Fertilization mode differentially impacts the evolution of vertebrate sperm components

Abstract

Environmental change frequently drives morphological diversification, including at the cellular level. Transitions in the environment where fertilization occurs (i.e., fertilization mode) are hypothesized to be a driver of the extreme diversity in sperm morphology observed in animals. Yet how fertilization mode impacts the evolution of sperm components—head, midpiece, and flagellum—each with different functional roles that must act as an integrated unit remains unclear. Here, we test this hypothesis by examining the evolution of sperm component lengths across 1103 species of vertebrates varying in fertilization mode (external vs. internal fertilization). Sperm component length is explained in part by fertilization mode across vertebrates, but how fertilization mode influences sperm evolution varies among sperm components and vertebrate clades. We also identify evolutionary responses not influenced by fertilization mode: midpieces evolve rapidly in both external and internal fertilizers. Fertilization mode thus influences vertebrate sperm evolution through complex component- and clade-specific evolutionary responses.

Evaluation of domestic animal sperm head morphology via flow cytometric DNA labelling and pulse shape analysis using bull and stallion spermatozoa as model species

“…Besides the importance of evaluation of sperm abnormalities in the quality control of breeding animals used either for artificial insemination or natural breeding, there is a growing interest in sperm morphology from the points of view of evolutionary aspects (Kahrl et al, 2021(Kahrl et al, , 2022 or taxonomy (Jamieson, 1991). A comprehensive database on sperm morphology and morphometry of animal taxa is continuously developed (Fitzpatrick et al, 2022).…”

Characterization of sperm and implications for male fertility in the last of the Rhynchocephalians

“…The general three-part structure of sperm is remarkably conserved across vertebrate lineages, with each section playing a distinct role in the cell’s function ( Horta et al, 2018 ). Sperm cells consist of a head containing genetic material packaged as chromosomes within the sperm’s nucleus, a midpiece housing mitochondria that provide the sperm with the energy necessary to move, and a tail that propels the cell towards the unfertilized egg ( Horta et al, 2018 ; Kahrl et al, 2022 ). Because each section serves a unique function within the sperm cell, these sections may respond differently to varying selection pressures ( Reinhardt et al, 2015 ).…”

“…Because each section serves a unique function within the sperm cell, these sections may respond differently to varying selection pressures ( Reinhardt et al, 2015 ). Subsequently, variation in the length and shape of each sperm section can be observed across taxa ( Horta et al, 2018 ), between modes of fertilization within a taxa ( Kahrl et al, 2021 , 2022 ) and in response to the intensity of selection pressures such as cryptic female choice and inter-male sperm competition (hereafter ‘sperm competition’) ( Firman et al, 2017 ; Lüpold et al, 2020 ). These structural changes can also influence the speed at which sperm move; for example, the sperm midpiece houses the mitochondria that produce ATP, the energy source for sperm movement ( Lüpold and Pitnick, 2018 ; Lara et al, 2020 ).…”

“…In general, theory suggests that higher levels of sperm competition may result in an increase in both the overall length of sperm and the length of each section ( Briskie et al, 1997 ; Fitzpatrick et al, 2009 ); this covariance could be the result of genetic or other functional and mechanistic constraints. However, recent research has found that sperm sections can display distinct rates of phenotypic diversification ( Immler et al, 2012 ; Rowe et al, 2015 ; Kahrl et al, 2019 ; Fitzpatrick et al, 2020 ; Friesen et al, 2020 ; Reuland et al, 2021 ), suggesting that the independent evolution of sperm sections is possible ( Kahrl et al, 2022 ), though this is poorly understood in many taxa. Thus, it is important to consider variation in the length of each section independently.…”

Sperm length evolution in relation to body mass is shaped by multiple trade-offs in tetrapods

“…The smallest and longest sperm recorded so far are both found in arthropods, while sperm size in vertebrates does not show the same level of variation, ranging from slightly more than 10 μm (in external fertilizers such as bony fishes and frogs) to approximately 10 3 μm (in some urodeles) 4 . It has been recently demonstrated on a large taxonomical scale that the fertilization mode represents an important source of variation, with external fertilizers having, on average, shorter sperm than internal fertilizers 1,5 . Moreover, sperm competition (i.e., when sperm from different males compete to fertilize the same eggs [6][7][8] ) leads to the evolution of i) larger testes, and ii) longer sperm 9 (with exceptions limited to a few taxa reviewed in 10 .…”