A couple of weeks ago, I indulged in a little shameless self-promotion, writing about my new chapter on volvocine individuality in Biological Individuality, Integrating Scientific, Philosophical, and Historical Perspectives. Now two graduate students in the Michod lab at the University of Arizona, Erik Hanschen and Dinah Davison, have published their own take on volvocine individuality in Philosophy, Theory, and Practice in Biology (“Evolution of individuality: a case study in the volvocine green algae“). The article is open-access, and Hanschen and Davison are listed as equal contributors.
Erik Hanschen, readers may recall, was the lead author on the Gonium genome paper, and (full disclosure) he was my lab mate in Michael Doebeli’s lab at the University of British Columbia. Dinah Davison studies phenotypic variation in volvocine algae, and I previously wrote about the work she presented at AbSciCon.
The new paper has much in common with my chapter, though I don’t think any of the authors knew it existed when they were writing it. In that sense, it’s a good example of convergence, or maybe I should say parallelism since the lead authors and I share an intellectual ancestor in Rick Michod. Both papers review concepts of biological individuality and consider how they apply to various genera of volvocine algae, and both argue for a continuous, rather than dichotomous, view of individuality (in other words, that individuality comes in degrees, as opposed to being a category that a given biological unit either is or is not).
There are some important differences, though, and I’ll mostly be focusing on the novel aspects of the new paper. One of these is in the treatment of Chlamydomonas. Hanschen and Davison explicitly consider the consequences of palmelloid formation, which I did not talk about in the context of individuality:
Unicellular Chlamydomonas reinhardtii (Figure 1) forms multicellular clusters under certain conditions. One form of multicellular clusters, non-motile palmelloid clusters, are thought to form through the adhesion of daughter cells via an extracellular matrix or by failure of daughter cells to hatch out of the mother cell wall (Harris 2009; Khona et al. 2016). These clusters typically include 2, 4, 8, or 16 cells. Palmelloid clusters can facultatively form as a result of treatment inhibiting daughter cell hatching (e.g., calcium deprivation, chelating agents, high salt concentrations) and treatment resulting in cell wall aberrations…[skipping a lot here]
Multicellular Chlamydomonas clusters have clear spatial boundaries, but as cells are able to leave palmelloid clusters (Khona et al. 2016) we do not consider them indivisible. Cell clusters may form via aggregation between separate genetic strains, suggesting Chlamydomonas clusters are not always genetically homogenous (Sathe and Durand 2015); however, in the other studies discussed above, the clusters are considered to be clonally formed and genetically homogenous. Germ-soma division of labor is not present. The case of palmelloid clusters illustrates the challenges involved in distinguishing the level of selection leading to increased physiological unity and the presence of true group adaptations…
Another important difference is that Hanschen and Davison consider Tetrabaena to have cytoplasmic bridges connecting cells as well as rotational asymmetry of the basal bodies and flagella:
During reproduction, each cell in a Tetrabaena colony undergoes two rounds of cell division, producing a four-celled colony. These cells are attached through cytoplasmic bridges which result from incomplete cytokinesis (Arakaki et al. 2013); these bridges likely serve to keep the cells in the group.
Integration is enhanced by the existence of rotational asymmetry in the arrangement and rotation of basal bodies (Table 1). These basal bodies connect flagella to the cell wall, allowing for flagellar beating. Rotational asymmetry is unique and universal (in all species where it has been studied) to colonial/multicellular species (Kirk 2005; Arakaki et al. 2013), suggesting that this rotation plays an important role in colonial motility and thus may be considered a group-level adaptation.
Cytoplasmic bridges and rotation of the basal bodies had not been reported in Tetrabaena when I wrote my chapter, so I hope I can be forgiven for getting this wrong (I did acknowledge the mistake in my review of the 2015 Volvox Meeting).
Overall, the new paper is probably more pluralistic than my chapter in terms of the individuality criteria they consider. I chose to privilege more recent, evolutionary views of individuality, mostly variations on the theme that individuals are units of evolution. Hanschen and Davison argue for a ‘multidimensional’ perspective on individuality and discuss, in addition to evolutionary views, things like indivisibility, physiological unity, and spatial boundedness:
We suggest researchers embrace a multidimensional approach based on multiple individuality criteria to determine the kinds of individuality present in their system and how selection may be aﬀected. This approach may provide insight into individuality in taxa of interest, as well as how evolution is subsequently impacted. Our approach has utilized a multiplicity of individuality criteria. Mechanistic, trait-based definitions of individuality were critical to inform phenomenological, selection-based definitions of individuality, providing insight to how selection might be acting in the volvocine algae. This multidimensional approach to individuality, composed of trait-based definitions, selection-based definitions, and ecological context, may be informative in future research, particularly in the context of comparative studies.
They conclude that, while some criteria don’t differ much among volvocine species, some have changed considerably during the transition to multicellular life:
We find that the evolution of multicellular individuality from unicellular ancestors in the volvocine green algae likely involves minor changes in genetic homogeneity, genetic uniqueness, and spatial/temporal boundaries. While necessary for the initiation of group-level selection and evolution, these criteria do not appear to change substantially in the extent they are satisfied during the evolution of individuality in this lineage. Other individuality criteria, including division of labor, indivisibility, and the presence of multilevel selection, vary dramatically in how they are fulfilled. Examining these criteria in the context of ecology suggests three kinds of multicellular individuals: uncommitted multicellular individuals (Tetrabaena and Gonium), committed multicellular individuals (Pandorina and Eudorina), and committed, diﬀerentiated multicellular individuals (Pleodorina and Volvox).
Arakaki, Y. et al. 2013. The simplest integrated multicellular organism unveiled. PLoS One 8:e81641. doi: 10.1371/journal.pone.0081641
Hanschen ER, Davison DR, Grochau-Wright ZI, Michod RE. Evolution of individuality: a case study in the volvocine green algae. Philos. Theory, Pract. Biol. 2017;9:3. doi: 10.3998/ptb.6959004.0009.003
Herron, M. D. 2017. Cells , colonies, and clones : individuality in the volvocine algae. In S. Lidgard & L. K. Nyhart, eds., Biological Individuality: Integrating Scientific, Philosophical, and Historical Perspectives (pp. 63–83). University of Chicago Press, Chicago.