I think about the evolution of multicellularity a lot, and I talk about it with colleagues. One of the things we talk about is what general principles we can infer from the many independent origins of multicellularity, for example in land plants, animals, red algae, brown algae, green algae, and fungi. Those are the groups that have evolved what we might call complex multicellularity, and one of the things we notice is that they all develop clonally; that is, they start out as a single cell, and when that cell divides, the daughter cells stick together. We notice that complex multicellularity has never evolved in species with aggregative development, when free-living cells come together to form a multicellular body, as they do in cellular slime molds and myxobacteria. Some aggregative developers have evolved a couple of different cell types, but all of the groups that have reached higher degrees of complexity develop by cell division and the products of cell division staying together. All, that is, except for fungi. Fungi are weird.
Fungi don’t really develop clonally in the way I’ve described, but they don’t really not develop clonally either. That’s because their cells don’t divide in the way we’re used to thinking about, through repeated rounds of mitosis. In mitosis, duplication of the genome is coupled to cell division: the chromosomes duplicate, they move to either end of the cell, then the cell divides. The chromosomes double, then they halve, so the daughter cells end up with the same number as the mother cell. That’s not how it works in fungi. Instead, they form filaments called hyphae (singular hypha) that grow at the tip. In some cases, partitions called septa (singular septum) form behind the growing tip, dividing the hyphae into individual cells. In some cases, no septa form, and each hypha is effectively one long, skinny cell with lots of nuclei (this is called a coenocyte).
So fungi don’t really develop by repeated rounds of cell division in the same sense that animals, plants, etc. do. Hyphae just grow, and they are divided into cells as sort of an afterthought, if they are divided into cells at all. Fungi with coenocytic (or aseptate) hyphae aren’t really even multicellular in the same sense as plants and animals are. Different people have different qualifications for what counts as multicellular, but it’s a stretch to call something multicellular that doesn’t have multiple cells. Fungi are weird.
For one thing, they weren’t content to evolve complex multicellularity once, as each of the well-behaved multicellular groups did. Noooo, they had to do it again and again, probably between eight and eleven times:
As usual in this sort of reconstruction, there’s some uncertainty in the exact number of times a trait (complex multicellularity in this case) has evolved, because there are multiple reconstructions possible. We tend to prefer the ones that require fewer changes, but there’s no hard and fast rule that says that the reconstruction requiring the fewest changes is always right. In this case, the inference of at least multiple independent origins or complex multicellularity seems sound, because it requires quite a few fewer changes than the scenario with a single origin:
The other unambiguously complex multicellular groups—animals, plants, and brown algae—are each monophyletic, so complex multicellularity probably evolved just once within each of these groups. If we want to call red and Ulvophyte green algae complex, that would be an additional two or three origins (reds are thought to have possibly represent two origins of multicellularity). So outside of the fungi, we might charitably say there have been around six independent origins of complex multicellularity; Nagy is saying there were more than that just in the fungi. Fungi are weird.
Weirder still, complex multicellularity in the fungi does not seem to require very many genes. In 2017, Nguyen and colleagues found that the genome of Neolecta irregularis, a complex multicellular fungus, contains only 5500 genes. To put that in perspective, most complex multicellular fungi have about twice that many genes. Volvox has around 14,500, Chlamydomonas just a few less, the filamentous brown alga Ectocarpus over 16,000, and the green alga Ulva (sea lettuce) around 13,000. 5500 is more typical of yeast, and not much more than some strains of E. coli (for example, E. coli 0157:H7 EC4486 has 5429). Fungi are weird.
Whenever we’re looking for commonalities among the various origins of complex multicellularity, commonalities that might suggest general principles for the transition to multicellular life, the fungi tend to either buck the pattern or provide an ambiguous fit. I have to admit that when fungi come up in these discussions, I have an unfortunate tendency to say “Who knows? Fungi are weird.” However, if László Nagy is right that complex multicellularity has arisen 8-11 times within the fungi, we might fairly say that the fungi include most origins of complex multicellularity. If so, maybe it’s not the fungi who are weird. If fungi truly include the majority of origins of complex multicellularity, fungi are the norm. Maybe it’s the rest of us that are weird.
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