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.
Highlights
In his historical 1970 sperm competition paper, Dr Geoff Parker discussed the sequence of possible events influencing sperm evolution [1]
On p.526, he says: “ it seems likely that the reproductive behavior of insects followed a path from external fertilization to internal fertilization with spermatophores, and later to copulation with the spermatophore deposited inside the reproductive tract of the female
We found a strong and statistically significant correlation between internal fertilization and atypical centriolar composition, suggesting that atypical centrioles evolved as part of the evolutionary sexual cascade that occurred after the appearance of internal fertilization
Summary
In his historical 1970 sperm competition paper, Dr Geoff Parker discussed the sequence of possible events influencing sperm evolution [1]. Natural selection might have had a subordinate role to intrasexual selection during most of the earlier stages of this pathway.”. This series of natural selection events is called the sexual cascade [2]. Internal fertilizers have evolved a large diversity of sperm morphologies [3,4] including longer sperm [5]. Significant attention has been given to evolutionary adaptions in sperm head and tail morphology [6,7,8,9,10,11]. Little is known about the structural evolution of the sperm neck and the centrioles within it (Figure 1)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
