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.
At the Evolution of Complex Life conference that took place here in Atlanta last month, László Nagy talked about some of his work with fungi. As it turns out, fungi are even weirder than I thought.
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:
Figure 1A from Nagy et al. 2018. The phylogenetic distribution of complex multicellularity in fungi. Green dots indicate lineages with known complex multicellular representatives. Images courtesy of Renee Lebeuf, Cimon Jules, George Rogers, Bálint Dima and László G. Nagy. Pictures of Modicella and Endogone (bottom right) are from Smith et al. (2013) and Yamamoto et al. (2015).
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:
Figure 5 from Nagy et al. 2018. Alternative phylogenetic models for the recurrent origins of complex multicellularity in fungi. Gains and losses of complex multicellularity across fungi under two contrasting models are shown by vertical blue and red bars, respectively. The model implying convergence requires 8–11 independent origins to explain the phylogenetic distribution of complex multicellular fungi, whereas a model implying a single origin requires one gain and >16 losses. Clades containing complex multicellular species are marked by pie charts with the blue section corresponding to the estimated fraction of complex multicellular species.
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.
Stable links:
Cock JM et al. 2010 The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465, 617–621. (doi:10.1038/nature09016)
Lukjancenko O, Wassenaar TM, Ussery DW. 2010 Comparison of 61 Sequenced Escherichia coli Genomes. Microb. Ecol. 60, 708–720. (doi:10.1007/s00248-010-9717-3)
Nagy LG. 2017. Evolution: complex multicellular life with 5,500 genes. Curr. Biol. 27, R609–R612. (doi:10.1016/j.cub.2017.04.032)
Merchant SS et al. 2007 The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245–250. (doi:10.1126/science.1143609)
Nagy LG, Kovács GM, Krizsán K. 2018. Complex multicellularity in fungi: evolutionary convergence, single origin, or both? Biol. Rev. 93, 1778–1794. (doi:10.1111/brv.12418)
Nguyen TA, Cissé OH, Yun Wong J, Zheng P, Hewitt D, Nowrousian M, Stajich JE, Jedd G. 2017. Innovation and constraint leading to complex multicellularity in the Ascomycota. Nat. Commun. 8. (doi:10.1038/ncomms14444)
Prochnik SE et al. 2010 Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329, 223–226. (doi:10.1126/science.1188800)
Tarnita CE, Taubes CH, Nowak MA. 2013 Evolutionary construction by staying together and coming together. J. Theor. Biol. 320, 10–22. (doi:10.1016/j.jtbi.2012.11.022)
Wow! I have shivers.
A question would be how common a reversion to unicellularity is in the other multicellular groups. Myxozoa would have been a candidate, but current knowledge is more ambiguous. Transmissible cancers in bivalves are a possibility – are the propagules unicellular? are the tumours multicellular or colonial?
Another question would be how does character assignment on the fungal tree change as you change the ratio of the probabilities of transition in either direction? (You show the trees for the extreme values, but what about the intermediate values?)
“Fungi are weird”
Fungi say the same thing about humans. : )