{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T16:16:41Z","timestamp":1789661801506,"version":"4.0.1"},"reference-count":62,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2014,8,20]],"date-time":"2014-08-20T00:00:00Z","timestamp":1408492800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Evolution and Development"],"published-print":{"date-parts":[[2014,9]]},"abstract":"<jats:title>SUMMARY<\/jats:title>\n                  <jats:sec>\n                    <jats:label\/>\n                    <jats:p>\n                      Understanding the robustness of developmental systems requires insights into the sensitivity of underlying molecular and cellular parameters to perturbations, and how such sensitivity evolves. We address these issues using vulval cell fate determination\u2014a reproducible and robust patterning process regulated by a cross\u2010talk of EGF\u2010Ras\u2010MAPK and Delta\u2010Notch pathways. Although the final vulval cell fate pattern is identical in all\n                      <jats:italic>Caenorhabditis<\/jats:italic>\n                      species, the patterning process underlies extensive cryptic genetic variation between and within species. Here, we tested whether this cryptic genetic variation translates into variation in developmental sensitivity to environmental perturbations. We disrupted vulval patterning using thermal perturbations to quantify and compare environmental sensitivity of different system parameters between distinct genotypes of\n                      <jats:italic>C. elegans<\/jats:italic>\n                      and\n                      <jats:italic>C. briggsae<\/jats:italic>\n                      . Thermal perturbations globally debuffered vulval development, triggering diverse pattering variants, whose frequency and spectra were strongly species\u2010 and genotype\u2010dependent. This condition\u2010dependent variation indicates that environmental sensitivity of different system properties, such as vulval competence or vulval induction, is subject to evolutionary change. High temperature induced a genotype\u2010specific decrease of secondary fate induction and corresponding Notch pathway activity in the\n                      <jats:italic>C. elegans<\/jats:italic>\n                      N2 strain; in contrast, hypoinduction of the primary cell fate was never observed. Vulval precursor cells therefore differ in temperature sensitivity and such cell\u2010specific sensitivity shows evolutionary variation. We further compared spectra of temperature\u2010induced vulval variants to the ones induced by mutation accumulation in the same genotypes. In response to either perturbation, we observed similar genotype\u2010dependence of variant production, allowing identification of distinct system features most sensitive to both mutation and environment. Taken together, we show how sensitivity of system parameters regulating\n                      <jats:italic>Caenorhabditis<\/jats:italic>\n                      vulval development depends on subtle interactions between perturbations and genetic background. Our results imply that cryptic genetic variation may reflect evolutionary variation in developmental robustness, therefore potentially contributing to the maintenance of phenotypic precision when facing perturbations.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1111\/ede.12091","type":"journal-article","created":{"date-parts":[[2014,8,20]],"date-time":"2014-08-20T23:19:46Z","timestamp":1408576786000},"page":"278-291","source":"Crossref","is-referenced-by-count":14,"title":["Cryptic genetic variation uncovers evolution of environmentally sensitive parameters in\n                    <i>Caenorhabditis<\/i>\n                    vulval development"],"prefix":"10.1111","volume":"16","author":[{"given":"St\u00e9phanie","family":"Grimbert","sequence":"first","affiliation":[{"name":"Institut de Biologie Valrose CNRS UMR7277, Parc Valrose 06108 Nice cedex 02 France"},{"name":"INSERM U1091 06108 Nice cedex 02 France"},{"name":"Universit\u00e9 Nice Sophia Antipolis UFR Sciences 06108 Nice cedex 02 France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Braendle","sequence":"additional","affiliation":[{"name":"Institut de Biologie Valrose CNRS UMR7277, Parc Valrose 06108 Nice cedex 02 France"},{"name":"INSERM U1091 06108 Nice cedex 02 France"},{"name":"Universit\u00e9 Nice Sophia Antipolis UFR Sciences 06108 Nice cedex 02 France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2014,8,20]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-11-157"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1017\/CBO9780511606830"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1086\/589455"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0406056102"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2012.12.001"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1055642"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1000877"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2008.09.011"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12038-009-0073-8"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1002\/bies.20456"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0070-2153(07)80005-6"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2013.01.009"},{"key":"e_1_2_7_14_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003661"},{"key":"e_1_2_7_15_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.1996.8471"},{"key":"e_1_2_7_16_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-9822(01)00202-0"},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2004.03.010"},{"key":"e_1_2_7_18_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001230"},{"key":"e_1_2_7_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2003.10.001"},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/sj.hdy.6800915"},{"key":"e_1_2_7_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2006.12.024"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1088\/1478-3975\/9\/4\/045001"},{"key":"e_1_2_7_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.gde.2012.08.003"},{"key":"e_1_2_7_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2012.01.002"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1086\/432265"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg1426"},{"key":"e_1_2_7_27_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.271.5246.200"},{"key":"e_1_2_7_28_1","doi-asserted-by":"publisher","DOI":"10.1101\/gad.981602"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01762870"},{"key":"e_1_2_7_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(83)90377-X"},{"key":"e_1_2_7_31_1","doi-asserted-by":"publisher","DOI":"10.1002\/jez.b.21161"},{"key":"e_1_2_7_32_1","doi-asserted-by":"publisher","DOI":"10.1038\/358470a0"},{"key":"e_1_2_7_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2011.02.040"},{"key":"e_1_2_7_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2004.09.001"},{"key":"e_1_2_7_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(95)90317-8"},{"key":"e_1_2_7_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2007.10.061"},{"key":"e_1_2_7_37_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-11-339"},{"key":"e_1_2_7_38_1","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.105.051649"},{"key":"e_1_2_7_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2009.07.005"},{"key":"e_1_2_7_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2010.06.002"},{"key":"e_1_2_7_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(02)02596-X"},{"key":"e_1_2_7_42_1","doi-asserted-by":"publisher","DOI":"10.1101\/gad.495308"},{"key":"e_1_2_7_43_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1073846"},{"key":"e_1_2_7_44_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg3688"},{"key":"e_1_2_7_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2011.05.675"},{"key":"e_1_2_7_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2011.06.006"},{"key":"e_1_2_7_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-2660(08)60529-5"},{"key":"e_1_2_7_48_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.2010.01110.x"},{"key":"e_1_2_7_49_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature749"},{"key":"e_1_2_7_50_1","doi-asserted-by":"publisher","DOI":"10.1038\/24550"},{"key":"e_1_2_7_51_1","volume-title":"Biometry","author":"Sokal 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