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.

Keywords: centriole; evolution; external fertilization; internal fertilization; sperm; sperm competition.

Figure 1

Atypical centrioles have distinct structures. (A) A mammalian sperm showing the locations of the atypical and canonical centrioles in the sperm neck. To the left, a cross section of the PC and DC depicting microtubule organization. (B) The number and size of spermatozoan centrioles vary throughout evolution. Shown are four animal groups (color-coded) organized based on the number and type of their spermatozoan centrioles. Animals with two centrioles (black). Animals with just one canonical centriole also have an atypical centriole: the proximal centriole-like (PCL, red) structure in insects and the atypical distal centriole (DC, blue) in mammals. Animals with DC remanent (green). Color code in the Atypical DC: green color marks the presence of microtubules, and magenta marks rod proteins.

Figure 2

Fish species with a single canonical centriole evolved independently multiple times from an ancestral state with two canonical centrioles. (A–C) A phylogenetic tree depicting fertilization mode (internal or external) and canonical centriole number (1 or 2) in the main branches of vertebrates and fish. (A) Depicts the main fish groups. (B) Depicts ray-fin fish (Actinopterygii). (C) Depicts Euacanthomorphacea. In some cases, we provide the scientific name and common name in parentheses. Vertebrata, Chondrichthyes (Cartilaginous fish), Teleostei (Bony fishes), and Poeciliinae are bolded and enlarged because they are specifically referenced in the text. The number of fish species in a category appear as a numeral in parentheses. The figure contains the names of all fish families analyzed in this survey.