The downsizing of gigantic scales and large cells in the genus Mallomonas (Synurales, Chrysophyceae)
Siver et al.19 identified three categories of fossil Mallomonas species uncovered in the extensive Giraffe Pipe locality. One group of species had scales with morphological characteristics similar to, and difficult to separate from, modern congeners. Based on a morphological species concept, these could be viewed as representing the same species. A second group had morphologically different scales, but ones that could be linked to one or more modern species. The third group possessed scales that could not be directly linked to any modern species. The majority of the species contained in the latter group lacked a V-rib and well developed dome, and were considered as stem organisms within the broad section Planae. Siver et al.19 further reported that the mean size of scales in the group containing the extinct stem taxa was larger than those fossil taxa grouped with modern congeners.The current study adds additional modern and fossil species to the database used by Siver et al.19, including the oldest known taxon from the Cretaceous Wombat locality, and provides the first attempt to reconstruct cell size for fossil Mallomonas species. Based on the expanded database, several trends with respect to the evolution of scale and cell size of Mallomonas taxa can be made. First, there is a strong relationship between scale width and scale length that was similar for both fossil and modern forms. Second, as a group, fossil taxa had scales that are significantly larger than those produced by modern species, especially with respect to surface area. The five species with the largest scales belong to extinct fossil species, four of which belong to the group of stem taxa within section Planae. These scales are massive compared with modern forms, and support the concept of scale gigantism for early members of the Mallomonas clade containing species with scales that lack a V-rib and dome (Fig. 1; subclade A2). Third, assuming the model relating scale and cell size can be applied to the geologic record, fossil species produced significantly larger cells than modern forms.Because the models relating scale length to scale width were similar for modern and fossil species, the assumption is that the models developed relating scale size to cell size are appropriate for fossil taxa. In addition, the precise overlapping pattern of scales comprising the cell covering on modern species has recently been documented for Eocene fossil species22, indicating that this architectural design was well evolved by at least the early Eocene. Thus, making the assumption that other fossil taxa had similarly constructed cell coverings is reasonable, and further supports the application of the models relating scale and cell size to these fossil forms.Based on the model estimates, the mean cell size of the fossil species is approximately twice as large as the average cell produced by modern organisms. This doubling of cell size was also observed for the smallest species. The mean size of the five smallest modern species (M. canina, M. mangofera, M. dickii, M. madagascariensis, and M. gutata) was 9.3 × 5 µm, compared to the mean cell size estimated for the five smallest fossil taxa (M. pseudohamata, M. preisigii, M. dispar, M. bakeri and M. GP4) of 18 × 8.7 µm. The cell size discrepancy is even greater for fossil species that lack modern congeners, and especially for the extinct stem species within section Planae that possessed an average cell size of 69.2 × 20.8 µm, with a maximum cell size of 81.7 × 22.7 µm for M. GP13. The scales produced by these large fossil cells were not only massive in size, but also robust and heavily silicified. It is likely that these large cells covered with large, heavy and cumbersome scales would have been slow swimmers that expended significantly more energy to maintain their position in the water column than modern species. Perhaps these cells were also more prone to predation by larger zooplankton, and a combination of decreased motility and greater predation provided the evolutionary pressure for smaller and faster cells with less dense siliceous components, and ultimately caused the demise of the large-celled fossil species. In contrast, it is also possible that the stimulus initially resulting in the evolution of the larger species was the fact that they were too big to be preyed upon by smaller invertebrates.Several points regarding the models used to estimate cell size are warranted. First, it is important to note that because the scale sizes used to estimate cell sizes for the larger fossil taxa are at the end of the range used to produce the model, caution needs to be exercised. The assumption is being made that the linear relationship of the model holds for the larger scales, and that the linear relationship does not begin to flatten and reach a maximum cell size. However, there is no indication that the relationship is reaching an asymptote, nor reason to assume that the model would not hold for organisms that produce larger siliceous components. Second, the scale and cell size data used to produce the models consisted of the midpoint values of the ranges given in the literature. Thus, the cell sizes inferred from the models represent a midpoint estimate of the range for each species, and not an upper size limit. Third, there is more data available in the literature documenting scale size than there is for cell size for most modern Mallomonas species. Additional data on cell size, especially inclusion of mean values, may help to further fine-tune the models. Lastly, the formula of an ellipse was used to estimate scale surface area for the few species with “square-shaped” scales. Although this may slightly underestimate the surface area, using a formula for a square or rectangle would have resulted in an overestimation. Because the few species with square-shaped scales were primarily the extinct fossil taxa lacking modern congeners, their cell size may actually have been slightly larger than estimated in this study.Interestingly, fossil scales that have morphologically similar (identical) modern counterparts were not significantly different in size from each other, implying that their corresponding cells were also of similar size. These taxa have significantly smaller scales compared to those species with gigantic scales, and closer to the mean of modern species. Perhaps, this is why the lineages of these morphologically-identical species have survived for tens of millions of years. Despite maintaining virtually identical scale types, the degree of genetic difference from a physiological or reproductive perspective between taxa with virtually identical siliceous components remains unknown19,23.The extinct scale types are not only significantly larger than those of species with modern congeners, but some have a tendency of being more rectangular to square-shaped. In contrast, fossil scale types that can be linked to modern species, along with their contemporary counterparts, tend to have elliptical-shaped scales. This is especially true of body scales15,16,19. Although a few smaller species of Mallomonas form spherical cells, the vast majority of species produce ellipsoidal-shaped cells, and this is especially true of species forming larger cells15,16. Smaller elliptical-shaped scales would be more efficient in covering a curving ellipsoidal cell surface than larger and square-shaped scales, and allow for a closer fitting cell covering. Jadrná et al.26 recently reported that scales of the closely related synurophyte genus, Synura, have also become smaller and more elongate over geologic time, complementing the observations for Mallomonas. Taken together, these findings support the idea that the evolutionary trend for synurophyte organisms has been towards smaller, elliptical scales.Cyanobacteria, a prokaryotic group of organisms estimated to have evolved by 3.5–3.4 Ga, represent one of the earliest known and smallest life forms on Earth27. Since the evolution of these early prokaryotes, Smith et al.28 estimated that the maximum body size of subsequent life forms has increased approximately 18-fold, with large jumps occurring with the evolution of eukaryote cells, and another concurrent with the advent of multicellularity. In contrast, shifts in the sizes of siliceous scales and corresponding cells of Mallomonas species are small in comparison, within an order of magnitude, and similar to changes observed for prokaryote organisms and other unicellular protists over the Geozoic28,29.Despite the overall lack of historical information on cell size for the majority of unicellular eukaryote lineages, there are data for some organisms that build resistant cell walls or coverings that are taxonomically diagnostic and become incorporated into the fossil record. Diatoms produce a siliceous cell wall known as the frustule, a structure composed of top and bottom pieces called valves that are held together with additional structures called girdle bands. Frustules, or their valve components, can be uncovered from the fossil record and used to provide a direct measure of cell size. Using this technique, Finkel et al.29 reported that the size of planktic marine diatoms declined over the Cenozoic, and correlated the shift with abiotic forcing factors, including a rise in sea surface temperature and water column stratification. Foraminifera are heterotrophic marine protists that build shells out of calcium carbonate, the latter of which can also become part of the fossil record. Changes in the size of foraminifera shells over the Cenozoic have also been correlated with shifts in the intensity of water column stratification30. At this time, it is not known if the decline in cell size for Mallomonas species in the section Planae lineage recorded in the current study was the result of abiotic variables (e.g. energy expenditure or temperature), biotic factors (e.g. predation), or a combination of forcing variables.The current study has provided a means to link scale size to cell size for Mallomonas that, in turn, can be used to trace shifts in cell size over geologic time. As additional scales of Mallomonas species are uncovered from the fossil record, the scale-to-cell size model will be a valuable tool for continuing to unravel the evolutionary history of cell size for this important photosynthetic organism. Other groups of unicellular protists, including euglyphids, heliozoids and rotosphaerids, are similar to synurophytes in that they build cell coverings using numerous overlapping siliceous scales or plates that can become fossilize. Perhaps the same technique of relating scale size to cell size could be used to develop models for these protist organisms, and similarly applied to the fossil record.It is interesting to note that most modern Mallomonas species with large body scales are found in warm tropical regions, including M. bronchartiana Compère, M. pseudobronchartiana Gusev, Siver & Shin, M. velari Gusev, Siver & Shin31, M. vietnamica Gusev, Kezlya & Trans32, M. gusakovii33 and several varieties of M. matvienkoae16. In addition, the modern tropical taxa M. neoampla Gusev & Siver and M. vietnamica share several rare features of their scales and bristles with fossil species recorded from the Giraffe locality, suggesting a possible link between the modern tropical and fossil floras. During the early to middle Eocene, the Earth experienced warm greenhouse conditions and lacked a cryosphere34. The Giraffe locality, positioned near the Arctic Circle, had an estimated mean annual temperature 17 °C warmer, and a mean annual precipitation over four times higher, than present conditions35. In fact, the assemblage of plants and animals in the Eocene Arctic has been described as analogous to those found today in eastern Asia36. Perhaps tropical regions, especially in southeastern Asia, offered refugia for some of the ancient Mallomonas lineages.In summary, multiple extinct fossil species of the diverse and common synurophyte genus, Mallomonas, are reported here to have possessed gigantic scales that are significantly larger than those found on modern species. Based on a model relating scale to cell size, cells of fossil Mallomonas species were estimated to be, on average, twice as large as modern species. A combination of larger cells with heavy siliceous scales that fit less effectively around the cell may have resulted in slower cells more prone to predation, heavier cells requiring more energy resources to maintain their position in the water column, and ultimately their demise. Additional fossil species, especially representing other localities and time periods, will ultimately strengthen our understanding of the evolution of scale and cell size in synurophyte algae. More
