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. 2024 Jan 2;15:117. doi: 10.1038/s41467-023-44411-8

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© The Author(s) 2024

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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Fig. 1 — a The sperm centriole evolutionary cascade hypothesis. Each panel depicts the spermatozoan head and neck morphology (left), the spermatozoan centrioles (middle, in green), and the zygotic centriolar configuration (right). (i) Stage 1: the pre-mammalian centriolar configuration. Spermatozoon with a ball-shaped head, centrally inserted neck (tail attached below the head base center), and canonical proximal (PC) and distal centrioles (DC). Centriole-dependent zygote with two centrosomes emanating asters. (ii) Stage 2: the mammalian centriolar configuration. Sperm competition improved sperm behavior at this stage. Spermatozoon with a paddle-shaped head, centrally inserted neck, and canonical proximal and distal centrioles. Centriole-dependent zygote with two centrosomes emanating asters. (iii) Stage 3: the Eumuroida (subgroup of murids) centriolar configuration. The cost of increased miscarriage rates eliminated the need for zygotic centrioles at this stage. Spermatozoon with a sickle-shaped head, neck attached to the base either centrally or off-center (tail attached asymmetrically, below the head base), and canonical proximal and distal centrioles. Centriole-independent embryonic development. (iv) Stage 4: the murid (house mouse) centriolar configuration. Spermatozoan centrioles were freed from the functional constraints imposed by the centriole’s role in the embryo, allowing for innovation in sperm morphology. Spermatozoon with a sickle-shaped head, lateral head-neck attachment (tail attached to the side of the head, parallel to the base), and remnant centrioles. Centriole-independent embryonic development. b–e A summary of rodent evolution, depicting their phylogenetic tree (b), proximal centriolar structure (c), head shape (d), and neck attachment (e). No PC, proximal centriolar structure not observed; uk, unknown; canon presence of a structurally canonical proximal centriole; sickle, sickle-shaped head; paddle, paddle-shaped head; lateral, neck attachment on one side of the head; O-C base, off-center neck attachment to the base of the head; base, neck attachment near the center of the base of the head.