Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae
Abstract 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 orga...
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BMC
2024-04-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-024-01878-1 |
| _version_ | 1797209096254914560 |
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| author | Charles Ross Lindsey Andrew H. Knoll Matthew D. Herron Frank Rosenzweig |
| author_facet | Charles Ross Lindsey Andrew H. Knoll Matthew D. Herron Frank Rosenzweig |
| author_sort | Charles Ross Lindsey |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-24T09:49:16Z |
| format | Article |
| id | doaj.art-d52a6c6456724831b55a3da49389555d |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-24T09:49:16Z |
| publishDate | 2024-04-01 |
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| series | BMC Biology |
| spelling | doaj.art-d52a6c6456724831b55a3da49389555d2024-04-14T11:29:26ZengBMCBMC Biology1741-70072024-04-0122112110.1186/s12915-024-01878-1Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algaeCharles Ross Lindsey0Andrew H. Knoll1Matthew D. Herron2Frank Rosenzweig3School of Biological Sciences, Georgia Institute of TechnologyDepartment of Organismic and Evolutionary Biology, Harvard UniversitySchool of Biological Sciences, Georgia Institute of TechnologySchool of Biological Sciences, Georgia Institute of TechnologyAbstract 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.https://doi.org/10.1186/s12915-024-01878-1MulticellularityCellular differentiationPhylogenyMolecular clockFossil calibrationAncestral state reconstruction |
| spellingShingle | Charles Ross Lindsey Andrew H. Knoll Matthew D. Herron Frank Rosenzweig Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae BMC Biology Multicellularity Cellular differentiation Phylogeny Molecular clock Fossil calibration Ancestral state reconstruction |
| title | Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae |
| title_full | Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae |
| title_fullStr | Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae |
| title_full_unstemmed | Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae |
| title_short | Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae |
| title_sort | fossil calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the volvocine algae |
| topic | Multicellularity Cellular differentiation Phylogeny Molecular clock Fossil calibration Ancestral state reconstruction |
| url | https://doi.org/10.1186/s12915-024-01878-1 |
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