Evolutionary cell biology: two origins, one objective

Abstract

All aspects of biological diversification ultimately trace to evolutionary modifications at the cellular level. This central role of cells frames the basic questions as to how cells work and how cells come to be the way they are. Although these two lines of inquiry lie respectively within the traditional provenance of cell biology and evolutionary biology, a comprehensive synthesis of evolutionary and cell-biological thinking is lacking. We define evolutionary cell biology as the fusion of these two eponymous fields with the theoretical and quantitative branches of biochemistry, biophysics, and population genetics. The key goals are to develop a mechanistic understanding of general evolutionary processes, while specifically infusing cell biology with an evolutionary perspective. The full development of this interdisciplinary field has the potential to solve numerous problems in diverse areas of biology, including the degree to which selection, effectively neutral processes, historical contingencies, and/or constraints at the chemical and biophysical levels dictate patterns of variation for intracellular features. These problems can now be examined at both the within- and among-species levels, with single-cell methodologies even allowing quantification of variation within genotypes. Some results from this emerging field have already had a substantial impact on cell biology, and future findings will significantly influence applications in agriculture, medicine, environmental science, and synthetic biology.

Keywords: adaptive evolution; cell biology; cellular evolution; evolutionary cell biology; random genetic drift.

Fig. 1.

Taxonomic distribution of research articles and sequenced genomes. Modern taxonomy identifies five major eukaryotic supergroups: the Excavates (turquoise), Chromalveolates (orange), Archaeplastida (green), Amoebozoa (purple), and Opisthokonts (red). Although the total number of species on earth remains unknown, it is clear that there are far more unicellular eukaryotes than the combined total of all animals (Metazoa, an Opisthokont lineage), fungi (also Opisthokonts), and plants (Archaeplastida). However, research activity displays considerable taxonomic bias. As of January 2014, the National Center for Biotechnology Information taxonomy browser (www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi) lists 338 Archaeal genomes (dark gray), 20,709 Eubacteria (light gray), 769 Metazoa, 1,201 Fungi, 251 green plants/algae, and 336 genomes from all other eukaryotic taxa (13% of eukaryotic genomes). The taxonomic distribution of PubMed citations is as follows: Archaea, 19,000; Eubacteria, 397,000; Metazoa, 576,000; Fungi, 135,000; green plants/algae, 168,000; and all other eukaryotes combined, 97,000 (<9% of publications on Eukaryotes).