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I primarily study various aspects of the evolutionary origins of multicellularity through a combination of experimental, theoretical, and comparative approaches. My main model systems are the volvocine algae (Volvox and kin) and their close unicellular relative, Chlamydomonas reinhardtii.

I am currently serving as a Program Director in the Evolutionary Processes Cluster in the National Science Foundation’s Division of Environmental Biology. Anything I post here or on social media reflects only my personal views and does not necessarily represent the views of my employer or the United States.

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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.

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I have been working as a rotating Program Director at the National Science Foundation for the last three and a half years, and I’m now a permanent Program Director in the Division of Environmental Biology‘s Evolutionary Processes Cluster. My lab at Georgia Tech is closed, and I am no longer employed there.

Anything I post here reflects only my personal views and does not necessarily represent the views of my employer or the United States.

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Seyed Alireza Zamani-Dahaj, Anthony Burnetti, Thomas C. Day, Peter J. Yunker, William C. Ratcliff, and I have published a new article in the latest issue of Genes. This follows up on our previous paper on heritability with an empirical test of some of its assumptions and predictions.

Abstract:

The major transitions in evolution include events and processes that result in the emergence of new levels of biological individuality. For collectives to undergo Darwinian evolution, their traits must be heritable, but the emergence of higher-level heritability is poorly understood and has long been considered a stumbling block for nascent evolutionary transitions. Using analytical models, synthetic biology, and biologically-informed simulations, we explored the emergence of trait heritability during the evolution of multicellularity. Prior work on the evolution of multicellularity has asserted that substantial collective-level trait heritability either emerges only late in the transition or requires some evolutionary change subsequent to the formation of clonal multicellular groups. In a prior analytical model, we showed that collective-level heritability not only exists but is usually more heritable than the underlying cell-level trait upon which it is based, as soon as multicellular groups form. Here, we show that key assumptions and predictions of that model are borne out in a real engineered biological system, with important implications for the emergence of collective-level heritability.

Zamani-Dahaj, S.A., A. Burnetti, T.C. Day, P.J. Yunker, W.C. Ratcliff, and M.D. Herron. 2023. Spontaneous emergence of multicellular heritability. Genes 14: 1635. doi: 10.3390/genes14081635

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Carl Simpson has authored a review of The Evolution of Multicellularity in Trends in Ecology & Evolution:

What features do all multicellular organisms share due to the common evolutionary problems and what differences are due to the constraints imposed by their unicellular ancestors? That is no easy task; not least because the answers to those questions span all biological disciplines. The new volume, The Evolution of Multicellularity edited by M.D. Herron et al., pulls together current thought on multicellularity from workers across a constellation of fields. This volume does a wonderful job covering the issues: from how to recognize multicellularity (Chapter 2), multilevel selection (Chapter 3), to multicellularity in fungi (Chapter 14), algae, and plants (Chapters 15 and 16).

Simpson, C., Coming together to understand multicellularity. Trends in Ecology & Evolution. doi https://doi.org/10.1016/j.tree.2023.01.007

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With the permission of the publisher and the authors, we have made internally peer-reviewed but unformatted drafts of all 18 chapters of The Evolution of Multicellularity available for download. Please note that there may be substantive differences between these pre-publication versions and the final book chapters.

The full book is available on Amazon and direct from the publisher in hardcover and ebook formats. The paperback is due out in 12-18 months, at which point the price of the ebook will drop.

Continue reading →

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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!

Continue reading →

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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, Ulva, Chara, 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

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Phylogeny

Ross Lindsey’s master’s thesis is now an article in BMC Biology, “Phylotranscriptomics points to multiple independent origins of multicellularity and cellular differentiation in the volvocine algae”:

We performed RNA sequencing (RNA-seq) on 55 strains representing 47 volvocine algal species and obtained similar data from curated databases on 13 additional strains. We then compiled a dataset consisting of transcripts for 40 single-copy, protein-coding, nuclear genes and subjected the predicted amino acid sequences of these genes to maximum likelihood, Bayesian inference, and coalescent-based analyses. These analyses show that multicellularity independently evolved at least twice in the volvocine algae and that the colonial family Goniaceae is not monophyletic. Our data further indicate that cellular differentiation arose independently at least four, and possibly as many as six times, within the volvocine algae.

Altogether, our results demonstrate that multicellularity and cellular differentiation are evolutionarily labile in the volvocine algae, affirming the importance of this group as a model system for the study of major transitions in the history of life.

Lindsey, C.R., F. Rosenzweig, & M.D. Herron. 2021. Phylotranscriptomics points to multiple independent origins of multicellularity and cellular differentiation in the volvocine algae. BMC Biology 19:182, part of the In the Light of Evolution series. doi: 10.1186/s12915-021-01087-0

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A new paper by former grad student Jacob Boswell, current grad student Ross Lindsey, Emily Cook, and Frank Rosenzweig is out in Biology Methods & Protocols (open access article):

Long-term preservation of laboratory strains of Chlamydomonas reinhardtii has historically involved either liquid nitrogen cryopreservation, which is expensive and labor intensive, or storage on agar plates, which requires frequent transfer to new plates, and which may leave samples susceptible to contamination as well as genetic drift and/or selection. The emergence of C. reinhardtii as a model organism for genetic analysis and experimental evolution has produced an increasing demand for an efficient method to cryopreserve C. reinhardtii populations. The GeneArt™ Cryopreservation Kit for Algae provides the first method for algal storage at −80°C; however, little is known about how this method affects recovery of different clones, much less polyclonal populations. Here, we compare postfreeze viability of clonal and genetically mixed samples frozen at −80°C using GeneArt™ or cryopreserved using liquid nitrogen. We find that the GeneArt™ protocol yields similar percent recoveries for some but not all clonal cultures, when compared to archiving via liquid N2. We also find that relative frequency of different strains recovered from genetically mixed populations can be significantly altered by cryopreservation. Thus, while cryopreservation using GeneArt™ is an effective means for archiving certain clonal populations, it is not universally so. Strain-specific differences in freeze–thaw tolerance complicate the storage of different clones, and may also bias the recovery of different genotypes from polyclonal populations.

Boswell, J., C. R. Lindsey, E. Cook, F. Rosenzweig, & M. D. Herron. 2021. Cryopreservation of clonal and polyclonal populations of Chlamydomonas reinhardtii. Biology Methods & Protocols 6:1-6. doi: 10.1093/biomethods/bpab011

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Congratulations to Charles “Ross” Lindsey for successfully defending his Master’s thesis, “Phylotranscriptomics of the volvocine algae: A model clade for the study of differentiated multicellularity,” on Friday, January 15, 2021!