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Evolutionary processes have transformed simple cellular life into a great diversity of forms, ranging from the ubiquitous eukaryotic cell design to the more specific cellular forms of spirochetes, cyanobacteria, ciliates, heliozoans, amoeba, and many others. The cellular traits that constitute these forms require an evolutionary explanation. Ultimately, the persistence of a cellular trait depends on its net contribution to fitness, a quantitative measure. Independent of any positive effects, a cellular trait exhibits a baseline energetic cost that needs to be accounted for when quantitatively examining its net fitness effect. Here, we explore how the energetic burden introduced by a cellular trait quantitatively affects cellular fitness, describe methods for determining cell energy budgets, summarize the costs of cellular traits across the tree of life, and examine how the fitness impacts of these energetic costs compare to other evolutionary forces and trait benefits. 

Most creatures on Earth are single cell organisms. The tree of life comprises three domains, two of which – bacteria and archaea – are formed exclusively of creatures that spend their existence as independent cells. Yet even eukaryotes, the domain which include animals and plants, feature single cell species such as yeasts and algae. Regardless of which group they belong to, all single-celled organisms must find food in their environment. For this, many are equipped with flagella, whip-like structures that protrude from the cell and allow it to swim. In fact, archaea, bacteria and eukaryotes have all independently evolved these structures. However, flagella are also expensive for an organism to build, maintain and operate. They are only worth having if the advantages they bring to the cell compensate for their cost; many single-cell species do not carry flagella and obtain their food without having to swim. To explore this trade-off, Schavemaker and Lynch calculated the cost of building and using flagella for about 200 species across the tree of life. The analysis show that the amount of energy spent on flagella varied between 0.1% and 40% of the entire cell budget. This investment is only worthwhile if the cell is above a certain size. Smaller than this, and the organism is better off obtaining its food passively. The results also show that while eukaryotic flagella are much bigger and quite different than their bacterial counterpart, both appendages share the same patterns of cost effectiveness. However only eukaryotic cells, which are on average larger than bacteria, can afford to evolve such sizable and complex structures; making just one would cost more than the entire energy budget of a bacterial cell. Many single-cell species which are critical for the health of the planet are equipped with flagella, such as the microorganisms which recycle matter in the oceans and release carbon dioxide. Understanding the costs and benefits of flagella could explain more about this aspect of the carbon cycle, and therefore global warming. 

Abstract Understanding why various organisms evolve alternative ways of living requires information on both the fitness advantages of phenotypic modifications and the costs of constructing and operating cellular features. Although the former has been the subject of a myriad of ecological studies, almost no attention has been given to how organisms allocate resources to alternative structures and functions. We address these matters by capitalizing on an array of observations on diverse ciliate species and from the emerging field of evolutionary bioenergetics. A relatively robust and general estimator for the total cost of a cell per cell cycle (in units of ATP equivalents) is provided, and this is then used to understand how the magnitudes of various investments scale with cell size. Among other things, we examine the costs associated with the large macronuclear genomes of ciliates, as well as ribosomes, various internal membranes, osmoregulation, cilia, and swimming activities. Although a number of uncertainties remain, the general approach taken may serve as blueprint for expanding this line of work to additional traits and phylogenetic lineages.