Genetic coordination of sperm morphology and seminal fluid proteins promotes male reproductive success in Drosophila melanogaster

Spermatozoal morphology is highly variable both among and within species and in ways that can significantly impact fertilization success. In Drosophila melanogaster, paternity success depends on sperm length of both competing males and length of the female's primary sperm storage organ. We found that genes upregulated in long sperm testes are enriched for lncRNAs and seminal fluid proteins (Sfps). Transferred in seminal fluid to the female during mating, Sfps are secreted by the male accessory glands (AG) and affect female remating rate, physiology, and behavior with concomitant advantages for male reproductive success. Despite being upregulated in long sperm testes, they have no known function in testis tissue. We found that Sex Peptide and ovulin (Acp26Aa) knockouts resulted in shorter sperm, suggesting that Sfps may regulate sperm length during spermatogenesis. However, knockout of AG function did not affect sperm length, suggesting that AG expression has no influence on spermatogenic processes. We also found that long sperm males are better able to delay female remating, suggesting higher Sfp expression in AG. These results might suggest that long sperm males have a double advantage in sperm competition by both delaying female remating, likely through transfer of more Sfps, and by resisting sperm displacement. However, we also found that this extra advantage does not necessarily translate to more progeny or higher paternity success. Thus, we found that multiple components of the ejaculate coordinate to promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain.

Fertilization Modes And The Evolution of Sperm Characteristics In Marine Fishes: Paired Comparisons of The Externally And Internally Fertilizing Species

Background: Fertilization modes may affect sperm characteristics, such as morphology, velocity, and motility. However, there is surprisingly little information on how fertilization mode affects sperm evolution because several factors (e.g. sperm competition and phylogeny) are intricately intertwined with this factor when phylogenetically distant species are compared. Here, we compared sperm characteristics between six externally and four internally fertilizing marine fishes from three different groups containing close relatives, taking into account the level of sperm competition. We also analysed the relationship between relative testis mass (as an index of sperm competition level) and sperm characteristics.Results: Sperm head morphology was significantly longer in species with internal fertilization than in those with external fertilization, suggesting that a longer head is advantageous for swimming in viscous ovarian fluid or the complex ovarian structure. In addition, sperm motility differed between external fertilizers and internal fertilizers; sperm of externally fertilizing species were only motile in seawater, and sperm of internally fertilizing species were only motile in an isotonic solution. These results suggest that sperm motility has adapted according to the fertilization mode. In contrast, total sperm length and sperm velocity did not correlate with fertilization mode, perhaps because of the different levels of sperm competition. Relative testis mass is positively correlated with sperm velocity and negatively correlated with the ratio of sperm head length/flagellum length. This finding suggests that species with high levels of sperm competition have sperm that are fast and have relatively long flagella compared to head length. These results contradict a previous assumption that the evolution of internal fertilization increases total sperm length. In addition, copulatory behaviour with internal insemination may involve a large intromittent organ, but this is not essential in fish, probably due to the avoidance of water resistance.Conclusions: We propose a new scenario of sperm evolution in which internal fertilization increases sperm head length but not total sperm length and changes sperm motility. In contrast, sperm competition affects sperm length and velocity. Our findings provide a new perspective on the evolutionary biology of sperm in fish.

Longer Sperm Swim More Slowly in the Canary Islands Chiffchaff

Sperm swimming performance affects male fertilization success, particularly in species with high sperm competition. Understanding how sperm morphology impacts swimming performance is therefore important. Sperm swimming speed is hypothesized to increase with total sperm length, relative flagellum length (with the flagellum generating forward thrust), and relative midpiece length (as the midpiece contains the mitochondria). We tested these hypotheses and tested for divergence in sperm traits in five island populations of Canary Islands chiffchaff (Phylloscopus canariensis). We confirmed incipient mitochondrial DNA differentiation between Gran Canaria and the other islands. Sperm swimming speed correlated negatively with total sperm length, did not correlate with relative flagellum length, and correlated negatively with relative midpiece length (for Gran Canaria only). The proportion of motile cells increased with relative flagellum length on Gran Canaria only. Sperm morphology was similar across islands. We thus add to a growing number of studies on passerine birds that do not support sperm morphology–swimming speed hypotheses. We suggest that the swimming mechanics of passerine sperm are sufficiently different from mammalian sperm that predictions from mammalian hydrodynamic models should no longer be applied for this taxon. While both sperm morphology and sperm swimming speed are likely under selection in passerines, the relationship between them requires further elucidation.

Can Sexual Selection Drive the Evolution of Sperm Cell Structure?

Sperm cells have undergone an extraordinarily divergent evolution among metazoan animals. Parker recognized that because female animals frequently mate with more than one male, sexual selection would continue after mating and impose strong selection on sperm cells to maximize fertilization success. Comparative analyses among species have revealed a general relationship between the strength of selection from sperm competition and the length of sperm cells and their constituent parts. However, comparative analyses cannot address causation. Here, we use experimental evolution to ask whether sexual selection can drive the divergence of sperm cell phenotype, using the dung beetle Onthophagus taurus as a model. We either relaxed sexual selection by enforcing monogamy or allowed sexual selection to continue for 20 generations before sampling males and measuring the total length of sperm cells and their constituent parts, the acrosome, nucleus, and flagella. We found differences in the length of the sperm cell nucleus but no differences in the length of the acrosome, flagella, or total sperm length. Our data suggest that different sperm cell components may respond independently to sexual selection and contribute to the divergent evolution of these extraordinary cells.

Morphometric Characteristics of the Spermatozoa of Blue Fox (Alopex lagopus) and Silver Fox (Vulpes vulpes)

The results presented in this study are the first such extensive characterization of the sperm morphometry of the blue fox (Alopex lagopus) and silver fox (Vulpes vulpes), as representatives of the family Canidae. Canine spermatozoa, especially the sperm of farmed foxes, are not often described in studies on reproduction. The aim of the study was a detailed comparison of the morphometric dimensions and shape of the sperm of two fox species: silver fox and blue fox. Semen collected from 10 silver foxes and 10 blue foxes was used for the study. The specimens were stained with silver nitrate. Measurements were performed of the length, width, perimeter, and area of the head; the area of the acrosome and its coverage; the length of the midpiece and its coverage; the length of the tail; and the length of the end piece of the tail. In addition, four head shape indices were calculated: ellipticity, elongation, roughness and regularity. The following values for the morphometric parameters and shape indices were obtained for blue fox and silver fox, respectively: head length—6.72 µm and 6.33 µm; head width—4.54.µm and 4.21 µm; head perimeter—18.11 µm and 17.37 µm; head area—21.94 µm2 and 21.11 µm2; acrosome area—11.50 µm2 and 10.92 µm2; midpiece length—12.85 µm and 12.79 µm; tail end piece length—3.44 µm and 3.28 µm; tail length—65.23 µm and 65.09 µm; acrosome coverage—52.43% and 52.83%; midpiece coverage—19.71% and 19.65%; sperm length—71.95 µm and 71.42 µm; ellipticity—1.49 and 1.52; elongation—0.19 and 0.20; roughness—0.84 and 1.88; regularity—1.09 and 0.99. The significance of differences between species was verified by Tukey’s test at p ≤ 0.05. Statistically significant differences between species were found for the following parameters: head length, width, perimeter and area; acrosome area; tail, end piece, and total sperm length; roughness and regularity. The differences in the size and shape of sperm can be used to establish reference patterns for fox sperm enabling more accurate species identification.

How sperm competition shapes the evolution of testes and sperm: a meta-analysis

Females of many species mate with multiple males, thereby inciting competition among ejaculates from rival males for fertilization. In response to increasing sperm competition, males are predicted to enhance their investment in sperm production. This prediction is so widespread that testes size (correcting for body size) is commonly used as a proxy of sperm competition, even in the absence of any other information about a species' reproductive behaviour. By contrast, a debate about whether sperm competition selects for smaller or larger sperm has persisted for nearly three decades, with empirical studies demonstrating every possible response. Here, we synthesize nearly 40 years of sperm competition research in a meta-analytical framework to determine how the evolution of sperm number (i.e. testes size) and sperm size (i.e. sperm head, midpiece, flagellum and total length) is influenced by varying levels of sperm competition across species. Our findings support the long-held assumption that higher levels of sperm competition are associated with relatively larger testes. We also find clear evidence that sperm competition is associated with increases in all components of sperm length. We discuss these results in the context of different theoretical predictions and general patterns in the breeding biology and selective environment of sperm. This article is part of the theme issue ‘Fifty years of sperm competition’.