A comparative test of the gamete dynamics theory for the evolution of anisogamy in Bryopsidales green algae

Togashi, Tatsuya; Horinouchi, Yusuke; Parker, Geoff A.

doi:10.1098/rsos.201611

Cited by 6 publications

(3 citation statements)

References 45 publications

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“…(Note: a gone cell constitutes the haploid meiotic product arising from a diploid zygospore. 69 ) Chlamydomonas reinhardtii , Tetrabaena , and Gonium produce all four haploid gone cells per diploid zygospore. 47 According to our ASR results full meiotic hatching is lost either once or twice in the volvocine algae ( Supplementary Figures 29 and 30 ) Our Mr. Bayes ASR indicates a single loss, but this could be an artifact arising from low sampling of taxa that exhibit full meiotic hatching.…”

Section: Resultsmentioning

confidence: 99%

Fossil-calibrated inference of divergence times among the Volvocine algae enables reconstruction of the steps that led to differentiated multicellularity

Lindsey,

Knoll,

Herron

et al. 2023

Preprint

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Throughout its nearly four-billion-year history, life has undergone evolutionary transitions in which simpler subunits have become integrated to form a more complex whole. Many of these transitions opened the door to innovations that resulted in increased biodiversity and/or organismal efficiency. The evolution of multicellularity from unicellular forms represents one such transition, one that paved the way for cellular differentiation, including differentiation of male and female gametes. A useful model for studying the evolution of multicellularity and cellular differentiation is the volvocine algae, a clade of freshwater green algae whose members range from unicellular to colonial, from undifferentiated to completely differentiated, and whose gamete types can be isogamous, anisogamous, or oogamous. To better understand how multicellularity, differentiation, and gametes evolved in this group, we used comparative genomics and fossil data to establish a geologically calibrated roadmap of when these innovations occurred. Our results, presented as ancestral-state reconstructions, show that multicellularity arose independently twice in this clade. Our chronograms indicate multicellularity evolved during the Carboniferous-Triassic periods in Goniaceae + Volvocaceae, and possibly as early as the Cretaceous in Tetrabaenaceae. Using divergence time estimates we inferred when, and in what order, specific developmental changes occurred that led to differentiated multicellularity and oogamy. We find that in the volvocine algae the temporal sequence of developmental changes leading to differentiated multicellularity is much as proposed by David Kirk, and that multicellularity is correlated with the acquisition of anisogamy and oogamy. Lastly, morphological, molecular, and divergence time data suggest the possibility of cryptic species in Tetrabaenaceae.

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Section: Resultsmentioning

confidence: 99%

Fossil-calibrated inference of divergence times among the Volvocine algae enables reconstruction of the steps that led to differentiated multicellularity

Lindsey,

Knoll,

Herron

et al. 2023

Preprint

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“…Prior to the evolution of anisogamy, the number of "gone cells" released from a zygospore decreases. (Note: a gone cell constitutes the haploid meiotic product arising from a diploid zygospore [154].) Chlamydomonas reinhardtii, Tetrabaena, and Gonium produce all four haploid gone cells per diploid zygospore [88].…”

Section: Ancestral-state Reconstructions Support Previous Findings Th...mentioning

confidence: 99%

Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae

Lindsey,

Knoll,

Herron

et al. 2024

BMC Biol

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Background Throughout its nearly four-billion-year history, life has undergone evolutionary transitions in which simpler subunits have become integrated to form a more complex whole. Many of these transitions opened the door to innovations that resulted in increased biodiversity and/or organismal efficiency. The evolution of multicellularity from unicellular forms represents one such transition, one that paved the way for cellular differentiation, including differentiation of male and female gametes. A useful model for studying the evolution of multicellularity and cellular differentiation is the volvocine algae, a clade of freshwater green algae whose members range from unicellular to colonial, from undifferentiated to completely differentiated, and whose gamete types can be isogamous, anisogamous, or oogamous. To better understand how multicellularity, differentiation, and gametes evolved in this group, we used comparative genomics and fossil data to establish a geologically calibrated roadmap of when these innovations occurred. Results Our ancestral-state reconstructions, show that multicellularity arose independently twice in the volvocine algae. Our chronograms indicate multicellularity evolved during the Carboniferous-Triassic periods in Goniaceae + Volvocaceae, and possibly as early as the Cretaceous in Tetrabaenaceae. Using divergence time estimates we inferred when, and in what order, specific developmental changes occurred that led to differentiated multicellularity and oogamy. We find that in the volvocine algae the temporal sequence of developmental changes leading to differentiated multicellularity is much as proposed by David Kirk, and that multicellularity is correlated with the acquisition of anisogamy and oogamy. Lastly, morphological, molecular, and divergence time data suggest the possibility of cryptic species in Tetrabaenaceae. Conclusions Large molecular datasets and robust phylogenetic methods are bringing the evolutionary history of the volvocine algae more sharply into focus. Mounting evidence suggests that extant species in this group are the result of two independent origins of multicellularity and multiple independent origins of cell differentiation. Also, the origin of the Tetrabaenaceae-Goniaceae-Volvocaceae clade may be much older than previously thought. Finally, the possibility of cryptic species in the Tetrabaenaceae provides an exciting opportunity to study the recent divergence of lineages adapted to live in very different thermal environments.

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“…In ulvophyceans, uniparental inheritance of organelles appears to be imperfect in isogamous species: mitochondrial and chloroplast genomes are inherited biparentally as well as uniparentally in some crosses [15,16]. In this study, we focus on a slightly anisogamous ulvophycean green alga, Monostroma angicava, that has a low anisogamy ratio (female gamete volume/male gamete volume [17]) (see [18] for more strongly anisogamous species). This alga has a dioecious heteromorphic haplo-diplontic life cycle with a haploid multicellular male or female gametophyte generation and a diploid unicellular sporophyte generation [17,[19][20][21][22][23] (figure 1).…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial uniparental inheritance achieved after fertilization challenges the nuclear–cytoplasmic conflict hypothesis for anisogamy evolution

Togashi,

Parker,

Horinouchi

2023

Biol. Lett.

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In eukaryotes, a fundamental phenomenon underlying sexual selection is the evolution of gamete size dimorphism between the sexes (anisogamy) from an ancestral gametic system with gametes of the same size in both mating types (isogamy). The nuclear–cytoplasmic conflict hypothesis has been one of the major theoretical hypotheses for the evolution of anisogamy. It proposes that anisogamy evolved as an adaptation for preventing nuclear–cytoplasmic conflict by minimizing male gamete size to inherit organelles uniparentally. In ulvophycean green algae, biparental inheritance of organelles is observed in isogamous species, as the hypothesis assumes. So we tested the hypothesis by examining whether cytoplasmic inheritance is biparental in Monostroma angicava , a slightly anisogamous ulvophycean that produces large male gametes. We tracked the fates of mitochondria in intraspecific crosses with PCR-RFLP markers. We confirmed that mitochondria are maternally inherited. However, paternal mitochondria enter the zygote, where their DNA can be detected for over 14 days. This indicates that uniparental inheritance is enforced by eliminating paternal mitochondrial DNA in the zygote, rather than by decreasing male gamete size to the minimum. Thus, uniparental cytoplasmic inheritance is achieved by an entirely different mechanism, and is unlikely to drive the evolution of anisogamy in ulvophyceans.

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A comparative test of the gamete dynamics theory for the evolution of anisogamy in Bryopsidales green algae

Cited by 6 publications

References 45 publications

Fossil-calibrated inference of divergence times among the Volvocine algae enables reconstruction of the steps that led to differentiated multicellularity

Fossil-calibrated inference of divergence times among the Volvocine algae enables reconstruction of the steps that led to differentiated multicellularity

Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae

Mitochondrial uniparental inheritance achieved after fertilization challenges the nuclear–cytoplasmic conflict hypothesis for anisogamy evolution

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