb.1991.0056","article-title":"The incidences and evolution of cytoplasmic male killers","volume":"244","author":"Hurst","year":"1991","journal-title":"Proc. R. Soc. Lond. Ser. B"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"329","DOI":"10.3201\/eid0604.000402","article-title":"Male-killing bacteria in insects: mechanisms, incidence, and implications","volume":"6","author":"Hurst","year":"2000","journal-title":"Emerg. Infect. Dis."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"161","DOI":"10.3390\/insects3010161","article-title":"Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications","volume":"3","author":"Kageyama","year":"2012","journal-title":"Insects"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1002\/evl3.28","article-title":"Feminizing Wolbachia endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species","volume":"1","author":"Kageyama","year":"2017","journal-title":"Evol. Lett."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1038\/s41579-025-01164-z","article-title":"Origin and function of beneficial bacterial symbioses in insects","volume":"23","author":"Kaltenpoth","year":"2025","journal-title":"Nat. Rev. Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1111\/oik.01421","article-title":"Contributions of juvenile and adult diet to the lifetime reproductive success and lifespan of a spider","volume":"124","author":"Kleinteich","year":"2015","journal-title":"Oikos"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"5112","DOI":"10.1128\/AEM.01043-13","article-title":"Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform","volume":"79","author":"Kozich","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1159\/000323497","article-title":"Insights into the meiotic behavior and evolution of multiple sex chromosome systems in spiders","volume":"133","author":"Kr\u00e1l","year":"2011","journal-title":"Cytogenet. Genome Res."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"e70149","DOI":"10.1111\/1462-2920.70149","article-title":"Wolbachia feminises a spider host with assistance from co-infecting symbionts","volume":"27","author":"Mackevicius-Dubickaja","year":"2025","journal-title":"Environ. Microbiol."},{"key":"ref23","article-title":"Elevated temperatures disrupt Wolbachia-induced feminization via microbial community dynamics across generations in a spider host","author":"Mackevicius-Dubickaja","year":"2026","journal-title":"Mol. Ecol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"R490","DOI":"10.1016\/j.cub.2024.04.027","article-title":"Rapid spread of a vertically transmitted symbiont induces drastic shifts in butterfly sex ratio","volume":"34","author":"Miyata","year":"2024","journal-title":"Curr. Biol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1146\/annurev.genet.41.110306.130119","article-title":"Genomics and evolution of heritable bacterial symbionts","volume":"42","author":"Moran","year":"2008","journal-title":"Annu. Rev. Genet."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1111\/j.1365-2311.2011.01274.x","article-title":"Wolbachia-induced feminisation newly found in Eurema hecabe, a sibling species of Eurema mandarina (Lepidoptera: Pieridae)","volume":"36","author":"Narita","year":"2011","journal-title":"Ecol. Entomol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"2409","DOI":"10.1098\/rspb.2006.3592","article-title":"Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX\/X0 sex-determination system","volume":"273","author":"Negri","year":"2006","journal-title":"Proc. R. Soc. Lond. Ser. B"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1273","DOI":"10.1098\/rspb.2005.3436","article-title":"Costs and benefits of a superinfection of facultative symbionts in aphids","volume":"273","author":"Oliver","year":"2006","journal-title":"Proc. R. Soc. Lond. Ser. B"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e16697","DOI":"10.1111\/1462-2920.16697","article-title":"Warm temperature inhibits cytoplasmic incompatibility induced by endosymbiotic Rickettsiella in spider hosts","volume":"26","author":"Proctor","year":"2024","journal-title":"Environ. Microbiol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1038\/sj.hdy.6885990","article-title":"Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity","volume":"83","author":"Rigaud","year":"1999","journal-title":"Heredity"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"2039","DOI":"10.1111\/mec.14449","article-title":"Context-dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum","volume":"27","author":"Rock","year":"2018","journal-title":"Mol. Ecol."},{"key":"ref32","volume-title":"Master\u2019s Thesis","author":"Rosenwald","year":"2020"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"20201107","DOI":"10.1098\/rspb.2020.1107","article-title":"Endosymbiotic Rickettsiella causes cytoplasmic incompatibility in a spider host","volume":"287","author":"Rosenwald","year":"2020","journal-title":"Proc. R. Soc. London, Ser. B"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"e61989","DOI":"10.7554\/eLife.61989","article-title":"Symbiont-mediated cytoplasmic incompatibility: what have we learned in 50 years?","volume":"9","author":"Shropshire","year":"2020","journal-title":"eLife"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"1500","DOI":"10.1111\/j.1558-5646.1994.tb02192.x","article-title":"Evolution of incompatibility-inducing microbes and their hosts","volume":"48","author":"Turelli","year":"1994","journal-title":"Evolution"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"e114","DOI":"10.1371\/journal.pbio.0050114","article-title":"From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila","volume":"5","author":"Weeks","year":"2007","journal-title":"PLoS Biol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1038\/nrmicro1969","article-title":"Wolbachia: master manipulators of invertebrate biology","volume":"6","author":"Werren","year":"2008","journal-title":"Nat. Rev. Microbiol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"144","DOI":"10.2307\/2347977","article-title":"Extra-binomial variation in logistic linear models","volume":"31","author":"Williams","year":"1982","journal-title":"Appl. Stat."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2026.1798411\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T05:41:23Z","timestamp":1777527683000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2026.1798411\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,30]]},"references-count":38,"alternative-id":["10.3389\/fmicb.2026.1798411"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2026.1798411","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,30]]},"article-number":"1798411"}}