The first proposed criterion is that a unitary multicellular organism, unlike a colonial aggregation of unicellular organisms, must develop as a multicellular body and reproduce only after reaching a multicellular vegetative stage. On this definition, colonies formed by independently living cells, such as those in slime molds, myxobacteria and some algae, remain distinct from organisms whose life cycle obligatorily includes a multicellular phase. The author also treats multinucleate bodies that lack genuine cellular partitions, including those of some ciliates and protists, as nonmulticellular under the criterion.

The second criterion concerns how a multicellular body produces a daughter organism. Reproduction may be monocytic, when a new organism originates from one cell, such as a spore, zygote, gamete, parthenogenetic egg or totipotent somatic cell, or polycytic, when it originates from many cells through fragmentation, fission or budding. The review also emphasizes that sexual and asexual reproduction need not increase the number of individuals, and it treats parthenogenesis as a variant of sexual reproduction because the offspring develops from a specialized gamete. In plants, parthenogenesis is distinguished from other forms of apomixis in which embryos arise from cells other than the egg.

Based on the monocytic criterion, the review divides obligate multicellularity into protonemal, siphonoseptal and embryogenic forms. Protonemal multicellularity begins when a spore or zygote divides to form a filamentous protonema, with daughter cells growing after division; examples occur among bacteria and numerous algal and plant lineages. Siphonoseptal multicellularity begins with repeated nuclear divisions without cytoplasmic division, producing a multinucleate siphon that may later become partitioned by septa; the review identifies this pattern in green algae, yellow-green algae, fungi and fungus-like organisms. Some bodies that separate into cenocytes and later fuse are interpreted as colonies rather than multicellular organisms under this framework.

Embryogenic multicellularity is described as the most complex of the three forms. It develops through obligate accumulative oogamy or accumulative aplanosporia, in which the gamete or spore is larger than the ordinary cells of the maternal body, sometimes by hundreds or thousands of times in size. Palintomic divisions, in which nuclear and cytoplasmic division recur without intervening growth, or syntomic divisions, in which the cytoplasm is divided into numerous compartments, then produce an embryo or an asexual analogue termed an embryoid. The embryo depends on maternal nourishment or stored reserves until it begins an independent life. The review associates this form with all animals, higher-plant sporophytes and selected algal and plant life cycles.

Complex multicellular organisms with differentiated tissues and organs are described as developing through the embryogenic route. The author proposes that a large, structured egg and rapid cleavage help establish developmental organization, including predetermined cleavage and the formation of tissues and organs. No embryogenic multicellularity is identified among prokaryotes, although the review presents this as a probable evolutionary explanation rather than a directly tested mechanism. It attributes the absence partly to limited internal transport in prokaryotic cells, noting that their lack of an endoplasmic reticulum restricts diffusion-based transport and cell size. The large bacterium Thiomargarita namibiensis, reaching 0.75 millimetres in diameter, is exceptional because much of its interior is vacuolar and only a thin peripheral layer contains cytoplasm.

The review then considers a problem created by multicellular growth: male and female gametes must become available at the same place and time, but the larger parental bodies mature at different rates and immobile female gametes cannot travel far. It identifies three broad solutions: retaining eggs on or within the maternal organism until sperm arrive, synchronously releasing gametes into the external environment, or releasing them passively in response to shared environmental cues. The author argues that the first arrangement is the simplest and occurs in many archaic plants, fungi, algae and animals, including sponges, Trichoplax, dicyemids, orthonectids, Volvox and higher plants.

From this distribution, the review infers that internal fertilization, defined broadly to include fertilization on the maternal body, was ancestral to multicellular animals. It contrasts this inference with traditional diagrams of animals arising from choanoflagellate colonies, in which eggs are commonly shown entering open water. Archaic organisms lacked the coordinated nervous, muscular and reproductive structures used by later animals to eject gametes together, while rupture of an individual gametangium would not ensure simultaneous release among separate individuals. The proposed sequence instead places zygote division and early development within the colonial body, followed by formation of a mobile dispersal stage comparable to the synzoospore concept associated with Zakhvatkin and represented in modern sponges by a comparable larval role.

External fertilization is therefore treated as a later animal innovation enabled in cnidarians and ctenophores by nervous systems, gonads, musculature and, in some groups, reproductive ducts. The review also examines less coordinated alternatives, including water-flow-mediated gamete release in some demosponges and tidal synchronization in algae such as Fucus, where gametangia may dry at low tide and rupture after rewetting. It attributes the predominance of spore-based reproduction in plants to the difficulty of synchronizing gamete release, while noting that many flowering plants depend on animal pollinators and that some red algae use crustaceans for gamete transfer. The synthesis remains a broad review with variable evidence across taxonomically difficult groups, particularly fungi, algae and colonial organisms, and its evolutionary conclusions are explicitly dependent on the proposed reproductive definitions and classifications.

Subject of Research: Evolutionary origins of multicellularity and reproductive modes

Article Title: Ancient reproductive modes and criteria of multicellularity

Article References: Gavrilov-Zimin, I. A. (2023). Ancient reproductive modes and criteria of multicellularity. Comparative Cytogenetics, 17, 195-238. https://doi.org/10.3897/compcytogen.17.109671

Image Credits: AI Generated

DOI: 10.3897/compcytogen.17.109671

Keywords: multicellularity, evolutionary biology, reproductive modes, internal fertilization, viviparity, embryogenesis, protonemal multicellularity, siphonoseptal multicellularity, algae, animals, Ancient, reproductive

The study, published in Scientific Reports, was led by Professor Tamiki Komatsuzaki of Hokkaido University and focused on one of biology’s classic model organisms: the soil-dwelling amoeba Dictyostelium discoideum. This single-celled organism has long fascinated scientists because of what it does when food runs out. When bacteria are scarce and starvation sets in, the amoebas begin releasing a chemical signal called cyclic AMP, or cAMP. Neighboring cells detect the signal, respond by releasing more of it, and begin crawling toward its source. The result is a spreading chemical wave that sweeps across the colony, and the cells ride that wave toward one another, eventually assembling into a multicellular organism. This dramatic transformation helps the amoebas survive hostile conditions, and it recapitulates, in miniature, the kind of collective cell behavior that underlies development, immunity, and disease in animals.

For decades, researchers studying this aggregation process have faced a practical dilemma. One approach is to track individual cells, following each amoeba’s path frame by frame to see how it moves. That works reasonably well when cells are sparse, but it becomes nearly impossible once the cells crowd together during aggregation, when one cell’s trail blurs into its neighbor’s. A second approach is to measure the cAMP wave itself, determining the direction in which the chemical signal is traveling across the colony. But these two measurements have traditionally been carried out separately, leaving a crucial gap: no direct, simultaneous view of how the wave’s dynamics relate to what each individual cell is actually doing at that instant. “How individual cells read passing waves of chemical signals and translate them into coordinated group migration has been hard to pin down,” Komatsuzaki explained.

The new study closes that gap with an ingenious imaging strategy. The team used fluorescent microscopy to record both cell movement and cAMP levels at the same time, frame by frame, throughout the aggregation process. Then came the clever part. The researchers took their sharp images and deliberately blurred them by different amounts, creating a series of versions of the same footage at different spatial scales. To each blurred version, they applied a computational technique called particle image velocimetry, or PIV, a method originally developed in fluid dynamics to trace the flow of liquids and gases by tracking patterns of motion between successive frames.

The logic behind the multiscale blurring is elegant. In the sharpest images, the analysis picks out the trajectories of individual cells, revealing each amoeba’s personal path across the colony floor. But as the images are blurred more heavily, the small, jittery movements of individual cells average out, and what remains is the larger, smoother pattern of motion embedded in the colony as a whole — the signature of the cAMP wave itself. By analyzing the same footage at multiple scales simultaneously, the researchers could directly compare the dynamics of the chemical wave with the movements of individual cells throughout the entire experiment, without ever having to separate the cells physically or measure the wave by an independent method. The team describes the result as a multiscale Eulerian velocity vector field: a map of motion that captures both the fine-grained behavior of single cells and the coarse-grained behavior of the collective at every moment.

Armed with this technique, the researchers tracked the amoebas continuously from two to seventeen hours after the onset of starvation, covering the full arc of the aggregation process. What they saw was a strikingly consistent pattern of behavior. As a cAMP wave approaches a cell, the amoeba surges forward to meet it almost head-on, racing toward the incoming chemical signal. But when the wave crests and begins to recede, something unexpected happens: the cell does not reverse direction to chase the departing wave. Instead, its motion stays locked in the same direction it was already traveling, carrying it forward even as the signal moves away. Only after the wave has passed does the cell settle down, resting directionless in the trough of the wave until the next one arrives — at which point the entire cycle repeats.

Komatsuzaki offered a vivid analogy for this behavior. “It’s like watching a crowd of surfers paddle hard to catch a wave, ride it together, and then bob around waiting for the next one,” he said. The image is apt in more than spirit. Each amoeba behaves like a surfer who paddles furiously toward an incoming swell, gains momentum as the wave lifts, coasts in the same direction even after the wave has passed beneath, and then drifts idly until the next swell appears. No individual surfer needs to know where the shore is or what the other surfers are doing; the collective pattern emerges from each cell responding to the same passing wave at the same time.

The directional locking that the researchers observed is particularly significant for understanding the physics of chemotaxis, the process by which cells move toward chemical attractants. A naive expectation might be that a cell responding to a chemical gradient would simply follow the gradient, reversing course whenever the gradient reverses. The amoebas do something subtly different: their response to the wave is temporally asymmetric, with a strong forward surge during the rising phase of the wave and a persistence of motion during the falling phase. This asymmetry, repeated wave after wave across thousands of cells, is what allows the colony to funnel itself steadily inward toward the aggregation center. The large-scale cAMP waves, visualized in the team’s images as smooth ripples spreading across the colony, were found to move in a direction precisely opposite to the average direction of individual cell movement — a 180-degree reversal that becomes visible only when single-cell motion and wave motion are compared side by side.

According to the authors, the findings offer the first systematic map of how the amoebas’ collective behavior emerges from individual action. That map matters beyond the world of social amoebae. Because the imaging technique separates single-cell motion from collective motion in the same dataset, the team believes it could be applied to far more complex systems, including populations of mammalian cells. One tantalizing possibility is identifying which cells act as “leaders” — initiating and shaping the waves — and which act as “followers,” responding to signals generated by others. In immune responses, where swarming neutrophils and other cells coordinate their pursuit of pathogens, and in cancer biology, where collectively invading tumor cells move through tissue in coordinated groups, such leader-follower dynamics are thought to play a decisive role but are notoriously hard to disentangle.

The study also demonstrates the value of borrowing tools from other disciplines. Particle image velocimetry was developed to measure fluid flow in wind tunnels and rivers, not to watch amoebas crawl across a petri dish. By adapting it to multiscale biological imaging, the researchers have created a method that treats a cell colony like a flowing medium with structure at every scale — a perspective that may prove broadly useful for studying active matter, tissue mechanics, and developmental biology. For now, the work provides something biologists have long lacked: a direct, quantitative picture of the moment when solitary cells stop being solitary. In the starved amoeba’s simple act of paddling toward a chemical wave and riding it together with its neighbors lies a principle that echoes through wound healing, immune defense, and cancer spread — the principle that a crowd, given the right signal, can behave like a single living thing.

Subject of Research: Collective cell migration in Dictyostelium discoideum via cAMP chemotactic wave signaling

Article Title: Study reveals how individual cells ‘surf’ chemical waves to form a collective

Article References: Study reveals how individual cells ‘surf’ chemical waves to form a collective. (n.d.). Original publication

Image Credits: AI Generated

DOI: Not provided

Keywords: Dictyostelium discoideum, cAMP, chemotaxis, collective cell migration, particle image velocimetry, fluorescent imaging, Hokkaido University, multicellularity, cell signaling, immune response, cancer biology, Scientific Reports