© The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in ISME Journal 9 (2015): 1365–1377, doi:10.1038/ismej.2014.221. ; Emiliania huxleyi is the most abundant calcifying plankton in modern oceans with substantial intraspecific genome variability and a biphasic life cycle involving sexual alternation between calcified 2N and flagellated 1N cells. We show that high genome content variability in Emiliania relates to erosion of 1N-specific genes and loss of the ability to form flagellated cells. Analysis of 185 E. huxleyi strains isolated from world oceans suggests that loss of flagella occurred independently in lineages inhabiting oligotrophic open oceans over short evolutionary timescales. This environmentally linked physiogenomic change suggests life cycling is not advantageous in very large/diluted populations experiencing low biotic pressure and low ecological variability. Gene loss did not appear to reflect pressure for genome streamlining in oligotrophic oceans as previously observed in picoplankton. Life-cycle modifications might be common in plankton and cause major functional variability to be hidden from traditional taxonomic or molecular markers. ; This research was supported by a Marie Curie International Incoming Fellowship FUNSEXDEPHYND to PvD within the 7th European Community Framework Programme, FONDECYT Projects 1110575 (to PvD) and 312004 (to DM-F), the French Agence Nationale de la Recherche/Investissements d’Avenir Grants POSEIDON and OCEANOMICS (Grant No. ANR-11-BTBR-0008 to CdV and IP), the European ERA-net program BiodivERsA under the BioMarks project (to EMB), funding from NASA and NSF (Grants NNX11AF55G and EF-0424599 to DMG and SD), the Genoscope 2007-2008 sequencing initiative and the PACES research program of the Alfred Wegener Helmholtz Institute Helmhotz Centre for Polar and Marine Research.