Elucidation of the brown algal gamete evolution with a new timeframe and organelle data

Seok-Wan Choi1, Louis Graf1, Ji Won Choi1, Hiroshi Kawai2, Seung Wook Jung3, Chang Geun Choi3 and Hwan Su Yoon1

1Department of Biological Sciences, Sungkyunkwan University, Suwon 16419, Korea

2Kobe University Research Center for Inland Seas, Rokkodai, Nadaku, Kobe, 657-8501, Japan

3Department of Ecological Engineering, College of Environmental and Marine Technology, Pukyong National University, Busan 48513, Korea

 

Brown algae (Phaeophyceae) are one of the six eukaryotic lineages that achieved complex multicellularity and shows morphological variability of gametes (isogamy, anisogamy and oogamy). In contrast to the previous theoretical assumption that asserted correlation between anisogamy and cellular complexity and instability of isogamy (the PBS theory), there exist multiple lineages of isogamous species in the brown algae. However, the factors that prevented gametes from diversifying into large eggs and small sperms have remained unclear. Based on the robust phylogeny constructed with plastome data, we estimated the timing of lineage diversification and transitions in gamete types within the brown algae. We showed that simple multicellular brown ancestor achieved complex multicellularity with cell-to-cell communication and tissue differentiation ca. 900-800 Mya, after which ancestral isogamy has persisted extraordinarily long with parthenogenetic ability, which is consistent with the recent modeling paper. We also presented reversions of oogamy to isogamy occurred during or after the Late Paleozoic ice age (360-260 Mya) and two mass extinctions (Permian–Triassic and Triassic–Jurassic), implying that the parthenogenetic post-glacial colonization and recovery after extinctions induced the transitions back to the original isogamous states. With comparing the extent of incomplete lineage sorting in organelle genomes between isogamous and non-isogamous lineages, we present an ‘isogamous ancestral polymorphism’ model to elucidate the possible advantages of parthenogenetic isogamous species during the re-colonization process. The main findings of the study will shed light on future studies on the relationship between the gamete dimorphism and various strategies of life cycle.