All known complex life exists as cells - fluid compartments bounded by a membrane and containing genetic material. Most cells are reproductively distinct and in competition with their neighbours for space and resources. However, on several occasions single-celled organisms have evolved to co-operate, resulting in the segregation of reproductive and somatic cells. This had lead to the evolution of the main lineages of macroscopic multicellular life that visually dominate both the land and the seas.
The main multicellular groups that we see today are:
• Green algae, including plants
• Red and brown algae
When did multicellularity evolve?
It is difficult to judge when multicellularity evolved in these lineages for several reasons:
• Early forms lacked hard tissues such as bone, shell or cellulose and so rarely fossilise.
• Older fossils are likely to have been distorted or destroyed over time.
• It is difficult to differentiate colonial living from true multicellularity based on fossils.
• It is difficult to relate fossil structures to modern groups, or even prove that they are organic.
• Genetic comparisons using are hard to make between very distantly related groups due to convergent sequence evolution.
The further back in time you go the less reliable much of the fossil evidence becomes. However, it is clear that multicellular plants, animals and fungi existed over 500 million years ago. The tube-shaped fossil Grypania is thought to be a primitive alga (though some believe it could be a bacteria) and is found in rocks that are 2.1 billion years old.
How and why did multicellularity evolve?
Origin of the first cell types
Many unicellular organisms show different morphology and behaviour at during their life cycle; for example motile and mitotic stages, or haploid and diploid stages. It is thought that the first differentiated cell types of multicellular organisms were multiple cell states existing at the same time in a group of cells.
The different cell types within a multicellular organism contain the same DNA sequences; it is just the relative levels of expression of these genes that changes. This mirrors the case seen in unicellular organisms that express different genes during stages of their life cycle.
Evolution only favours mutations that increase the fitness of the individuals that carry them. For the evolution of multicellularity this presents a problem because the transition to multicellularity involves a change in the level of selection from individual cells to an individual made up of many cells.
A theory of the origins of multicellularity must therefore account, not only for the benefits of complex multicellularity, but also for the benefits of primitive grouping behaviour of cells and for a separation of a germ line from other somatic cells.
The main advantage of aggregation for non-differentiated groups of cells would have been defence. A ball of cells is safer from being engulfed by predatory cells, while a thin sheet of cells embedded in a secreted matrix can provide far greater adhesion than each cell could individually. This can be seen for example in bacterial biofilms, which are highly resistant to mechanical or chemical disruption. Another benefit of larger size is the maintenance of homeostasis.
At some point on the road to true multicellularity some cells in the group have to sacrifice their ability to reproduce so that others can, resulting in separate somatic and germ lines. This is a hard transition to explain through natural selection because a cell that divides less than another should be outcompeted and replaced by it. However, it is important to remember that selection does not act on a cell per se, but on the information in its genes. A cell is more closely related to the other cells in its group than those of another group. Therefore natural selection can favour a cell that reduces its own reproductive potential, so long as it increases the reproductive potential of its sister cells by a greater amount. This is known as kin selection.
Further increase in cell numbers in a multicellular organism allows greater sub-division of labour, such as specialised digestive or sensory cells. Cells can also be combined in particular structures to give rise to complex tissues, organs and organ systems. Some organ systems, such as the nervous system in animals, can allow complex and novel behaviours.
An increase in size can allow a greater foraging range. Large plants can search a wider area for sunlight, some animals can travel for many miles to find food, and some huge fungi can spread through acres of soil to digest detritus.
Physical mechanisms for the origin of multicellular life
There are three main hypotheses for the physical mechanism of the origin of multicellular life:
The Symbiotic Theory
The Coenocytial Theory
The Colonial Theory
This protist is an important model organism for studying the selective pressures and genetics of multicellularity. These cells usual exist as haploid individuals in the soil. When food is scarce the cells undergo either a social cycle or sexual cycle.
In a social cycle the cells aggregate and form a fruiting body, from which cells are shed as spores into the wind. In the sexual cycle, two cells of opposite mating types fuse and cannibalise the other cells, forming a macrocyst which undergoes meiosis and produces recombinant offspring cells.
It is interesting to note that the multicellular behaviour only occurs when food is scarce, as it is only then that the benefits of multicellularity outweigh the costs. In the social cycle, the cells that form the stalk of the fruiting body do not form spores and die, while in the sexual cycle the cannibalised cells also die. However, if the cells did not aggregate then the food would be used up and they would all perish. Unfortunately the complexities of the selective pressures are beyond the scope of this article.
This genus of freshwater green algae is of interest as a model system because it shows primitive multicellular traits that can be studied as proxies for the first multicellular plants and animals. It is estimated that Volvocine algae became colonial around 200 million years ago.
These organisms exist as hollow spherical colonies, which can contain tens of thousands of cells held together by an extracellular matrix. The cells show some specialisation, for example more developed light-sensing cells are found towards the anterior. Crucially, the colonies contain both somatic and germ cells.
Species of Volvox can be monoecious (with both male and female cells in the same individual) or dioecious (with separate male and female individuals). Daughter colonies are formed from the germ cells and are released from within the parental sphere as it disintegrates.
Important principles in complex multicellularity
Where did all the genes go?
One major surprise that emerged from the genome sequencing projects of the late 20th century was that the number of genes found in the human genome, and indeed of all animals, was far smaller than predicted. Early predictions were that the human genome would contain hundreds of thousands of genes. More recent estimates are for only 20,000 genes.
Further work has shown that, while the number of genes does not differ as much as expected, the gene regulatory networks (GRNs) are much more complex in multicellular organisms. In the same way that biochemical and physical properties are subdivided between the cells of a multicellular organism, so too is the expression of the genes.
With hindsight this is not so surprising. All organisms, whether just a single cell or one made up of trillions of cells, must perform the same basic functions – feeding, reproduction, metabolism, sensing, and excretion. It is the extensive gene regulation that is essential for generating the hundreds of cell types we see in many multicellular organisms.
Examples of important gene families in animal multicellularity
While it is rare to find a completely novel gene in a multicellular lineage that isn’t shared by its unicellular relatives, we do see expansion of particular gene families through gene duplication. Below are some examples of such groups in animals:
• Hox genes. These transcription factors are involved in antero-posterior patterning. They are expressed in a canonical manner in overlapping regions and give identity to different segments of the animal. A greater number of Hox genes means that more morphologically distinct segments can be produced.
• Intercellular signalling pathways. All cells receive and respond to signals from their environment. In a multicellular organism cells must also communicate extensively with each other to coordinate behaviours such as growth, development and enzyme secretion. We see, therefore, an expansion of signalling ligands and membrane receptions such as wnts, notch, FGFs, tyrosine kinase receptors and many others. These range from direct cell-cell signally to hormones that can signal across many metres. The “hippo” pathway is one that allows cells to sense the density of their neighbours, and is therefore important in controlling organ size.
• Adhesion molecules and extracellular matrix molecules. Cells have to be able to adhere to each other or else large organisms would fall apart. In animals we see a large number of cell adhesion complexes such as adherens junctions. Different adhesion proteins adhere to other specific proteins. Tissues and organ structures are maintained as separate populations through cells adhering to like cells.
Changes of scale
While the size of a single cell can vary greatly, multicellular organisms have a much greater capacity to evolve to achieve very large sizes. This is due to the constraints imposed by allometric scaling, where the magnitude of different properties of an object change at different rates relative to one another.
For example, the surface area of a sphere is equal to 4πr^2 while the volume is equal to (4/3)πr^3. Because the surface area is proportional to the radius squared, while the volume is proportional to the radius cubed, a 2-fold increase in the length of a sphere will lead to a 4-fold increase in the surface area and an 8-fold increase in the volume.
As the maximum rate of diffusion across a membrane is proportional to its surface area, while oxygen usage is roughly proportional to cell volume, the larger a cell gets the more difficult it becomes for it to acquire enough oxygen, carbon dioxide, or nutrients through its membrane. This is why the largest single cells are generally extremely flat.
Multicellular organisms are able to overcome these constraints through the formation of particular tissues, structures and organs made of different kinds of cells. For example:
• Respiration. Both animals and plants have tissues with very high surface area for gaseous exchange. In animals we find lungs, gills, or tracheal systems, while plant leaves contain spongy mesophyll.
• Circulation. To overcome the limits of diffusion within the body, many animals use a muscular pump to circulate fluid around the body. In mammals the heart is a complex pump and the blood flows in blood vessels in a double circulation system; first through the lungs and then through the rest of the body.
A fundamental principle of multicellularity is that not all cells get to reproduce. As a human, if you have 3 children then only 3 of your cells get to survive into the next generation. The rest of the trillions of cells in your body are destined to decay and die. Most of time these doomed cells quietly behave, because in doing their job they allow some germ cells, which carry the same genes as them, to survive. However, over time and due to exposure to environmental factors such as UV radiation, DNA mutations build up. These mutations can disrupt the regulatory mechanisms that prevent normal cells from proliferating out of control. This is called cancer, and can be thought of as a return to selfish behaviour.
Because cancers kill their host or die with them, the cancer cells only evolve within the body and lifetime of the individual that carries them. However it is interesting to note the rise of Devil Facial Tumour Disease (DFTD), a cancer that can be passed between Tasmanian Devils through biting. Here the cancerous cells act as a pathogen, they are independent from their hosts in terms of selection.
Note: Once a somatic cell line is established then its inability to survive and reproduce outside the body prevents defection being profitable (i.e. the relationship of somatic cells with their neighbours is synergistic – they cannot gain more from defection than co-operation). However, cancers still occur due to inevitable DNA damage during an animal’s lifespan. Selection at the level of the organism will tend to reduce the incidence of cancers to a certain extent, but as the incidence of most cancers increases with age, and older animals are more likely to have already reproduced, the selective pressure will be quite weak.
In addition, if a mutation reduces the incidence of cancer in the old, for example by reducing mitochondrial metabolism, but which would also decrease the fertility of the young, then this mutation will not be favoured by natural selection.
As mentioned, some bacteria form biofilms and cyanobacteria can form colonies with several different cell types. In general though, Prokaryotes (bacteria and archaebacteria) do not show large complex multicellular forms. There are several ideas as to why this might be the case: They lack organelles and so might lack the metabolic resources to maintain and copy a large genome. They also generally show less gene regulation than eukaryotic cells.
So the evolution of multicellularity occurred many times independently and the main multicellular lineages existed well over half a billion years ago. The benefits of multicellularity are increased size and increased efficiency through sub-division of labour. Multicellular organisms show large amounts of genetic regulation to restrict and control cell behaviour. Cancer is when mutations cause cells to behave in a selfish manner, much as single cells do. Prokaryotes show some simple multicellular forms, but it is not certain why there are no complex multicellular forms.
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