The effects of sexual reproduction on the evolution of multicellularity in green algae

Abstract

Nearly all multicellular organisms reproduce sexually, whereas asexual reproduction is predominant in unicellular species. However, it is unclear why we see such a tight co-occurrence between multicellularity and sex. Here, we investigate the effect sexual reproduction has on the evolution of multicellularity in the green algae, Chlamydomonas reinhardtii, specifically on the variation and novel phenotypes it creates through recombination. C. reinhardtii is facultatively multicellular, forming groups in response to environmental factors, such as temperature. We directly compare rates of multicellularity (% of cells in groups with more than four cells) between asexually reproducing parents and their sexually produced offspring under two temperature treatments (room-temperature, 20°C, and cold, 8.5°C). We found that multicellularity differed greatly between strains and that this variation was heritable. Sexual reproduction did not lead to a general increase in variation in rates of multicellularity, but did occasionally lead to offspring with more extreme rates of multicellularity. Offspring rates of multicellularity under cold conditions were highly variable across different parental crosses with genotype-by-genotype (G×G) interactions explaining a large fraction of the variation in rates of multicellularity. Lastly, we tested whether multicellularity has an effect on fitness (as estimated from population growth rates), and found that more multicellular lineages had lower fecundity under control conditions, but not under cold conditions. Together, our results suggest that under temperature stress, through increased variation in rates of multicellularity and exploration of novel phenotypic space, sexual reproduction, through recombination of epistatically interacting genes, has the potential to initiate the evolution of multicellularity.

Popular Abstract

Sex: crucial for becoming multicellular?

As Ella Fitzgerald and Louis Armstrong already sang in their hit "Let's do it", sex is ubiquitous all around us. Plants, animals, fungi, they all partake in sexual reproduction, at least once every so often. Unicellular species however most often reproduce clonally, without sex, they just split in two. Why is sex so common in multicellular species?

Sex involves the coming together of two individuals, both contributing their genes to a single cell, to create new offspring. There's a lot of costs associated with sex, from finding a mate to the number of genes you pass on. In many ways, asexual reproduction, which involves splitting yourself in two, is much easier and allows you to have more offspring. However, there’s also many benefits to sex. One of these is that sex creates novelty. Think of your own family for a second: you're not exactly the same as your parents or siblings, maybe you’re taller or more sociable. These new characters (phenotypes) arise via recombination: when your parents mated, their genes got mixed up. That's why you might have your mother's eyes but your father's smile. Without this recombination, we wouldn't have had the huge diversity in animals and plants, as variation in a trait is crucial for a trait to evolve. Perhaps this recombination during sex was crucial for creating the first multicellular organisms? If single cells were just copying themselves asexually all the time, obligate multicellularity might never have evolved.

Sticky kids
To investigate this we looked at algae, specifically Chlamydomonas reinhardtii. This algae can reproduce sexually but can also replicate itself asexually. Normally it lives on its own as single cells, but sometimes after replicating, the daughter cells stick together creating groups of cells, it is facultatively multicellular. We picked out 12 individual strains of algae, 6 "males" and 6 "females”. Some of these prefer to live the solitary life, while others are found sticking together more often. This “stickiness” is an early form of multicellularity, but is not set in stone with individual strains sometimes being more unicellular and more multicellular at other times. We let these algae mate with each other to see if their offspring were more variable in their multicellularity than their parents. Just like in humans, you might be super sociable, but your siblings might like being on their own, while your parents are somewhere in between. We did not really see this, offspring were generally not more variable than their parents. We did see that offspring were sometimes more multicellular than their parents: in one cross, while parents were in groups for a maximum of around 25% of the time at most, one of their offspring was living in groups around 75% of the time. If the parents would just have been cloning themselves, we would likely never have seen such high rates of multicellularity.

So why were offspring not more variable than each of their parents? For this, we looked at whether there was epistasis, which means that the effect of a gene is dependent on the other genes you carry with you. We indeed found evidence for this. To put this in algae terms, if an algae offspring received a gene from their father that creates the glue to stick together, but the gene from their mother makes them want to break free, they’ll never stick together. With a different mother, that also has sticky genes, the paternal glue genes might have caused the kids to always stick together. This tells us that multicellularity is determined by multiple genes. Second, it can explain how one offspring can be very multicellular while their parents were not: the genes from their parents worked in synergy to provide a super-sticky algae! Through my research, I have shown that sex can lead to more multicellular algae than would happen under asexual reproduction. Such algae might later completely lose the ability to live on their own, leading to obligate multicellularity. Sex may also have assisted in acquiring other characteristics and reducing conflict in the multicellular groups, helping maintain cells with a social life.

Master’s Degree Project in Biology – Evolutionary Biology, 60 credits
Department of Biology, Lund University

Advisors: Charlie Cornwallis, Colin Olito,
Department of Biology, Lund University

• author: Groenendal, Mart W. A.
• supervisor: Charlie Cornwallis; Colin Olito
• organization: Degree Projects in Biology
• course: BION03 20232
• year: 2024
• type: H2 - Master's Degree (Two Years)
• subject: Biology and Life Sciences
• language: English
• id: 9176998
• date added to LUP: 2024-10-23 15:02:26
• date last changed: 2024-10-23 15:02:26