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. 2014 Mar 3;14(1):37.
doi: 10.1186/1471-2148-14-37.

New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy

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New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy

Hisayoshi Nozaki et al. BMC Evol Biol. .

Abstract

Background: The evolution of oogamy from isogamy, an important biological event, can be summarized as follows: morphologically similar gametes (isogametes) differentiated into small "male" and large "female" motile gametes during anisogamy, from which immotile female gametes (eggs) evolved. The volvocine green algae represent a model lineage to study this type of sex evolution and show two types of gametic unions: conjugation between isogametes outside the parental colonies (external fertilization during isogamy) and fertilization between small motile gametes (sperm) and large gametes (eggs) inside the female colony (internal fertilization during anisogamy and oogamy). Although recent cultural studies on volvocine algae revealed morphological diversity and molecular genetic data of sexual reproduction, an intermediate type of union between these two gametic unions has not been identified.

Results: We identified a novel colonial volvocine genus, Colemanosphaera, which produces bundles of spindle-shaped male gametes through successive divisions of colonial cells. Obligately anisogamous conjugation between male and female motile gametes occurred outside the female colony (external fertilization during anisogamy). This new genus contains 16- or 32-celled spheroidal colonies similar to those of the volvocine genera Yamagishiella and Eudorina. However, Colemanosphaera can be clearly distinguished from these two genera based on its sister phylogenetic position to the enigmatic flattened colonial volvocine Platydorina and external fertilization during anisogamy. Two species of Colemanosphaera were found in a Japanese lake; these species are also distributed in European freshwaters based on a published sequence of an Austrian strain and the original description of Pandorina charkowiensis from Ukraine.

Conclusions: Based on phylogeny and morphological data, this novel genus exhibits a missing link between Platydorina and the typical spheroidal colonial volvocine members such as Pandorina or Yamagishiella. Considering the external obligate anisogamy, oogamy evolution may have been preceded by the transition from external to internal fertilization during anisogamy within the volvocine green algae.

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Figures

Figure 1
Figure 1
Light microscopy of vegetative colonies of two species of Colemanosphaera. (A)-(D) C. charkowiensis (Korshikov) Nozaki et al. comb. nov. 2013-0615-IC-7. (A), (B) Two views of a 32-celled colony shown at the same magnification. (A) Surface view. (B) Optical section. (C), (D) Two views of cells shown at the same magnification. (C) Surface view showing contractile vacuoles (cv) distributed in only the anterior end of cells. (D) Optical section. Note multiple pyrenoids (p) and strong longitudinal striations in the chloroplast periphery. (E)-(I) C. angeleri Nozaki sp. nov. 2010-0126-1. (E), (F) Two views of a 32-celled colony shown at the same magnification. (E) Surface view. (F) Optical section. (G)-(I) Three views of cells showing contractile vacuoles (cv) and pyrenoids (p), shown at the same magnification throughout.
Figure 2
Figure 2
Bayesian inference (BI) tree of the Volvocaceae based on the chloroplast five genes. For details of the methods, see the Methods Section. Branch lengths are proportional to the genetic distances, which are indicated by the scale bar above the tree. Numbers on the left, middle, or right side at the branches represent posterior probabilities (PP) of BI (≥0.95), bootstrap values (≥50%, based on 1,000 replicates) obtained with the maximum likelihood and maximum parsimony analyses, respectively. Asterisks at the branches indicate 1.00 PP and 100% bootstrap values by the two methods.
Figure 3
Figure 3
Light microscopy of sexual reproduction in Colemanosphaera charkowiensis (Korshikov) Nozaki et al. comb. nov. (A), (B), (E)-(L) 2013-0615-IC-3x4x7. (C), (D) 2010-0713-E5. (A), (B) Sperm packets (bundles of male gametes) shown at the same magnification. (C), (D) Male gametes shown at the same magnification. Note cytoplasmic protrusion (asterisk) near the base of the flagella (f). (E)-(K) Successive stages of male and female gamete release and conjugation. Note male gamete (arrow) fusing with female gamete. (E)-(H) Shown at the same magnification throughout. (I)-(K) Shown at the same magnification throughout. (L) Mature aplanozygotes.
Figure 4
Figure 4
Maximum likelihood (ML) tree of two species of Colemanosphaera and an Austrian strain (ASW05157) based on internal transcriber spacer region of nuclear ribosomal DNA. For details of the methods, see the Methods Section. Branch lengths are proportional to the genetic distances, which are indicated by the scale bar above the tree. Numbers on the left or right side at the branches represent bootstrap values (≥50%, based on 1,000 replicates) obtained with the ML and maximum parsimonious analyses, respectively.
Figure 5
Figure 5
Diagram showing phylogeny and evolution of sexual reproduction characteristics within the colonial volvocine greens. Based on the present study.

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