Atypical Centriolar Composition Correlates with Internal Fertilization in Fish

Abstract

The sperm competition theory, as proposed by Geoff Parker, predicts that sperm evolve through a cascade of changes. As an example, internal fertilization is followed by sperm morphology diversification. However, little is known about the evolution of internal sperm structures. The centriole has an ancient and evolutionarily conserved canonical structure with signature 9-fold, radially symmetric microtubules that form the cell’s centrosomes, cilia, and flagella. Most animal spermatozoa have two centrioles, one of which forms the spermatozoan flagellum. Both are delivered to the egg and constitute the embryo’s first two centrosomes. The spermatozoa of mammals and insects only have one recognizable centriole with a canonical structure. A second sperm centriole with an atypical structure was recently reported in both animal groups and which, prior to this, eluded discovery by standard techniques and criteria. Because the ancestors of both mammals and insects reproduced by internal fertilization, we hypothesized that the transition from two centrioles with canonical composition in ancestral sperm to an atypical centriolar composition characterized by only one canonical centriole evolved preferentially after internal fertilization. We examined fish because of the diversity of species available to test this hypothesis–as some species reproduce via internal and others via external fertilization–and because their spermatozoan ultrastructure has been extensively studied. Our literature search reports on 277 fish species. Species reported with atypical centriolar composition are specifically enriched among internal fertilizers compared to external fertilizers (7/34, 20.6% versus 2/243, 0.80%; p < 0.00001, odds ratio = 32.4) and represent phylogenetically unrelated fish. Atypical centrioles are present in the internal fertilizers of the subfamily Poeciliinae. Therefore, internally fertilizing fish preferentially and independently evolved spermatozoa with atypical centriolar composition multiple times, agreeing with Parker’s cascade theory.

The Evolution of Centriole Degradation in Mouse Sperm

“…The fan-shaped, atypical distal centriole was discovered in 2018 using advanced electron microscopy (Fishman et al, 2018); therefore, studies of spermatozoa prior to this year mainly addressed the presence or lack of barrel-shaped centrioles. Two barrel-shaped proximal and distal centrioles are found in the spermatozoa of most basal vertebrate external fertilizers (Turner et al, 2022). In contrast, classic transmission electron microscopy (TEM) studies in mammalian spermatozoa found only one barrel-shaped centriole, the proximal centriole, with a few exceptions in marsupial and some rodent species that appear to lack it ( Sfig 1 ).…”

“…At this stage, the two centrioles are required for early embryogenesis (zygote to blastocyst), exhibiting centriole-dependent embryonic development (Yabe et al, 2007). Stage 2 – The mammalian centriolar configuration : sperm competition within the female reproductive tract of internal fertilizers selected for sperm with atypical centrioles, suggesting that atypical centrioles are an innovation associated with changes in the mode of fertilization (Fishman et al, 2017; Khire et al, 2016; Turner et al, 2022), as internal fertilization provides unique challenges to the sperm. For example, in mammals, sperm swim in a multi-compartmentalized female reproductive tract with varying viscoelastic mucus and complex landscapes, including microgrooves (reviewed in Tung and Suarez, 2021).…”

The Centriole’s Role in Miscarriages

“…The DC is canonical in six distantly related fish clades, but the PC is either atypical or undetected ( Turner et al, 2017 ). While it is possible that these species lost their PC, another, more likely explanation is that the PC is modified to the point of being unrecognizable.…”