The Evolution of Centriole Structure: Heterochrony, Neoteny, and Hypermorphosis

Abstract

Centrioles are subcellular organelles that were present in the last eukaryotic common ancestor, where the centriole’s ancestral role was to form cilia. Centrioles have maintained a remarkably conserved structure in eukaryotes that have cilia, while groups that lack cilia have lost their centrioles, highlighting the structure–function relationship that exists between the centriole and the cilium. In contrast, animal sperm cells, a ciliated cell, exhibit remarkable structural diversity in the centriole. Understanding how this structural diversity evolved may provide insight into centriole assembly and function, as well as their unique role in sperm. Here, we apply concepts used in the study of the evolution of animal morphology to gain insight into the evolution of centriole structure. We propose that centrioles with an atypical structure form because of changes in the timing of centriole assembly events, which can be described as centriolar “heterochrony.” Atypical centrioles of insects and mammals appear to have evolved through different types of heterochrony. Here, we discuss two particular types of heterochrony: neoteny and hypermorphosis. The centriole assembly of insect sperm cells exhibits the retention of “juvenile” centriole structure, which can be described as centriolar “neoteny.” Mammalian sperm cells have an extended centriole assembly program through the addition of novel steps such as centrosome reduction and centriole remodeling to form atypical centrioles, a form of centriole “hypermorphosis.” Overall, centriole heterochrony appears to be a common mechanism for the development of the atypical centriole during the evolution of centriole assembly of various animals’ sperm.