Experimental evolution of multicellularity
Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae t...
Saved in:
| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 5; pp. 1595 - 1600 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
31.01.2012
National Acad Sciences |
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes. |
|---|---|
| AbstractList | Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes. [PUBLICATION ABSTRACT] Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes. Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes. Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among< ell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes. |
| Author | Borrello, Mark Travisano, Michael Ratcliff, William C Denison, R. Ford |
| Author_xml | – sequence: 1 fullname: Ratcliff, William C – sequence: 2 fullname: Denison, R. Ford – sequence: 3 fullname: Borrello, Mark – sequence: 4 fullname: Travisano, Michael |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22307617$$D View this record in MEDLINE/PubMed |
| BookMark | eNpdkUtLJDEUhYMo2j7WrnSa2QwIpffmWdkMiDijILhQ1yFdlWg11ZWepErGf2-K1vaxSRb3u4dz7tklm13oHCGHCKcIip0tO5tOEVEwyhD0BpnkFwvJNWySCQBVRckp3yG7Kc0BQIsStskOpQyURDUhJ5f_ly42C9f1tp2659AOfRO6afDTxdD2TeXadmhtbPqXfbLlbZvcwdu_Rx7-XN5fXBU3t3-vL85vikoI3hdyNqMUnEU389RT4bDWtaclkwCszO5KKzwD5ym3QjuwimlX11hZJT1mZo_8Xukuh9nC1VW2Fm1rltmljS8m2MZ8nXTNk3kMz4ZRpZDLLPDrTSCGf4NLvVk0aQxiOxeGZDSFnB-kyuTPb-Q8DLHL6YxGLaUu9Sh3toKqGFKKzq-tIJixBTO2YD5ayBvHnxOs-fezfwLGzQ85bYRBoUUGjlbAPPUhrgmOfIzI8_zHau5tMPYxNsk83FFADoCqzN7ZKxuJoeA |
| CitedBy_id | crossref_primary_10_1098_rsos_160544 crossref_primary_10_1111_nyas_13515 crossref_primary_10_1128_aem_00764_23 crossref_primary_10_1186_s12898_020_00281_y crossref_primary_10_1086_684100 crossref_primary_10_1093_bjps_axv033 crossref_primary_10_1007_s13752_018_0311_0 crossref_primary_10_1038_s41467_021_21050_5 crossref_primary_10_1038_s42003_022_03228_9 crossref_primary_10_1093_biosci_biu045 crossref_primary_10_1016_j_shpsc_2014_10_006 crossref_primary_10_1111_evo_12101 crossref_primary_10_1039_c2cc32387g crossref_primary_10_1007_s10539_015_9482_2 crossref_primary_10_1007_s00249_024_01702_2 crossref_primary_10_1186_s12052_015_0041_8 crossref_primary_10_7554_eLife_08595 crossref_primary_10_1098_rsif_2021_0716 crossref_primary_10_1098_rspb_2019_1098 crossref_primary_10_3390_fermentation6010020 crossref_primary_10_7554_eLife_72707 crossref_primary_10_7554_eLife_92899 crossref_primary_10_1016_j_jmb_2019_09_023 crossref_primary_10_1098_rstb_2016_0420 crossref_primary_10_1371_journal_pcbi_1005860 crossref_primary_10_3389_fmicb_2018_00158 crossref_primary_10_1016_j_mib_2023_102394 crossref_primary_10_1111_pala_12047 crossref_primary_10_1016_j_fgb_2016_06_007 crossref_primary_10_1038_s42003_024_06485_y crossref_primary_10_1093_jxb_eraa213 crossref_primary_10_1002_bies_201200143 crossref_primary_10_1007_s11229_017_1673_8 crossref_primary_10_7554_eLife_47951 crossref_primary_10_1016_j_fbr_2018_08_001 crossref_primary_10_1038_ncomms3742 crossref_primary_10_1073_pnas_2122197119 crossref_primary_10_3389_fevo_2021_730714 crossref_primary_10_1016_j_mib_2015_06_018 crossref_primary_10_3390_pathogens7010011 crossref_primary_10_1016_j_mib_2014_12_007 crossref_primary_10_1093_femsyr_fox025 crossref_primary_10_1038_s41559_019_0940_0 crossref_primary_10_1098_rsif_2016_0121 crossref_primary_10_1007_s10539_013_9363_5 crossref_primary_10_1038_ismej_2017_69 crossref_primary_10_1111_evo_14549 crossref_primary_10_1111_j_1558_5646_2012_01802_x crossref_primary_10_1098_rsos_160554 crossref_primary_10_3389_fmicb_2021_619122 crossref_primary_10_7554_eLife_78822 crossref_primary_10_1007_s10539_012_9354_y crossref_primary_10_1007_s12268_022_1812_8 crossref_primary_10_3389_fmicb_2019_01568 crossref_primary_10_7554_eLife_00655 crossref_primary_10_1016_j_fgb_2022_103671 crossref_primary_10_3892_ol_2020_11829 crossref_primary_10_7554_eLife_46735 crossref_primary_10_1093_nsr_nwad200 crossref_primary_10_1016_j_cell_2013_02_026 crossref_primary_10_1016_j_mib_2015_01_003 crossref_primary_10_1098_rstb_2013_0362 crossref_primary_10_1016_j_molp_2024_03_011 crossref_primary_10_1038_s41467_021_23104_0 crossref_primary_10_1016_j_jtbi_2015_02_002 crossref_primary_10_1111_eva_12943 crossref_primary_10_1016_j_jtbi_2018_08_038 crossref_primary_10_7554_eLife_83296 crossref_primary_10_1007_s12038_013_9375_y crossref_primary_10_1371_journal_pone_0059664 crossref_primary_10_1098_rsif_2022_0018 crossref_primary_10_7554_eLife_54348 crossref_primary_10_1098_rstb_2021_0408 crossref_primary_10_1098_rsfs_2015_0057 crossref_primary_10_1140_epjp_s13360_022_03252_y crossref_primary_10_1098_rspb_2023_1722 crossref_primary_10_1111_jeu_12306 crossref_primary_10_1557_mrs_2013_133 crossref_primary_10_1016_j_fbr_2020_07_002 crossref_primary_10_1086_678257 crossref_primary_10_1098_rspb_2023_1055 crossref_primary_10_1016_j_tim_2017_02_015 crossref_primary_10_1007_s10539_019_9688_9 crossref_primary_10_1016_j_actaastro_2014_08_013 crossref_primary_10_1073_pnas_1922076117 crossref_primary_10_1088_1478_3975_13_3_031001 crossref_primary_10_1088_1478_3975_10_3_035001 crossref_primary_10_1098_rspb_2016_1303 crossref_primary_10_1371_journal_pgen_1006668 crossref_primary_10_1111_jpy_13461 crossref_primary_10_1002_jez_b_22907 crossref_primary_10_1016_j_jgr_2021_04_006 crossref_primary_10_1371_journal_pgen_1008606 crossref_primary_10_1007_s00294_018_0823_y crossref_primary_10_1016_j_jtbi_2020_110293 crossref_primary_10_3390_jof7110886 crossref_primary_10_1016_j_gde_2022_101943 crossref_primary_10_1007_s10710_013_9196_7 crossref_primary_10_1007_s13752_021_00376_9 crossref_primary_10_3390_genes12040487 crossref_primary_10_1146_annurev_fluid_010313_141426 crossref_primary_10_1017_S0024282921000256 crossref_primary_10_1016_j_jtbi_2013_09_024 crossref_primary_10_1371_journal_pcbi_1008406 crossref_primary_10_1093_gbe_evt142 crossref_primary_10_1371_journal_pgen_1005684 crossref_primary_10_1111_brv_12418 crossref_primary_10_1098_rsif_2017_0484 crossref_primary_10_3389_fcell_2021_823447 crossref_primary_10_1016_j_coisb_2017_11_007 crossref_primary_10_1073_pnas_2015565118 crossref_primary_10_1098_rsos_180912 crossref_primary_10_1038_s41559_024_02367_y crossref_primary_10_1016_j_ympev_2014_01_007 crossref_primary_10_1016_j_mimet_2021_106338 crossref_primary_10_1007_s13752_012_0072_0 crossref_primary_10_1098_rsos_192211 crossref_primary_10_1111_brv_12412 crossref_primary_10_7554_eLife_73715 crossref_primary_10_1128_spectrum_03847_22 crossref_primary_10_7554_eLife_55414 crossref_primary_10_1038_s41567_017_0012_9 crossref_primary_10_1007_s10539_016_9517_3 crossref_primary_10_1007_s13752_021_00387_6 crossref_primary_10_1111_j_1558_5646_2012_01782_x crossref_primary_10_3998_ptpbio_6284 crossref_primary_10_1002_jez_b_22924 crossref_primary_10_1016_j_tplants_2016_02_004 crossref_primary_10_1093_femsyr_foab044 crossref_primary_10_1111_evo_13654 crossref_primary_10_1098_rsif_2016_0282 crossref_primary_10_4161_cam_19582 crossref_primary_10_1007_s13752_019_00317_7 crossref_primary_10_1016_j_cbpa_2017_08_012 crossref_primary_10_1016_j_gde_2018_05_006 crossref_primary_10_1016_j_mib_2016_04_007 crossref_primary_10_1098_rspb_2019_1948 crossref_primary_10_3390_genes14081635 crossref_primary_10_1038_s41567_017_0002_y crossref_primary_10_1371_journal_pbio_3001587 crossref_primary_10_15252_msb_202211353 crossref_primary_10_1038_s41522_022_00292_1 crossref_primary_10_1098_rspb_2015_2547 crossref_primary_10_1371_journal_pcbi_1005042 crossref_primary_10_1073_pnas_2208019119 crossref_primary_10_1093_evolut_qpad037 crossref_primary_10_1111_jeb_12804 crossref_primary_10_3389_fmicb_2017_01837 crossref_primary_10_1089_ast_2017_1779 crossref_primary_10_1128_MMBR_00008_18 crossref_primary_10_1098_rspb_2021_2722 crossref_primary_10_1134_S0031030113020044 crossref_primary_10_2142_biophys_63_316 crossref_primary_10_1002_yea_3241 crossref_primary_10_1186_s12862_023_02133_x crossref_primary_10_1002_ece3_5322 crossref_primary_10_1002_2015EF000339 crossref_primary_10_1016_j_algal_2023_103220 crossref_primary_10_1002_bies_201300052 crossref_primary_10_1073_pnas_1608278113 crossref_primary_10_3390_biology5020018 crossref_primary_10_1111_ede_12013 crossref_primary_10_7554_eLife_00367 crossref_primary_10_1128_mSystems_00018_20 crossref_primary_10_7554_eLife_23804 crossref_primary_10_1111_evo_13392 crossref_primary_10_1016_j_cub_2024_05_014 crossref_primary_10_1002_wcms_1701 crossref_primary_10_1534_genetics_116_198895 crossref_primary_10_1111_1462_2920_12866 crossref_primary_10_1038_s41559_024_02391_y crossref_primary_10_3389_fevo_2024_1335452 crossref_primary_10_1007_s12038_013_9344_5 crossref_primary_10_3389_fevo_2022_823588 crossref_primary_10_1016_j_mib_2022_102141 crossref_primary_10_1111_evo_13727 crossref_primary_10_1186_s12915_020_0762_1 crossref_primary_10_18632_aging_202727 crossref_primary_10_1093_femsec_fiac115 crossref_primary_10_1016_j_cub_2020_03_072 crossref_primary_10_1371_journal_pbio_3000397 crossref_primary_10_1002_ece3_7515 crossref_primary_10_1146_annurev_biophys_101220_072829 crossref_primary_10_1016_j_mib_2012_09_005 crossref_primary_10_1017_S1473550423000204 crossref_primary_10_1016_j_devcel_2017_09_016 crossref_primary_10_1016_j_jtbi_2014_06_026 crossref_primary_10_1038_s41598_017_16229_0 crossref_primary_10_1002_yea_3018 crossref_primary_10_1016_j_jtbi_2014_06_023 crossref_primary_10_1086_714488 crossref_primary_10_1098_rstb_2015_0444 crossref_primary_10_1007_s00446_021_00404_8 crossref_primary_10_1098_rstb_2012_0266 crossref_primary_10_1038_ncomms12085 crossref_primary_10_1371_journal_pbio_1001858 crossref_primary_10_1086_700095 crossref_primary_10_1128_mbio_01021_24 crossref_primary_10_1128_AAC_01371_12 crossref_primary_10_1016_j_mad_2018_09_001 crossref_primary_10_1038_nrg3564 crossref_primary_10_1063_5_0080845 crossref_primary_10_1093_gbe_evs083 crossref_primary_10_1186_s13068_024_02503_7 crossref_primary_10_1098_rsif_2015_0044 crossref_primary_10_1016_j_jhevol_2019_102671 crossref_primary_10_1016_j_cub_2020_08_006 crossref_primary_10_1016_j_physa_2018_11_023 crossref_primary_10_1111_evo_12760 crossref_primary_10_1515_bot_2016_0058 crossref_primary_10_1038_s41586_023_06052_1 crossref_primary_10_1098_rstb_2015_0438 crossref_primary_10_1111_evo_13615 crossref_primary_10_1098_rstb_2017_0106 crossref_primary_10_1002_jez_b_22727 crossref_primary_10_1016_j_gde_2017_09_003 crossref_primary_10_1016_j_tree_2020_07_013 crossref_primary_10_1128_EC_00184_12 crossref_primary_10_1016_j_ymben_2016_10_010 crossref_primary_10_1002_ece3_8067 crossref_primary_10_1007_s42087_021_00215_0 crossref_primary_10_1186_s12915_021_01087_0 crossref_primary_10_1016_j_cub_2023_03_031 crossref_primary_10_1016_j_physa_2017_11_080 crossref_primary_10_1146_annurev_micro_051421_121352 crossref_primary_10_1038_s41559_020_01363_2 crossref_primary_10_1002_ece3_3979 crossref_primary_10_3390_jof7090723 crossref_primary_10_1038_msb_2013_42 crossref_primary_10_1073_pnas_1209927110 crossref_primary_10_1126_science_1262053 crossref_primary_10_3390_fermentation3010004 crossref_primary_10_1098_rsif_2014_0982 crossref_primary_10_1093_bjps_axt055 crossref_primary_10_1371_journal_pcbi_1003803 crossref_primary_10_1093_evlett_qrae024 crossref_primary_10_3389_fcell_2023_1254636 crossref_primary_10_1007_s10516_018_9379_1 crossref_primary_10_1016_j_tree_2023_07_007 crossref_primary_10_1146_annurev_ecolsys_120213_091740 crossref_primary_10_1371_journal_pcbi_1010698 crossref_primary_10_1098_rsfs_2021_0082 crossref_primary_10_1038_s41467_023_39320_9 crossref_primary_10_1098_rsif_2016_0108 crossref_primary_10_1186_s12860_019_0234_z crossref_primary_10_1186_s12915_024_01878_1 crossref_primary_10_3390_genes11060690 crossref_primary_10_1086_716178 crossref_primary_10_1126_sciadv_adn2706 crossref_primary_10_1038_s41396_022_01275_y crossref_primary_10_3390_plants12183342 crossref_primary_10_1038_s41559_019_1086_9 crossref_primary_10_1086_697508 crossref_primary_10_3390_genes14040941 crossref_primary_10_1073_pnas_2315850121 crossref_primary_10_1371_journal_pcbi_1006987 crossref_primary_10_1016_j_tibs_2015_08_010 crossref_primary_10_1371_journal_pbio_3001844 crossref_primary_10_1128_JB_00469_20 crossref_primary_10_1016_j_bjm_2016_09_017 crossref_primary_10_7554_eLife_66711 crossref_primary_10_1038_ncomms15707 crossref_primary_10_1093_genetics_iyac042 crossref_primary_10_1038_nrmicro3178 crossref_primary_10_1038_nature_2012_9810 crossref_primary_10_7554_eLife_56349 crossref_primary_10_1103_PhysRevE_97_050401 crossref_primary_10_1016_j_tpb_2015_03_003 crossref_primary_10_1038_s41559_018_0503_9 crossref_primary_10_1007_s12038_014_9420_5 crossref_primary_10_1016_j_jtbi_2016_04_037 crossref_primary_10_21769_BioProtoc_3668 crossref_primary_10_7554_eLife_79665 crossref_primary_10_7554_eLife_84336 crossref_primary_10_1038_ncomms7102 crossref_primary_10_1128_mSphere_00702_18 crossref_primary_10_3389_fmicb_2016_01444 crossref_primary_10_3389_fmars_2018_00144 crossref_primary_10_1007_s11047_013_9380_y crossref_primary_10_1016_j_cub_2016_05_057 crossref_primary_10_1016_j_mbs_2016_03_002 crossref_primary_10_1111_jeb_13964 crossref_primary_10_1016_j_tcb_2012_08_010 crossref_primary_10_7717_peerj_7565 crossref_primary_10_1016_j_tree_2012_06_001 crossref_primary_10_1038_s41598_019_39558_8 crossref_primary_10_1038_s41598_020_63081_w crossref_primary_10_1111_tpj_12189 crossref_primary_10_1086_682588 crossref_primary_10_1098_rstb_2016_0175 crossref_primary_10_1186_s12934_023_02072_8 crossref_primary_10_1086_716634 crossref_primary_10_1038_nrmicro_2016_84 crossref_primary_10_3389_fpls_2014_00737 crossref_primary_10_1073_pnas_1202233109 crossref_primary_10_1098_rsos_191859 crossref_primary_10_1080_17435390_2018_1553253 crossref_primary_10_3390_genes12050661 crossref_primary_10_1007_s10682_017_9888_1 crossref_primary_10_1371_journal_pgen_1007691 crossref_primary_10_1162_artl_a_00284 crossref_primary_10_1140_epjp_i2017_11347_6 crossref_primary_10_1103_PhysRevX_14_011008 crossref_primary_10_1016_j_shpsc_2018_12_001 crossref_primary_10_1016_j_synbio_2017_10_004 crossref_primary_10_1093_genetics_iyac061 crossref_primary_10_1073_pnas_1305949110 crossref_primary_10_1134_S0006297922120100 crossref_primary_10_1098_rsif_2019_0054 crossref_primary_10_1111_evo_13701 |
| Cites_doi | 10.1098/rspb.2011.0766 10.1016/j.cub.2010.09.014 10.1111/j.1558-5646.2007.00304.x 10.1016/S0169-5347(97)01313-X 10.1111/j.1558-5646.2008.00541.x 10.1073/pnas.0811205106 10.1016/S1383-5742(02)00110-2 10.1038/nrc1016 10.1007/s10539-005-9018-2 10.1002/bies.20197 10.1038/nature06279 10.1002/(SICI)1520-6602(1998)1:1<27::AID-INBI4>3.0.CO;2-6 10.1016/j.jtbi.2005.08.043 10.1038/nrc2013 10.1099/00221287-147-9-2409 10.1016/j.femsyr.2004.07.007 10.1098/rstb.2009.0095 10.1126/science.1188800 10.1371/journal.pbio.1001122 10.1016/j.cell.2008.09.037 10.1371/journal.pbio.0060287 10.1093/icb/43.1.64 10.1146/annurev.ecolsys.36.102403.114735 10.1073/pnas.0702207104 10.1083/jcb.145.4.757 10.1038/cdd.2009.219 10.1111/j.1420-9101.2007.01466.x 10.1007/BF00647962 10.1016/0022-5193(64)90038-4 10.1038/35037734 10.1073/pnas.0335420100 10.1666/0094-8373(2005)031[0133:TDOES]2.0.CO;2 10.1007/BF02705126 10.1038/nature09201 10.1007/s00239-009-9201-1 10.1016/S0531-5565(01)00160-7 10.1093/emboj/19.24.6686 10.1111/j.1558-5646.2010.01103.x 10.1023/A:1006527528063 10.1002/bies.201000039 |
| ContentType | Journal Article |
| Copyright | copyright © 1993-2008 National Academy of Sciences of the United States of America Copyright National Academy of Sciences Jan 31, 2012 |
| Copyright_xml | – notice: copyright © 1993-2008 National Academy of Sciences of the United States of America – notice: Copyright National Academy of Sciences Jan 31, 2012 |
| DBID | FBQ CGR CUY CVF ECM EIF NPM AAYXX CITATION 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7X8 5PM |
| DOI | 10.1073/pnas.1115323109 |
| DatabaseName | AGRIS Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed CrossRef Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Calcium & Calcified Tissue Abstracts Chemoreception Abstracts Ecology Abstracts Entomology Abstracts (Full archive) Immunology Abstracts Neurosciences Abstracts Nucleic Acids Abstracts Oncogenes and Growth Factors Abstracts Virology and AIDS Abstracts Technology Research Database Environmental Sciences and Pollution Management Engineering Research Database AIDS and Cancer Research Abstracts Algology Mycology and Protozoology Abstracts (Microbiology C) Biotechnology and BioEngineering Abstracts Genetics Abstracts MEDLINE - Academic PubMed Central (Full Participant titles) |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) CrossRef Virology and AIDS Abstracts Oncogenes and Growth Factors Abstracts Technology Research Database Nucleic Acids Abstracts Ecology Abstracts Neurosciences Abstracts Biotechnology and BioEngineering Abstracts Environmental Sciences and Pollution Management Entomology Abstracts Genetics Abstracts Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) AIDS and Cancer Research Abstracts Chemoreception Abstracts Immunology Abstracts Engineering Research Database Calcium & Calcified Tissue Abstracts MEDLINE - Academic |
| DatabaseTitleList | Virology and AIDS Abstracts MEDLINE CrossRef |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database – sequence: 3 dbid: FBQ name: AGRIS url: http://www.fao.org/agris/Centre.asp?Menu_1ID=DB&Menu_2ID=DB1&Language=EN&Content=http://www.fao.org/agris/search?Language=EN sourceTypes: Publisher |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Sciences (General) |
| EISSN | 1091-6490 |
| EndPage | 1600 |
| ExternalDocumentID | 2577456201 10_1073_pnas_1115323109 22307617 109_5_1595 41477144 US201400178919 |
| Genre | Research Support, U.S. Gov't, Non-P.H.S Journal Article Feature |
| GroupedDBID | --- -DZ -~X .55 .GJ 0R~ 123 29P 2AX 2FS 2WC 3O- 4.4 53G 5RE 5VS 692 6TJ 79B 85S AACGO AAFWJ AANCE AAYJJ ABBHK ABOCM ABPLY ABPPZ ABPTK ABTLG ABZEH ACGOD ACIWK ACKIV ACNCT ACPRK ADULT ADZLD AENEX AEUPB AEXZC AFDAS AFFNX AFOSN AFRAH ALMA_UNASSIGNED_HOLDINGS ASUFR AS~ BKOMP CS3 D0L DCCCD DIK DNJUQ DOOOF DU5 DWIUU E3Z EBS EJD F20 F5P FBQ FRP GX1 HGD HH5 HQ3 HTVGU HYE JAAYA JBMMH JENOY JHFFW JKQEH JLS JLXEF JPM JSG JSODD JST KQ8 L7B LU7 MVM N9A NEJ NHB N~3 O9- OK1 P-O PNE PQQKQ R.V RHF RHI RNA RNS RPM RXW SA0 SJN TAE TN5 UKR VOH VQA W8F WH7 WHG WOQ WOW X7M XFK XSW Y6R YBH YKV YSK ZA5 ZCA ZCG ~02 ~KM ABXSQ AQVQM - 02 0R 1AW 55 AAPBV ABFLS ADACO AJYGW DZ H13 KM PQEST X XHC ADACV CGR CUY CVF ECM EIF IPSME NPM AAYXX CITATION 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7X8 ADQXQ 5PM |
| ID | FETCH-LOGICAL-c554t-6bb220ea1ebf2f25e1d9df283600380918a5f30ef24a59e0a739edd1ca76f1003 |
| IEDL.DBID | RPM |
| ISSN | 0027-8424 |
| IngestDate | Tue Sep 17 21:22:25 EDT 2024 Fri Aug 16 21:31:19 EDT 2024 Fri Sep 13 04:44:41 EDT 2024 Fri Aug 23 01:10:32 EDT 2024 Sat Sep 28 07:58:02 EDT 2024 Wed Nov 11 00:29:43 EST 2020 Fri Feb 02 07:04:34 EST 2024 Wed Dec 27 19:20:12 EST 2023 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 5 |
| Language | English |
| License | Freely available online through the PNAS open access option. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c554t-6bb220ea1ebf2f25e1d9df283600380918a5f30ef24a59e0a739edd1ca76f1003 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions: W.C.R., R.F.D., and M.T. designed research; W.C.R. performed research; W.C.R., R.F.D., M.B., and M.T. analyzed data; and W.C.R., R.F.D., M.B., and M.T. wrote the paper. Edited* by Richard E. Lenski, Michigan State University, East Lansing, MI, and approved December 14, 2011 (received for review September 19, 2011) |
| OpenAccessLink | https://www.pnas.org/content/pnas/109/5/1595.full.pdf |
| PMID | 22307617 |
| PQID | 919669896 |
| PQPubID | 42026 |
| PageCount | 6 |
| ParticipantIDs | proquest_journals_919669896 pubmedcentral_primary_oai_pubmedcentral_nih_gov_3277146 crossref_primary_10_1073_pnas_1115323109 proquest_miscellaneous_920230067 pubmed_primary_22307617 jstor_primary_41477144 fao_agris_US201400178919 pnas_primary_109_5_1595 |
| ProviderPackageCode | RNA PNE |
| PublicationCentury | 2000 |
| PublicationDate | 2012-01-31 |
| PublicationDateYYYYMMDD | 2012-01-31 |
| PublicationDate_xml | – month: 01 year: 2012 text: 2012-01-31 day: 31 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: Washington |
| PublicationTitle | Proceedings of the National Academy of Sciences - PNAS |
| PublicationTitleAlternate | Proc Natl Acad Sci U S A |
| PublicationYear | 2012 |
| Publisher | National Academy of Sciences National Acad Sciences |
| Publisher_xml | – name: National Academy of Sciences – name: National Acad Sciences |
| References | 20722725 - Evolution. 2011 Jan;65(1):3-20 12787815 - Mutat Res. 2003 Jun;543(3):235-49 21680410 - Integr Comp Biol. 2003 Feb;43(1):64-73 15489193 - FEMS Yeast Res. 2004 Nov;5(2):111-7 19013280 - Cell. 2008 Nov 14;135(4):726-37 12547910 - Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):1095-8 12612657 - Nat Rev Cancer. 2003 Mar;3(3):226-31 18036158 - J Evol Biol. 2008 Jan;21(1):104-10 18031303 - Evolution. 2008 Feb;62(2):436-51 15714559 - Bioessays. 2005 Mar;27(3):299-310 11118203 - EMBO J. 2000 Dec 15;19(24):6686-96 11048731 - Nature. 2000 Oct 12;407(6805):796-801 20616280 - Science. 2010 Jul 9;329(5988):223-6 20075938 - Cell Death Differ. 2010 May;17(5):763-73 12799498 - J Biosci. 2003 Jun;28(4):523-8 16288782 - J Theor Biol. 2006 Mar 21;239(2):257-72 20726010 - Bioessays. 2010 Oct;32(10):872-80 5875341 - J Theor Biol. 1964 Jul;7(1):1-16 17494740 - Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8597-604 17109012 - Nat Rev Cancer. 2006 Dec;6(12):924-35 21561969 - Proc Biol Sci. 2012 Jan 7;279(1726):116-21 21238226 - Trends Ecol Evol. 1998 Mar;13(3):112-6 18004383 - Nature. 2007 Nov 15;450(7168):411-4 19223580 - Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3254-8 10330404 - J Cell Biol. 1999 May 17;145(4):757-67 19805423 - Philos Trans R Soc Lond B Biol Sci. 2009 Nov 12;364(1533):3143-55 21857801 - PLoS Biol. 2011 Aug;9(8):e1001122 19209377 - J Mol Evol. 2009 Mar;68(3):256-68 19154376 - Evolution. 2009 Feb;63(2):306-23 11672984 - Exp Gerontol. 2001 Nov;36(10):1619-37 19067487 - PLoS Biol. 2008 Nov 25;6(11):e287 11535781 - Microbiology. 2001 Sep;147(Pt 9):2409-15 20971426 - Curr Biol. 2010 Oct 26;20(20):R875-6 20686567 - Nature. 2010 Aug 5;466(7307):720-6 Buss LW (e_1_3_3_27_2) 1987 e_1_3_3_17_2 e_1_3_3_16_2 e_1_3_3_19_2 e_1_3_3_38_2 e_1_3_3_18_2 e_1_3_3_39_2 e_1_3_3_13_2 e_1_3_3_36_2 e_1_3_3_12_2 e_1_3_3_37_2 e_1_3_3_15_2 e_1_3_3_34_2 Maynard Smith J (e_1_3_3_1_2) 1995 e_1_3_3_14_2 e_1_3_3_35_2 e_1_3_3_32_2 e_1_3_3_33_2 e_1_3_3_11_2 e_1_3_3_30_2 e_1_3_3_10_2 e_1_3_3_31_2 e_1_3_3_40_2 e_1_3_3_6_2 e_1_3_3_5_2 e_1_3_3_8_2 e_1_3_3_7_2 e_1_3_3_28_2 e_1_3_3_9_2 e_1_3_3_29_2 e_1_3_3_24_2 e_1_3_3_23_2 e_1_3_3_26_2 e_1_3_3_25_2 e_1_3_3_2_2 e_1_3_3_20_2 e_1_3_3_4_2 e_1_3_3_22_2 e_1_3_3_41_2 e_1_3_3_3_2 e_1_3_3_21_2 e_1_3_3_42_2 |
| References_xml | – ident: e_1_3_3_2_2 doi: 10.1098/rspb.2011.0766 – ident: e_1_3_3_34_2 doi: 10.1016/j.cub.2010.09.014 – ident: e_1_3_3_11_2 doi: 10.1111/j.1558-5646.2007.00304.x – ident: e_1_3_3_6_2 doi: 10.1016/S0169-5347(97)01313-X – ident: e_1_3_3_21_2 doi: 10.1111/j.1558-5646.2008.00541.x – ident: e_1_3_3_9_2 doi: 10.1073/pnas.0811205106 – ident: e_1_3_3_39_2 doi: 10.1016/S1383-5742(02)00110-2 – ident: e_1_3_3_8_2 doi: 10.1038/nrc1016 – ident: e_1_3_3_17_2 doi: 10.1007/s10539-005-9018-2 – ident: e_1_3_3_3_2 doi: 10.1002/bies.20197 – ident: e_1_3_3_20_2 doi: 10.1038/nature06279 – ident: e_1_3_3_13_2 doi: 10.1002/(SICI)1520-6602(1998)1:1<27::AID-INBI4>3.0.CO;2-6 – ident: e_1_3_3_19_2 doi: 10.1016/j.jtbi.2005.08.043 – ident: e_1_3_3_4_2 doi: 10.1038/nrc2013 – ident: e_1_3_3_32_2 doi: 10.1099/00221287-147-9-2409 – ident: e_1_3_3_29_2 doi: 10.1016/j.femsyr.2004.07.007 – ident: e_1_3_3_23_2 doi: 10.1098/rstb.2009.0095 – ident: e_1_3_3_41_2 doi: 10.1126/science.1188800 – ident: e_1_3_3_18_2 doi: 10.1371/journal.pbio.1001122 – ident: e_1_3_3_25_2 doi: 10.1016/j.cell.2008.09.037 – ident: e_1_3_3_5_2 doi: 10.1371/journal.pbio.0060287 – ident: e_1_3_3_35_2 doi: 10.1093/icb/43.1.64 – volume-title: The Major Transitions in Evolution year: 1995 ident: e_1_3_3_1_2 contributor: fullname: Maynard Smith J – ident: e_1_3_3_10_2 doi: 10.1146/annurev.ecolsys.36.102403.114735 – ident: e_1_3_3_40_2 doi: 10.1073/pnas.0702207104 – volume-title: The Evolution of Individuality year: 1987 ident: e_1_3_3_27_2 contributor: fullname: Buss LW – ident: e_1_3_3_30_2 doi: 10.1083/jcb.145.4.757 – ident: e_1_3_3_31_2 doi: 10.1038/cdd.2009.219 – ident: e_1_3_3_12_2 doi: 10.1111/j.1420-9101.2007.01466.x – ident: e_1_3_3_15_2 doi: 10.1007/BF00647962 – ident: e_1_3_3_24_2 doi: 10.1016/0022-5193(64)90038-4 – ident: e_1_3_3_36_2 doi: 10.1038/35037734 – ident: e_1_3_3_14_2 doi: 10.1073/pnas.0335420100 – ident: e_1_3_3_42_2 doi: 10.1666/0094-8373(2005)031[0133:TDOES]2.0.CO;2 – ident: e_1_3_3_22_2 doi: 10.1007/BF02705126 – ident: e_1_3_3_33_2 doi: 10.1038/nature09201 – ident: e_1_3_3_38_2 doi: 10.1007/s00239-009-9201-1 – ident: e_1_3_3_7_2 doi: 10.1016/S0531-5565(01)00160-7 – ident: e_1_3_3_26_2 doi: 10.1093/emboj/19.24.6686 – ident: e_1_3_3_37_2 doi: 10.1111/j.1558-5646.2010.01103.x – ident: e_1_3_3_16_2 doi: 10.1023/A:1006527528063 – ident: e_1_3_3_28_2 doi: 10.1002/bies.201000039 |
| SSID | ssj0009580 |
| Score | 2.5877564 |
| Snippet | Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental... |
| SourceID | pubmedcentral proquest crossref pubmed pnas jstor fao |
| SourceType | Open Access Repository Aggregation Database Index Database Publisher |
| StartPage | 1595 |
| SubjectTerms | Apoptosis Biological Evolution Biological Sciences Cell adhesion Cell division Cells Cellular differentiation determinate growth Ecological competition eukaryotic cells Evolution Forced migration Genes, Fungal Genotype Genotype & phenotype Genotypes labor life history new technology Phenotypes Physiology reproduction Saccharomyces cerevisiae Saccharomyces cerevisiae - cytology Saccharomyces cerevisiae - genetics Yeast Yeasts |
| Title | Experimental evolution of multicellularity |
| URI | https://www.jstor.org/stable/41477144 http://www.pnas.org/content/109/5/1595.abstract https://www.ncbi.nlm.nih.gov/pubmed/22307617 https://www.proquest.com/docview/919669896/abstract/ https://search.proquest.com/docview/920230067 https://pubmed.ncbi.nlm.nih.gov/PMC3277146 |
| Volume | 109 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1NT9wwEB2xnHqpSltKSoty4EArhU38uT5WCISQqCq1K3GzbMdukUp2xS79_Z3xJlmoOPVsZxTNjGfGyZs3AMdKJWWidlUKta5E8rJymMWqlkmfgnFN4NTgfP1VXc7F1Y282QE59MJk0H7wt6fd77vT7vZXxlYu78J0wIlNv12fcaY1TWqZwERzPlzRR6bd2abvhGH4FUwMfD6aT5edW1GMkJyqGiIMZYSDVnla2TYrTZJbDPBE4jzFp56rP_-FUT7KSxev4GVfUJZfNi--Bzuxew17_ZFdlSc9r_SnN_D5_BGbfxn_9E5XLlKZYYX0DZ9AqViXv4X5xfmPs8uqH5VQBawH1pXynrE6uib6xBKTsWlNmxh1aNR8hjXBzMnE65iYcNLE2mluYts2wWmVGtyzD7vdoosHUDIvRdKp9bgqaLhkMkokHgwLKvJYF3AyqMouN4wYNv_J1tySquxWwQUcoCqt-4nxys6_M7rNYQSYmQaX9rN-RxGiEWRUUcC7LGUr2lhpseiSBRwONrD9QVtZFKVoBqYqoBxX8YSQylwXFw-4hSbEU1Ym0dlgo_DB_AXoJ6YcNxD59tMV9MlMwt374Pv_fvIQXqBCCBeDefAD7K7vH-JHLHDW_ig79F9GW_Zp |
| link.rule.ids | 230,315,733,786,790,891,27957,27958,53827,53829 |
| linkProvider | National Library of Medicine |
| linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LbxMxEB615QAXoEDpUh574FCQNtn1M3tEVasATYVEg3qzvF4bKugmIgkHfj0zzu6mrbjAeeyR7BnPjOXP3wC8Viqo0mubBZfrTIRKZhazWFYzWQVX2sJx-uA8OVPjqfhwIS-2QHZ_YSJo31WXg-bH1aC5_BaxlfMrN-xwYsNPkyPOtKZOLdtwB88r090lvefaHa1_njAMwIKJjtFH8-G8sQuKEpJTXUOUoYyQ0Cr2K9vkpe1gZx1AkVhPcdbfKtDbQMprmenkAXzp1rQGpHwfrJbVwP2-Rff4z4t-CPfbWjV9txbvwpZvHsFuGw0W6WFLWf3mMbw9vtYoIPW_Wn9OZyGNiEV6HiC8K5b8T2B6cnx-NM7aLgyZw1JjmamqYiz3tvBVYIFJX9RlHRh9_sj5CMuNkZWB5z4wYWXpc6t56eu6cFarUOCYPdhpZo3fh5RVUgQd6gqlgvpWhlKJwF3JnPLc5wkcdjYw8zXZhomP5JobsoHZWC6BfbSRsV8xFJrpZ0YXRQwuo7JA0V40XK9CFIK2TiTwNGrZqC6NNFjPyQQOOuOa9gwvDKpS1F5TJZD2Ujx8tGW28bMVDqHm85TwSXX0hF5551cJ6Bs-0g8gXu-bErR85PduLf3sv2e-grvj88mpOX1_9vEA7uHmEPwG0-1z2Fn-XPkXWEctq5fx1PwBtbQYbg |
| linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LbxMxELZokRAXoEDbpTz2wKEgbbLrZ3xEpVF5tKoEkSoulu21oYJuIpJw4Ncz4-xu0opTzzMeyR57Zix__oaQ11JGqYOyRfSlKnh0orCQxYqaChe9tpVn-MH59EyeTPjHC3Gx0eorgfa9uxw0v64GzeWPhK2cXflhhxMbnp8eMaoUdmqZ1XG4Re7CmaW6u6j3fLuj1e8TCkGYU96x-ig2nDV2jpFCMKxtkDaUIhpapp5l69y0Fe20Ayki8ymM-l8VehNMuZGdxg_Jt25eK1DKz8Fy4Qb-7w3Kx1tN_BF50Nas-buVyg65E5rHZKeNCvP8sKWufvOEvD3eaBiQhz_tvs6nMU_IRXwmQNwrlP5PyWR8_PXopGi7MRQeSo5FIZ2jtAy2Ci7SSEWoal1Hip9ASjaCsmNkRWRliJRboUNpFdOhritvlYwV6OyS7WbahH2SUyd4VLF2IOXYvzJqySPzmnoZWCgzctj5wcxWpBsmPZYrZtAPZu29jOyDn4z9DiHRTL5QvDBCkBnpCkS7yXm9CV5xXD6ekb1kZW1aG2GgrhMZOegcbNqzPDdgSmKbTZmRvJfCIcQls02YLkEFm9Bj4kfTaTf0xru9lRF1bZ_0CsjvfV0C3k883623n9165Cty7_z92Hz-cPbpgNyHtUEUDmTd52R78XsZXkA5tXAv08H5B58FGu4 |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Experimental+evolution+of+multicellularity&rft.jtitle=Proceedings+of+the+National+Academy+of+Sciences+-+PNAS&rft.au=Ratcliff%2C+William&rft.au=Denison%2C+R.+Ford&rft.au=Borrello%2C+Mark&rft.au=Travisano%2C+Michael&rft.date=2012-01-31&rft.pub=National+Academy+of+Sciences&rft.issn=0027-8424&rft.eissn=1091-6490&rft.volume=109&rft.issue=5&rft.spage=1595&rft.epage=1600&rft_id=info:doi/10.1073%2Fpnas.1115323109&rft.externalDocID=41477144 |
| thumbnail_m | http://utb.summon.serialssolutions.com/2.0.0/image/custom?url=http%3A%2F%2Fwww.pnas.org%2Fcontent%2F109%2F5.cover.gif |
| thumbnail_s | http://utb.summon.serialssolutions.com/2.0.0/image/custom?url=http%3A%2F%2Fwww.pnas.org%2Fcontent%2F109%2F5.cover.gif |