Evolution of Cilia

Abstract

Anton van Leeuwenhoek's startling microscopic observations in the 1600s first stimulated fascination with the way that cells use cilia to generate currents and to swim in a fluid environment. Research in recent decades has yielded deep knowledge about the mechanical and biochemical nature of these organelles but only opened a greater fascination about how such beautifully intricate and multifunctional structures arose during evolution. Answers to this evolutionary puzzle are not only sought to satisfy basic curiosity, but also, as stated so eloquently by Dobzhansky (Am Zool 4: 443 [1964]), because "nothing in biology makes sense except in the light of evolution." Here I attempt to summarize current knowledge of what ciliary organelles of the last eukaryotic common ancestor (LECA) were like, explore the ways in which cilia have evolved since that time, and speculate on the selective processes that might have generated these organelles during early eukaryotic evolution.

Figure 1.

(A) Diagram of major eukaryotic clades diverging from a last eukaryotic common ancestor (LECA), with the root placed between unikont and bikont superclades. Branches are color-coded according to differences in orientation of ciliary central-pair microtubules, which appear perpendicular to the bend plane and fixed in unikonts (blue), perpendicular to the bend plane but floating in excavates (orange), and twisted (helical) and rotating in other bikonts (green). The LECA is cartooned as a single cell with a nucleus, a mitochondrion, and two flagella: an anterior motile flagellum and a posterior gliding flagellum. The dashed arrow indicates the first acquisition of a plastid through endosymbiosis of a cyanobacterium. (B) Diagrams of ciliary axonemal structures that were present in the LECA. (Left) Cross-sectional view from inside the cell. (Right) Longitudinal view of one 96-nm repeat along an outer doublet. MIA, Modifier of inner arms; ODA, outer dynein arm; IDA, inner dynein arm; DRC, dynein regulatory complex.

Figure 2.

Three alternative branching and extinction pathways leading from the last universal common ancestor (LUCA) to the first eukaryotic common ancestor (FECA), the last eukaryotic common ancestor (LECA), and present eukaryotic clades are diagrammed to explore mechanisms that selected for a LECA with 9+2 cilia. (A) Mitochondrial (Mito) endosymbiosis early, together with formation of a nucleus, transforms an archaeum into the FECA. Present diversity results from random branching and extinction, and alternate ciliary architectures are lost by chance. (B) Mitochondria are acquired early. Present clades result from rapid divergence from the LECA following a major extinction event, which chanced to preserve an organism with 9+2 cilia. (C) Horizontal gene transfer (HGT) between eubacteria and archaea generates an amitochondriate FECA. Much later, endosymbiosis of an α-proteobacterium creates the LECA, which rapidly diverges into present clades, whereas clades that lack mitochondria become extinct. The host for endosymbiosis, by chance, has 9+2 cilia. Arch., Archaea; Bact., bacteria.