Fig. 2 from Lindsey et al. 2024.

Ross Lindsey, now working on his PhD with Frank Rosenzweig, has published a new paper in BMC Biology, “Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the Volvocine algae.”

Background

Throughout its nearly four-billion-year history, life has undergone evolutionary transitions in which simpler subunits have become integrated to form a more complex whole. Many of these transitions opened the door to innovations that resulted in increased biodiversity and/or organismal efficiency. The evolution of multicellularity from unicellular forms represents one such transition, one that paved the way for cellular differentiation, including differentiation of male and female gametes. A useful model for studying the evolution of multicellularity and cellular differentiation is the volvocine algae, a clade of freshwater green algae whose members range from unicellular to colonial, from undifferentiated to completely differentiated, and whose gamete types can be isogamous, anisogamous, or oogamous. To better understand how multicellularity, differentiation, and gametes evolved in this group, we used comparative genomics and fossil data to establish a geologically calibrated roadmap of when these innovations occurred.

Results

Our ancestral-state reconstructions, show that multicellularity arose independently twice in the volvocine algae. Our chronograms indicate multicellularity evolved during the Carboniferous-Triassic periods in Goniaceae + Volvocaceae, and possibly as early as the Cretaceous in Tetrabaenaceae. Using divergence time estimates we inferred when, and in what order, specific developmental changes occurred that led to differentiated multicellularity and oogamy. We find that in the volvocine algae the temporal sequence of developmental changes leading to differentiated multicellularity is much as proposed by David Kirk, and that multicellularity is correlated with the acquisition of anisogamy and oogamy. Lastly, morphological, molecular, and divergence time data suggest the possibility of cryptic species in Tetrabaenaceae.

Conclusions

Large molecular datasets and robust phylogenetic methods are bringing the evolutionary history of the volvocine algae more sharply into focus. Mounting evidence suggests that extant species in this group are the result of two independent origins of multicellularity and multiple independent origins of cell differentiation. Also, the origin of the Tetrabaenaceae-Goniaceae-Volvocaceae clade may be much older than previously thought. Finally, the possibility of cryptic species in the Tetrabaenaceae provides an exciting opportunity to study the recent divergence of lineages adapted to live in very different thermal environments.

Lindsey, C. R.; A. H. Knoll, M. D. Herron, and F. Rosenzweig. 2024. Fossil-calibrated molecular clock data enable reconstruction of steps leading to differentiated multicellularity and anisogamy in the volvocine algae. BMC Biology 22:79. doi: 10.1186/s12915-024-01878-1.

The Evolution of Multicellularity, co-edited with Peter Conlin and Will Ratcliff, has been published by CRC Press. It’s available on Amazon, but cheaper to order direct, and for the time being you can save 20% with discount code FLA22 (I don’t know how long that will last).

The goal of this book is to provide an overview of the evolution of multicellularity: the types of multicellular groups that exist, their evolutionary relationships, the processes that led to their origins and subsequent evolution, and the conceptual frameworks in which their evolution is understood. In four main sections, the contributors review the philosophical issues and theoretical approaches to understanding the evolution of multicellularity, the evolution of aggregative multicellularity, the evolution of clonal multicellularity, and the evolution of multicellular life cycles and development. While the subject is too broad to cover in a truly comprehensive way, the contributors have done an outstanding job of synthesizing the critical information on their respective topics. We hope that this book will serve as a starting point for readers interested in the evolution of multicellularity, a reference for researchers on the subject, and a jumping-off point to stimulate future research.

The publisher has put pretty strict limits on what we can share (they want to sell books, after all), so I won’t be posting a downloadable version (I don’t, in fact, have one). However, the Foreword and Chapter 1 (together) can be downloaded for free, and some of the authors posted preprints of their chapters (which the publisher allowed). I have linked to these in the table of contents below. If I learn of others, I’ll update this post.

I’m biased, of course, but I really do think the authors have done an outstanding job with their respective chapters. I hope you think so, too!

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Jim Umen and I have published an article in the newest issue of Annual Review of Genetics. We review some green algae that are or have the potential to be models for the evolution of multicellularity, including Volvox, UlvaChara, and Caulerpa. Transitions from unicellular to multicellular (or, in the case of Caulerpa, giant, multinucleate unicellular) have been frequent and varied within the green algae, and we argue that studying diverse examples is necessary to understand how and why these transitions have taken place.

Abstract:

The repeated evolution of multicellularity across the tree of life has profoundly affected the ecology and evolution of nearly all life on Earth. Many of these origins were in different groups of photosynthetic eukaryotes, or algae. Here, we review the evolution and genetics of multicellularity in several groups of green algae, which include the closest relatives of land plants. These include millimeter-scale, motile spheroids of up to 50,000 cells in the volvocine algae; decimeter-scale seaweeds in the genus Ulva (sea lettuce); and very plantlike, meter-scale freshwater algae in the genus Chara (stoneworts). We also describe algae in the genus Caulerpa, which are giant, multinucleate, morphologically complex single cells. In each case, we review the life cycle, phylogeny, and genetics of traits relevant to the evolution of multicellularity, and genetic and genomic resources available for the group in question. Finally, we suggest routes toward developing these groups as model organisms for the evolution of multicellularity.

Umen, J. & M.D. Herron. 2021. Green algal models for multicellularity. Annual Review of Genetics  55:603-632. doi: 10.1146/annurev-genet-032321-091533 Free e-print

Postdoc Kimberly Chen has published a lay summary of our recent Scientific Reports paper, in which we showed that predation can drive the evolution of multicellularity in the green alga Chlamydomonas:

Multicellular life is one of the most astonishing wonders on Earth, but why and how does it arise in the first place, and at what cost? To help answer these questions, we exposed single-celled algae to predators and watched them evolve into multicellular life. Within a year, they had formed groups of cells to avoid being eaten – but at a price.

Chen, I-C. K. & M. D. Herron. 2019. Predators drive the evolution of multicellularity. The Science Breaker 257. doi: 10.25250/thescbr.brk257

A new paper describing the results of a yeast evolution experiment has been published in Evolution. Jordan Gulli exposed nascent multicellular “snowflake yeast” to an environment in which solitary multicellular clusters experienced low survival. In response, snowflake yeast evolved to form cooperative groups composed of thousands of multicellular clusters.

Gulli et al. 2019 Fig. 2
Figure 2 from Gulli et al. 2019. Evolution of proteinaceous aggregates that bind many multicellular clusters. When subjected to strong settling selection, snowflake yeast evolved to form cooperative aggregates composed of hundreds of clusters (A). A composite image (B) reveals the aggregates are composed of both protein (C, green, Qubit fluorescent protein stain) and DNA (D, red, propidium iodide). Cells embedded within the aggregate are shown in blue (E, Cell Tracker Blue). Scale bars are 500 μm.

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Our Director of Communications, Maureen Rouhi, has written a press release to accompany the new Scientific Reports paper, “De novo origins of multicellularity in response to predation.”

Coauthors currently at Georgia Tech in front of the Ramblin’ Wreck (left to right): Kimberly Chen, Will Ratcliff, Frank Rosenzweig, and me. Photo by Jennifer Pentz. Not shown: Josh Borin, Jacob Boswell, Jillian Walker, Alex Knox, and Maggie Boyd.

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A new paper describing the results of a microbial evolution experiment has been published in Scientific Reports. Predation by the filter-feeding predator Paramecium tetraurelia drove the evolution of simple multicellular structures in the green alga Chlamydomonas reinhardtii:

Herron et al. 2019 Fig. 2
Figure 2 from Herron et al. 2019. Depiction of C. reinhardtii life cycles following evolution with (B2, B5) or without (K1) predators for 50 weeks. Categories (A–D) show a variety of life cycle characteristics, from unicellular to various multicellular forms. Briefly, A shows the ancestral, wild-type life cycle; in B this is modified with cells embedded in an extracellular matrix; C is similar to B but forms much larger multicellular structures; while D shows a fully multicellular life cycle in which multicellular clusters release multicellular propagules. Representative microscopic images of each life cycle category are at the bottom (Depicted strain in boldface).

From the abstract:

Here we show that de novo origins of simple multicellularity can evolve in response to predation. We subjected outcrossed populations of the unicellular green alga Chlamydomonas reinhardtii to selection by the filter-feeding predator Paramecium tetraurelia. Two of five experimental populations evolved multicellular structures not observed in unselected control populations within ~750 asexual generations. Considerable variation exists in the evolved multicellular life cycles, with both cell number and propagule size varying among isolates. survival assays show that evolved multicellular traits provide effective protection against predation. These results support the hypothesis that selection imposed by predators may have played a role in some origins of multicellularity.

Herron MD, Borin JM, Boswell JC, Walker J, Knox CA, Boyd M, Rosenzweig F, Ratcliff WC. 2019 De novo origins of multicellularity in response to predation. Sci. Rep. 9, 2328. (doi: 10.1038/s41598-019-39558-8)

A new paper using analytical and simulation models to explore the relationships between particle-level heritability and collective-level heritability during major transitions has been published in BMC Biology:

Herron et al. 2018 Figure 3
Figure 3 from Herron et al. 2018.  Relative heritability of four collective-­level traits to cell-­level heritability for size.

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The paper describing the genetics of the multicellular Chlamydomonas reinhardtii strain that evolved in response to selection on settling rate is published in Royal Society Open Science:

Figure 3 from Herron et al. 2018. Results of phylostratigraphy analysis of differentially expressed genes. The y-axis represents the log odds of the observed degree of over/underrepresentation relative to genome-wide frequencies. The Bonferroni-corrected p-values result from a hypergeometric test (α = 0.0025, equivalent to a false discovery rate of 1%) performed in GeneMerge v. 1.4. ‘n.s.’, not significant.

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