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The multicellular green alga Volvox carteri and its morphologically diverse close relatives (the volvocine algae) are well suited for the investigation of the evolution of multicellularity and development. We sequenced the 138-mega-base pair genome of V. carteri and compared its approximately 14,500 predicted proteins to those of its unicellular relative Chlamydomonas reinhardtii. Despite fundamental differences in organismal complexity and life history, the two species have similar protein-coding potentials and few species-specific protein-coding gene predictions. Volvox is enriched in volvocine-algal-specific proteins, including those associated with an expanded and highly compartmentalized extracellular matrix. Our analysis shows that increases in organismal complexity can be associated with modifications of lineage-specific proteins rather than large-scale invention of protein-coding capacity.

The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved ‘snowflake’ yeast and the green alga Volvox carteri . We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This ‘entropic’ cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.

Flows generated by ensembles of flagella are crucial to development, motility and sensing, but the mechanisms behind this striking coordination remain unclear. We present novel experiments in which two micropipette-held somatic cells of Volvox carteri, with distinct intrinsic beating frequencies, are studied by high-speed imaging as a function of their separation and orientation. Analysis of time series shows that the interflagellar coupling, constrained by lack of connections between cells to be hydrodynamical, exhibits a spatial dependence consistent with theory. At close spacings it produces robust synchrony for thousands of beats, while at increasing separations synchrony is degraded by stochastic processes. Manipulation of the relative flagellar orientation reveals in-phase and antiphase states, consistent with dynamical theories. Flagellar tracking with exquisite precision reveals waveform changes that result from hydrodynamic coupling. This study proves unequivocally that flagella coupled solely through a fluid can achieve robust synchrony despite differences in their intrinsic properties. Sperm cells, as well as many bacteria and algae, propel themselves using whip-like appendages called flagella. Similar, shorter structures called cilia are also found on the surface of many cells, where they perform roles such as moving liquids over the cell. Each cilium or flagellum beats at its own characteristic rhythm, but there are many situations where cilia or flagella must synchronize their beating with other nearby cells. For example, an egg cell is swept along the Fallopian tube by the coordinated beating of the cilia lining the tube. Bull sperm cells are also known to synchronize the beating of their flagella when swimming close to each other. It has been suggested that the movement of the fluid surrounding the beating flagella could be the source of this synchronization. Experiments have produced results that match up with mathematical models describing this fluid movement. However, these experiments have often been designed in ways that didn’t fully exclude other possible sources of synchronization, such as chemical signalling, or—for flagella located on the same cell—a physical connection between the flagella. To overcome this shortcoming, Brumley et al. used high-speed imaging to watch the flagella of cells of Volvox carteri—a species of green alga—that were separated so that they could only communicate through the movement of the fluid around them. The flagella were still able to synchronize their beating, even when the two flagella naturally beat at substantially different rates. The distance between the flagella affects how well the beating synchronizes. When close together, the flagella can lock into the same rhythm for thousands of beats. However, as they move further apart, random biochemical fluctuations within the cells reduce the extent to which the flagella can synchronize. The flagella can also synchronize so that they move in the same direction at the same time, or in opposite directions, depending on how they are oriented relative to each other. Moreover, the results confirm that the fluid flow produced by a beating flagellum is sufficient to synchronize the beating of other nearby flagella.

Volvox sect. Volvox is a group of green algae with unique morphological features (thick cytoplasmic bridges between somatic cells and spiny zygote walls) and a worldwide distribution. Despite research interest in the diversity of organisms in ancient lakes, Volvox sect. Volvox from ancient lakes worldwide has not been identified to the species level. Here, we established clonal cultures of two species of this group originating from Lake Biwa, an ancient lake in Japan, and performed identification based on morphological and molecular data. One was identified as Volvox kirkiorum based on the nuclear ribosomal DNA internal spacer region (ITS) sequence, bisexual (monoicous or monoecious) spheroids, and zygote morphology. The other showed genetic separation from related species based on the secondary structure of the ITS and results of phylogenetic analysis of a combined data set from the nuclear actin gene, ITS, and two plastid genes (large subunit of RuBisCO and photosystem II CP43 apoprotein gene); it represented a new phylogenetic lineage within Volvox sect. Volvox , suggesting possible endemism in Lake Biwa. This species produced bisexual spheroids with different zygote morphology and zygote number from other species with bisexual spheroids in Volvox sect. Volvox . Therefore, Volvox biwakoensis Nozaki et H. Yamaguchi sp. nov. is described herein. This is the first endemic species of the genus Volvox described from an ancient lake.

Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals.

Volvox rousseletii is a dioecious species belonging to Volvox sect. Volvox that has previously only been found in Africa. During field surveys in a large dam lake (Lake Sagami) in Kanagawa Prefecture, central Japan, we encountered a Volvox sect. Volvox species that produces dioecious sexual spheroids in the water column. Although sexual induction of this species in culture did not produce adequately well-developed sexual spheroids for species identification, molecular data directly obtained from field-collected sexual spheroids verified the identity of field-collected male and female sexual spheroids as well as cultured materials. Based on molecular and morphological data, the species was identified as V. rousseletii. This is the first record of a dioecious species of Volvox sect. Volvox in Japan.

Variability is emerging as an integral part of development. It is therefore imperative to ask how to access the information contained in this variability. Yet most studies of development average their observations and, discarding the variability, seek to derive models, biological or physical, that explain these average observations. Here, we analyse this variability in a study of cell sheet folding in the green alga Volvox, whose spherical embryos turn themselves inside out in a process sharing invagination, expansion, involution, and peeling of a cell sheet with animal models of morphogenesis. We generalise our earlier, qualitative model of the initial stages of inversion by combining ideas from morphoelasticity and shell theory. Together with three-dimensional visualisations of inversion using light sheet microscopy, this yields a detailed, quantitative model of the entire inversion process. With this model, we show how the variability of inversion reveals that two separate, temporally uncoupled processes drive the initial invagination and subsequent expansion of the cell sheet. This implies a prototypical transition towards higher developmental complexity in the volvocine algae and provides proof of principle of analysing morphogenesis based on its variability.

Combining spectral imaging with compressive sensing (CS) enables efficient data acquisition by fully utilizing the intrinsic redundancies in natural images. Current compressive multispectral imagers, which are mostly based on array sensors (e.g, CCD or CMOS), suffer from limited spectral range and relatively low photon efficiency. To address these issues, this paper reports a multispectral imaging scheme with a single-pixel detector. Inspired by the spatial resolution redundancy of current spatial light modulators (SLMs) relative to the target reconstruction, we design an all-optical spectral splitting device to spatially split the light emitted from the object into several counterparts with different spectrums. Separated spectral channels are spatially modulated simultaneously with individual codes by an SLM. This no-moving-part modulation ensures a stable and fast system, and the spatial multiplexing ensures an efficient acquisition. A proof-of-concept setup is built and validated for 8-channel multispectral imaging within 420~720 nm wavelength range on both macro and micro objects, showing a potential for efficient multispectral imager in macroscopic and biomedical applications.

Understanding the emergence and evolution of multicellularity and cellular differentiation is a core problem in biology. We develop a quantitative model that shows that a multicellular form emerges from genetically identical unicellular ancestors when the compartmentalization of poorly compatible physiological processes into component cells of an aggregate produces a fitness advantage. This division of labour between the cells in the aggregate occurs spontaneously at the regulatory level owing to mechanisms present in unicellular ancestors and does not require any genetic predisposition for a particular role in the aggregate or any orchestrated cooperative behaviour of aggregate cells. Mathematically, aggregation implies an increase in the dimensionality of phenotype space that generates a fitness landscape with new fitness maxima, in which the unicellular states of optimized metabolism become fitness saddle points. Evolution of multicellularity is modelled as evolution of a hereditary parameter: the propensity of cells to stick together, which determines the fraction of time a cell spends in the aggregate form. Stickiness can increase evolutionarily owing to the fitness advantage generated by the division of labour between cells in an aggregate.

This paper represents an attempt to unify data from various lines of Volvox research: developmental biology, biogeography, and evolution. Several species (such as Volvox carteri and Volvox spermatosphaera) are characterized by rapid divisions of asexual reproductive cells, which may proceed in darkness. By contrast, several other species (such as Volvox aureus, Volvox globator, and Volvox tertius) exhibit slow and light/dependent divisions. The transition from the former pattern of asexual life cycle to the latter one has occurred in three lineages of the genus Volvox. Since V. aureus (unlike V. carteri) is able to complete the life cycle at a short photoperiod (8 h light/16 h dark regime), it is reasonable to suggest that the abovementioned evolutionary transitions might have occurred as adaptations to short winter days in high latitudes under warm climate conditions in the deep past. In the case of the lineage leading to V. tertius + Volvox dissipatrix, the crucial reorganizations of asexual life cycle might have occurred between about 45 and 60 million years ago in relatively high latitudes of Southern Hemisphere.