Alternative evolution of a spheroidal colony in volvocine algae: developmental analysis of embryogenesis in Astrephomene (Volvocales, Chlorophyta)

Abstract

BackgroundVolvocine algae, which range from the unicellular Chlamydomonas to the multicellular Volvox with a germ–soma division of labor, are a model for the evolution of multicellularity. Within this group, the spheroidal colony might have evolved in two independent lineages: Volvocaceae and the goniacean Astrephomene. Astrephomene produces spheroidal colonies with posterior somatic cells. The feature that distinguishes Astrephomene from the volvocacean algae is lack of inversion during embryogenesis; the volvocacean embryo undergoes inversion after successive divisions to orient flagella toward the outside. The mechanisms of inversion at the molecular and cellular levels in volvocacean algae have been assessed in detail, particularly in Volvox carteri. However, embryogenesis in Astrephomene has not been subjected to such investigations.ResultsThis study relied on light microscopy time-lapse imaging using an actively growing culture of a newly established strain to conduct a developmental analysis of Astrephomene as well as to perform a comparison with the similar spheroidal volvocacean Eudorina. During the successive divisions involved in Astrephomene embryogenesis, gradual rotation of daughter protoplasts resulted in movement of their apical portions toward the embryonic posterior, forming a convex-to-spheroidal cell sheet with the apical ends of protoplasts on the outside. Differentiation of the posterior somatic cells from the embryo periphery was traced based on cell lineages during embryogenesis. In contrast, in Eudorina, the rotation of daughter protoplasts did not occur during successive cell divisions; however, inversion occurred after such divisions, and a spheroidal embryo was formed. Indirect immunofluorescence microscopy of basal bodies and nuclei verified this difference between Astrephomene and Eudorina in the movement of embryonic protoplasts.ConclusionsThese results suggest different tactics for spheroidal colony formation between the two lineages: rotation of daughter protoplasts during successive cell divisions in Astrephomene, and inversion after cell divisions in Eudorina. This study will facilitate further research into the molecular and genetic mechanisms of the parallel evolution of the spheroidal colony in volvocine algae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0794-x) contains supplementary material, which is available to authorized users.

The evolution of sexes: A specific test of the disruptive selection theory

“…Multicellularity evolved at least three times in the TGV clade from a colonial ancestor: once in the Astrephomene lineage, once in the clade containing Volvox globator, and once in the clade containing the remaining Volvox species plus Pleodorina and Eudorina . These origins of multicellularity are consistent with a previous study (Herron et al., ) and are supported by having different developmental patterns (Hallmann, ; Yamashita et al., ). Anisogamy evolved at least twice in this phylogeny, once in the lineage leading to clade including the colonial Platydorina caudata and the related multicellular Volvox species, and once in the lineage leading to the colonial Eudorina and the related multicellular Pleodorina and Volvox .…”

“…A single origin is used to maintain consistency with the more detailed study of the evolution of multicellularity by Herron, Hackett, Aylward, and Michod (). The three origins of multicellularity in the entire tree are supported by each multicellular clade exhibiting a distinct form of development (Hallmann, ; Yamashita et al., ). The other exception to unambiguous mappings is the origin of oogamy in the clade containing Volvox tertius and Volvox aureus .…”

The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability

“…At the close of this discussion, it is meet to briefly dwell on questions of more evolutionary flavour: all genera of Volvocaceae and its sister group Goniaceae—with the exception of the single genus Astrephomene [ 79 ]—display some form of inversion [ 42 ]. There is a general trend among these genera for complexity of inversion to increase with cell number, enabling comparative studies of the evolution of this complexity [ 49 ].…”

Embryogenesis of flattened colonies implies the innovation required for the evolution of spheroidal colonies in volvocine green algae

“…The evolution of spheroidal colonies is thought to have occurred twice, in the ancestors of Astrephomene and in those of Volvocaceae [4–6]. The formation of spheroidal colonies during embryogenesis is based on different cellular mechanisms in the two lineages (Additional file 6: Figure S1) [7]. There are two extant lineages with ancestral flattened colonies, the genus Gonium and the family Tetrabaenaceae.…”