{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T06:24:16Z","timestamp":1791440656216,"version":"4.3.3"},"reference-count":29,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T00:00:00Z","timestamp":1682380800000},"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. Cell Dev. Biol."],"abstract":"<jats:p>Maternal effects are an evolutionary strategy used to improve offspring quality. In an example of maternal effects in honey bees (<jats:italic>Apis mellifera<\/jats:italic>), mother queens produce larger eggs in queen cells than in worker cells in order to breed better daughter queens. In our current study, morphological indexes, reproductive tissues, and the egg-laying ability of newly reared queens reared with eggs laid in queen cells (QE), eggs laid in worker cells (WE), and 2-day-old larvae in worker cells (2L) were evaluated. In addition, morphological indexes of offspring queens and working performance of offspring workers were examined. The thorax weight, number of ovarioles, egg length, and number of laid eggs and capped broods of QE were significantly higher than those of WE and 2L, indicating that the reproductive capacity of QE group was better than that of other groups. Furthermore, offspring queens from QE had larger thorax weights and sizes than those from the other two groups. Offspring worker bees from QE also had larger body sizes and greater pollen-collecting and royal jelly-producing abilities than those of other two groups. These results demonstrate that honey bees display profound maternal effects on queen quality that can be transmitted across generations. These findings provide a basis for improving queen quality, with implications in apicultural and agricultural production.<\/jats:p>","DOI":"10.3389\/fcell.2023.1156923","type":"journal-article","created":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T05:12:35Z","timestamp":1682399555000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["Honey bee maternal effects improve worker performance and reproductive ability in offspring"],"prefix":"10.3389","volume":"11","author":[{"given":"Longtao","family":"Yu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xujiang","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinxin","family":"Shi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weiyu","family":"Yan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaobo","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,4,25]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"48","DOI":"10.3390\/insects8020048","article-title":"Queen quality and the impact of honey bee diseases on queen health: Potential for interactions between two major threats to colony health","volume":"8","author":"Amiri","year":"2017","journal-title":"Insects"},{"key":"B2","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1093\/icb\/36.2.83","article-title":"Maternal effects in animal ecology","volume":"36","author":"Bernardo","year":"1996","journal-title":"Integr. Comp. Biol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1038\/35003565","article-title":"Egg investment is influenced by male attractiveness in the mallard","volume":"404","author":"Cunningham","year":"2000","journal-title":"Nature"},{"key":"B4","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1080\/09712119.2003.9706442","article-title":"Comparison of some features of queens reared from different honeybee (Apis mellifera L.) genotypes","volume":"24","author":"Dodologlu","year":"2003","journal-title":"J. Appl. Anim. Res."},{"key":"B5","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1007\/s000400050159","article-title":"Worker regulation of emergency queen rearing in honey bee colonies and the resultant variation in queen quality","volume":"46","author":"Hatch","year":"1999","journal-title":"Insectes Sociaux"},{"key":"B6","doi-asserted-by":"publisher","first-page":"337","DOI":"10.3896\/ibra.1.53.3.02","article-title":"A review of methods used in some European countries for assessing the quality of honey bee queens through their physical characters and the performance of their colonies","volume":"53","author":"Hatjina","year":"2014","journal-title":"J. Apic. Res."},{"key":"B7","doi-asserted-by":"publisher","first-page":"e5935","DOI":"10.13102\/sociobiology.v68i1.5935","article-title":"Honeybee (Apis mellifera) maternal effect causes alternation of DNA methylation regulating queen development","volume":"68","author":"He","year":"2021","journal-title":"Sociobiology"},{"key":"B8","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1080\/03670244.1973.9990324","article-title":"Maternal nutrition: A positive approach in family planning","volume":"2","author":"Hseuh","year":"1973","journal-title":"Ecol. Food & Nutr."},{"key":"B9","doi-asserted-by":"publisher","first-page":"688","DOI":"10.3390\/insects12080688","article-title":"Overview of bee pollination and its economic value for crop production","volume":"12","author":"Khalifa","year":"2021","journal-title":"Insects"},{"key":"B10","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.jip.2012.06.006","article-title":"Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae","volume":"111","author":"Kirsten","year":"2012","journal-title":"J. Invertebr. Pathology"},{"key":"B11","doi-asserted-by":"publisher","first-page":"12","DOI":"10.3390\/insects10010012","article-title":"Is the brood pattern within a honey bee colony a reliable indicator of queen quality?","volume":"10","author":"Lee","year":"2019","journal-title":"Insects"},{"key":"B12","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/s0169-5347(98)01472-4","article-title":"The adaptive significance of maternal effects","volume":"13","author":"Moussear","year":"1998","journal-title":"Trends Ecol. Evol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1080\/00218839.1983.11100589","article-title":"Honey productivity of honeybee colonies in relation to body weight, attractiveness and fecundity of the queen","volume":"22","author":"Nelson","year":"1983","journal-title":"J. Apic. Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1007\/bf02224522","article-title":"The laying of biased eggs by the ant Pheidole pallidula (Nyl,) (Hymenoptera, Formicidae)","volume":"27","author":"Passera","year":"1980","journal-title":"Insectes Sociaux"},{"key":"B15","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1007\/s00040-012-0267-1","article-title":"The effects of honey bee (Apis melliferaL.) queen reproductive potential on colony growth","volume":"60","author":"Rangel","year":"2013","journal-title":"Insectes Sociaux"},{"key":"B16","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1126\/science.1185563","article-title":"Clarity on honey bee collapse?","volume":"327","author":"Ratnieks","year":"2010","journal-title":"Science"},{"key":"B17","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.domaniend.2004.06.005","article-title":"Effects of maternal nutrition and porcine growth hormone (pGH) treatment during gestation on endocrine and metabolic factors in sows,fetuses and pigs, skeletal muscle development, and postnatal growth","volume":"27","author":"Rehfeldt","year":"2004","journal-title":"Domest. Anim. Endocrinol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1146\/annurev.es.18.110187.001233","article-title":"Maternal effects in plants","volume":"18","author":"Roach","year":"1987","journal-title":"Annu. Rev. Ecol. Evol. Sistematics"},{"key":"B19","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/B978-0-12-809633-8.20836-4","article-title":"Maternal effects on behavior","volume-title":"Encyclopedia of animal behavior","author":"Schwabl","year":"2019"},{"key":"B20","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/j.cub.2008.01.024","article-title":"Maternal effect on female caste determination in a social insect","volume":"18","author":"Schwander","year":"2008","journal-title":"Curr. Biol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1080\/10496500802173939","article-title":"A review and bibliography of the literature of honey bee colony collapse disorder: A poorly understood epidemic that clearly threatens the successful pollination of billions of dollars of crops in America","volume":"9","author":"Stankus","year":"2008","journal-title":"J. Agric. Food Inf."},{"key":"B22","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1007\/s00114-013-1065-y","article-title":"Genetic diversity affects colony survivor ship in commercial honey bee colonies","volume":"100","author":"Tarpy","year":"2013","journal-title":"Naturwissenschaften"},{"key":"B23","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/B978-0-12-800049-6.00051-2","article-title":"Maternal effects","volume-title":"encyclopedia of evolutionary Biology","author":"Van Dooren","year":"2016"},{"key":"B24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3896\/ibra.1.50.1.01","article-title":"A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010","volume":"50","author":"van Engelsdorp","year":"2011","journal-title":"J. Apic. Res."},{"key":"B25","doi-asserted-by":"publisher","first-page":"2208","DOI":"10.1016\/j.cub.2019.05.059","article-title":"A maternal effect on queen production in honeybees","volume":"29","author":"Wei","year":"2019","journal-title":"Curr. Biol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1107","DOI":"10.1098\/rstb.2008.0238","article-title":"What are maternal effects (and what are they not)?","volume":"364","author":"Wolf","year":"2009","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1080\/00218839.1971.11099669","article-title":"Correlations between the age at which honeybee brood was grafted, characteristics of the resultant queens, and results of insemination","volume":"10","author":"Woyke","year":"1971","journal-title":"J. Apic. Res."},{"key":"B28","doi-asserted-by":"publisher","first-page":"282","DOI":"10.3389\/fpsyt.2020.00282","article-title":"Effects of commercial queen rearing methods on queen fecundity and genome methylation","volume":"52","author":"Yi","year":"2020","journal-title":"Apidologie"},{"key":"B29","doi-asserted-by":"publisher","first-page":"486","DOI":"10.3390\/insects13050486","article-title":"High-quality queens produce high-quality offspring queens","volume":"13","author":"Yu","year":"2022","journal-title":"Insects"}],"container-title":["Frontiers in Cell and Developmental Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2023.1156923\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T05:12:39Z","timestamp":1682399559000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2023.1156923\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,25]]},"references-count":29,"alternative-id":["10.3389\/fcell.2023.1156923"],"URL":"https:\/\/doi.org\/10.3389\/fcell.2023.1156923","relation":{},"ISSN":["2296-634X"],"issn-type":[{"value":"2296-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,25]]},"article-number":"1156923"}}