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Editorial

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9 pages, 777 KiB

Open AccessEditorial

On the Origin and Evolution of Sperm Cells

by Heidi S. Fisher, Eduardo R. S. Roldan, Tomer Avidor-Reiss and Melissah Rowe

Cells 2023, 12(1), 159; https://doi.org/10.3390/cells12010159 - 30 Dec 2022

Cited by 1 | Viewed by 2470

Abstract

Sperm cells have intrigued biologists since they were first observed nearly 350 years ago by Antonie van Leeuwenhoek and Johan Ham [...] Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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Research

Jump to: Editorial, Review, Other

14 pages, 1180 KiB

Open AccessArticle

Biophysical Determinants and Constraints on Sperm Swimming Velocity

by Carl D. Soulsbury and Stuart Humphries

Cells 2022, 11(21), 3360; https://doi.org/10.3390/cells11213360 - 25 Oct 2022

Cited by 4 | Viewed by 2015

Abstract

Over the last 50 years, sperm competition has become increasingly recognised as a potent evolutionary force shaping male ejaculate traits. One such trait is sperm swimming speed, with faster sperm associated with increased fertilisation success in some species. Consequently, sperm are often thought [...] Read more.

Over the last 50 years, sperm competition has become increasingly recognised as a potent evolutionary force shaping male ejaculate traits. One such trait is sperm swimming speed, with faster sperm associated with increased fertilisation success in some species. Consequently, sperm are often thought to have evolved to be longer in order to facilitate faster movement. However, despite the intrinsic appeal of this argument, sperm operate in a different biophysical environment than we are used to, and instead increasing length may not necessarily be associated with higher velocity. Here, we test four predictive models (ConstantPower Density, Constant Speed, Constant Power Transfer, Constant Force) of the relationship between sperm length and speed. We collated published data on sperm morphology and velocity from 141 animal species, tested for structural clustering of sperm morphology and then compared the model predictions across all morphologically similar sperm clusters. Within four of five morphological clusters of sperm, we did not find a significant positive relationship between total sperm length and velocity. Instead, in four morphological sperm clusters we found evidence for the Constant Speed model, which predicts that power output is determined by the flagellum and so is proportional to flagellum length. Our results show the relationship between sperm morphology (size, width) and swimming speed is complex and that traditional models do not capture the biophysical interactions involved. Future work therefore needs to incorporate not only a better understanding of how sperm operate in the microfluid environment, but also the importance of fertilising environment, i.e., internal and external fertilisers. The microenvironment in which sperm operate is of critical importance in shaping the relationship between sperm length and form and sperm swimming speed. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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20 pages, 1146 KiB

Open AccessArticle

Sperm Numbers as a Paternity Guard in a Wild Bird

by Melissah Rowe, Annabel van Oort, Lyanne Brouwer, Jan T. Lifjeld, Michael S. Webster, Joseph F. Welklin and Daniel T. Baldassarre

Cells 2022, 11(2), 231; https://doi.org/10.3390/cells11020231 - 11 Jan 2022

Cited by 3 | Viewed by 5567

Abstract

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the [...] Read more.

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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21 pages, 3703 KiB

Open AccessArticle

Energy Metabolism and Hyperactivation of Spermatozoa from Three Mouse Species under Capacitating Conditions

by Ester Sansegundo, Maximiliano Tourmente and Eduardo R. S. Roldan

Cells 2022, 11(2), 220; https://doi.org/10.3390/cells11020220 - 10 Jan 2022

Cited by 21 | Viewed by 3055

Abstract

Mammalian sperm differ widely in sperm morphology, and several explanations have been presented to account for this diversity. Less is known about variation in sperm physiology and cellular processes that can give sperm cells an advantage when competing to fertilize oocytes. Capacitation of [...] Read more.

Mammalian sperm differ widely in sperm morphology, and several explanations have been presented to account for this diversity. Less is known about variation in sperm physiology and cellular processes that can give sperm cells an advantage when competing to fertilize oocytes. Capacitation of spermatozoa, a process essential for mammalian fertilization, correlates with changes in motility that result in a characteristic swimming pattern known as hyperactivation. Previous studies revealed that sperm motility and velocity depend on the amount of ATP available and, therefore, changes in sperm movement occurring during capacitation and hyperactivation may involve changes in sperm bioenergetics. Here, we examine differences in ATP levels of sperm from three mouse species (genus Mus), differing in sperm competition levels, incubated under non-capacitating and capacitating conditions, to analyse relationships between energetics, capacitation, and swimming patterns. We found that, in general terms, the amount of sperm ATP decreased more rapidly under capacitating conditions. This descent was related to the development of a hyperactivated pattern of movement in two species (M. musculus and M. spicilegus) but not in the other (M. spretus), suggesting that, in the latter, temporal dynamics and energetic demands of capacitation and hyperactivation may be decoupled or that the hyperactivation pattern differs. The decrease in ATP levels during capacitation was steeper in species with higher levels of sperm competition than in those with lower levels. Our results suggest that, during capacitation, sperm consume more ATP than under non-capacitating conditions. This higher ATP consumption may be linked to higher velocity and lateral head displacement, which are associated with hyperactivated motility. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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22 pages, 6138 KiB

Open AccessFeature PaperArticle

Sperm Cyst “Looping”: A Developmental Novelty Enabling Extreme Male Ornament Evolution

by Zeeshan A. Syed, Romano Dallai, Negar Nasirzadeh, Julie A. Brill, Patrick M. O’Grady, Siyuan Cong, Ethan M. Leef, Sarah Rice, Amaar Asif, Stephanie Nguyen, Matthew M. Hansen, Steve Dorus and Scott Pitnick

Cells 2021, 10(10), 2762; https://doi.org/10.3390/cells10102762 - 15 Oct 2021

Cited by 3 | Viewed by 4677

Abstract

Postcopulatory sexual selection is credited as a principal force behind the rapid evolution of reproductive characters, often generating a pattern of correlated evolution between interacting, sex-specific traits. Because the female reproductive tract is the selective environment for sperm, one taxonomically widespread example of [...] Read more.

Postcopulatory sexual selection is credited as a principal force behind the rapid evolution of reproductive characters, often generating a pattern of correlated evolution between interacting, sex-specific traits. Because the female reproductive tract is the selective environment for sperm, one taxonomically widespread example of this pattern is the co-diversification of sperm length and female sperm-storage organ dimension. In Drosophila, having testes that are longer than the sperm they manufacture was believed to be a universal physiological constraint. Further, the energetic and time costs of developing long testes have been credited with underlying the steep evolutionary allometry of sperm length and constraining sperm length evolution in Drosophila. Here, we report on the discovery of a novel spermatogenic mechanism—sperm cyst looping—that enables males to produce relatively long sperm in short testis. This phenomenon (restricted to members of the saltans and willistoni species groups) begins early during spermatogenesis and is potentially attributable to heterochronic evolution, resulting in growth asynchrony between spermatid tails and the surrounding spermatid and somatic cyst cell membranes. By removing the allometric constraint on sperm length, this evolutionary innovation appears to have enabled males to evolve extremely long sperm for their body mass while evading delays in reproductive maturation time. On the other hand, sperm cyst looping was found to exact a cost by requiring greater total energetic investment in testes and a pronounced reduction in male lifespan. We speculate on the ecological selection pressures underlying the evolutionary origin and maintenance of this unique adaptation. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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18 pages, 1714 KiB

Open AccessArticle

Ejaculate Allocation and Sperm Characteristics Differ among Alternative Male Types in a Species of Fish with Cooperation and Competition among Unrelated Males

by Suzanne H. Alonzo, Kelly A. Stiver, Holly K. Kindsvater, Susan E. Marsh-Rollo, Bridget Nugent and Erem Kazancıoğlu

Cells 2021, 10(10), 2612; https://doi.org/10.3390/cells10102612 - 1 Oct 2021

Cited by 8 | Viewed by 2759

Abstract

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects [...] Read more.

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only “sneak” spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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13 pages, 1064 KiB

Open AccessArticle

Sperm Accumulation Induced by the Female Reproductive Fluid: Putative Evidence of Chemoattraction Using a New Tool

by Alessandro Devigili, Silvia Cattelan and Clelia Gasparini

Cells 2021, 10(9), 2472; https://doi.org/10.3390/cells10092472 - 18 Sep 2021

Cited by 7 | Viewed by 3637

Abstract

There is considerable evidence that female reproductive fluid (FRF) interacts intimately with sperm, affecting several sperm traits, including sperm motility and longevity, and ultimately fertilization success. One of the first documented interactions between FRF and sperm is the ability of FRF to attract [...] Read more.

There is considerable evidence that female reproductive fluid (FRF) interacts intimately with sperm, affecting several sperm traits, including sperm motility and longevity, and ultimately fertilization success. One of the first documented interactions between FRF and sperm is the ability of FRF to attract and guide sperm towards the eggs. However, most of the evidence of FRF’s chemoattraction proprieties comes from a limited number of taxa, specifically mammals and invertebrate broadcasting spawners. In other species, small FRF volumes and/or short sperm longevity often impose methodological difficulties resulting in this gap in chemoattraction studies in non-model species. One of the outcomes of sperm chemotaxis is sperm accumulation towards high chemoattractant concentrations, which can be easily quantified by measuring sperm concentration. Here, we tested sperm accumulation towards FRF in the zebrafish, Danio rerio, using an ad hoc developed, 3D printed, device (‘sperm selection chamber’). This easy-to-use tool allows to select and collect the sperm that swim towards a chemical gradient, and accumulate in a chemoattractant-filled well thus providing putative evidence for chemoattraction. We found that sperm accumulate in FRF in zebrafish. We also found that none of the sperm quality traits we measured (sperm swimming velocity and trajectory, sperm motility, and longevity) were correlated with this response. Together with the 3D printable project, we provide a detailed protocol for using the selection chamber. The chamber is optimized for the zebrafish, but it can be easily adapted for other species. Our device lays the foundation for a standardized way to measure sperm accumulation and in general chemoattraction, stimulating future research aimed at understanding the role and the mechanisms of sperm chemoattraction by FRF. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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28 pages, 2915 KiB

Open AccessArticle

Parthenogenesis and the Evolution of Anisogamy

by George W. A. Constable and Hanna Kokko

Cells 2021, 10(9), 2467; https://doi.org/10.3390/cells10092467 - 18 Sep 2021

Cited by 4 | Viewed by 3268

Abstract

Recently, it was pointed out that classic models for the evolution of anisogamy do not take into account the possibility of parthenogenetic reproduction, even though sex is facultative in many relevant taxa (e.g., algae) that harbour both anisogamous and isogamous species. Here, we [...] Read more.

Recently, it was pointed out that classic models for the evolution of anisogamy do not take into account the possibility of parthenogenetic reproduction, even though sex is facultative in many relevant taxa (e.g., algae) that harbour both anisogamous and isogamous species. Here, we complement this recent analysis with an approach where we assume that the relationship between progeny size and its survival may differ between parthenogenetically and sexually produced progeny, favouring either the former or the latter. We show that previous findings that parthenogenesis can stabilise isogamy relative to the obligate sex case, extend to our scenarios. We additionally investigate two different ways for one mating type to take over the entire population. First, parthenogenesis can lead to biased sex ratios that are sufficiently extreme that one type can displace the other, leading to de facto asexuality for the remaining type that now lacks partners to fuse with. This process involves positive feedback: microgametes, being numerous, lack opportunities for syngamy, and should they proliferate parthenogenetically, the next generation makes this asexual route even more prominent for microgametes. Second, we consider mutations to strict asexuality in producers of micro- or macrogametes, and show that the prospects of asexual invasion depend strongly on the mating type in which the mutation arises. Perhaps most interestingly, we also find scenarios in which parthenogens have an intrinsic survival advantage yet facultatively sexual isogamous populations are robust to the invasion of asexuals, despite us assuming no genetic benefits of recombination. Here, equal contribution from both mating types to zygotes that are sufficiently well provisioned can outweigh the additional costs associated with syngamy. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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14 pages, 628 KiB

Open AccessArticle

Selection on Sperm Count, but Not on Sperm Morphology or Velocity, in a Wild Population of Anolis Lizards

by Ariel F. Kahrl, Matthew C. Kustra, Aaron M. Reedy, Rachana S. Bhave, Heidi A. Seears, Daniel A. Warner and Robert M. Cox

Cells 2021, 10(9), 2369; https://doi.org/10.3390/cells10092369 - 9 Sep 2021

Cited by 8 | Viewed by 3065

Abstract

Sperm competition is a widespread phenomenon that shapes male reproductive success. Ejaculates present many potential targets for postcopulatory selection (e.g., sperm morphology, count, and velocity), which are often highly correlated and potentially subject to complex multivariate selection. Although multivariate selection on ejaculate traits [...] Read more.

Sperm competition is a widespread phenomenon that shapes male reproductive success. Ejaculates present many potential targets for postcopulatory selection (e.g., sperm morphology, count, and velocity), which are often highly correlated and potentially subject to complex multivariate selection. Although multivariate selection on ejaculate traits has been observed in laboratory experiments, it is unclear whether selection is similarly complex in wild populations, where individuals mate frequently over longer periods of time. We measured univariate and multivariate selection on sperm morphology, sperm count, and sperm velocity in a wild population of brown anole lizards (Anolis sagrei). We conducted a mark-recapture study with genetic parentage assignment to estimate individual reproductive success. We found significant negative directional selection and negative quadratic selection on sperm count, but we did not detect directional or quadratic selection on any other sperm traits, nor did we detect correlational selection on any trait combinations. Our results may reflect pressure on males to produce many small ejaculates and mate frequently over a six-month reproductive season. This study is the first to measure multivariate selection on sperm traits in a wild population and provides an interesting contrast to experimental studies of external fertilizers, which have found complex multivariate selection on sperm phenotypes. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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17 pages, 1831 KiB

Open AccessArticle

Apical Sperm Hook Morphology Is Linked to Sperm Swimming Performance and Sperm Aggregation in Peromyscus Mice

by Kristin A. Hook, Lauren M. Wilke and Heidi S. Fisher

Cells 2021, 10(9), 2279; https://doi.org/10.3390/cells10092279 - 1 Sep 2021

Cited by 10 | Viewed by 4179

Abstract

Mammals exhibit a tremendous amount of variation in sperm morphology and despite the acknowledgement of sperm structural diversity across taxa, its functional significance remains poorly understood. Of particular interest is the sperm of rodents. While most Eutherian mammal spermatozoa are relatively simple cells [...] Read more.

Mammals exhibit a tremendous amount of variation in sperm morphology and despite the acknowledgement of sperm structural diversity across taxa, its functional significance remains poorly understood. Of particular interest is the sperm of rodents. While most Eutherian mammal spermatozoa are relatively simple cells with round or paddle-shaped heads, rodent sperm are often more complex and, in many species, display a striking apical hook. The function of the sperm hook remains largely unknown, but it has been hypothesized to have evolved as an adaptation to inter-male sperm competition and thus has been implicated in increased swimming efficiency or in the formation of collective sperm movements. Here we empirically test these hypotheses within a single lineage of Peromyscus rodents, in which closely related species naturally vary in their mating systems, sperm head shapes, and propensity to form sperm aggregates of varying sizes. We performed sperm morphological analyses as well as in vitro analyses of sperm aggregation and motility to examine whether the sperm hook (i) morphologically varies across these species and (ii) associates with sperm competition, aggregation, or motility. We demonstrate inter-specific variation in the sperm hook and then show that hook width negatively associates with sperm aggregation and sperm swimming speed, signifying that larger hooks may be a hindrance to sperm movement within this group of mice. Finally, we confirmed that the sperm hook hinders motility within a subset of Peromyscus leucopus mice that spontaneously produced sperm with no or highly abnormal hooks. Taken together, our findings suggest that any adaptive value of the sperm hook is likely associated with a function other than inter-male sperm competition, such as interaction with ova or cumulous cells during fertilization, or migration through the complex female reproductive tract. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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22 pages, 2695 KiB

Open AccessArticle

Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe

by Leon Green, Apostolos Apostolou, Ellika Faust, Kajsa Palmqvist, Jane W. Behrens, Jonathan N. Havenhand, Erica H. Leder and Charlotta Kvarnemo

Cells 2021, 10(7), 1743; https://doi.org/10.3390/cells10071743 - 9 Jul 2021

Cited by 9 | Viewed by 4551

Abstract

For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across [...] Read more.

For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across a wide salinity range. The family also contains several wide-spread invasive species. To better understand how these fishes tolerate such varying conditions, we measured sperm performance in relation to salinity from a freshwater and a brackish population within their ancestral Ponto-Caspian region of the round goby, Neogobius melanostomus. These two ancestral populations were then compared to nine additional invaded sites across northern Europe, both in terms of their sperm traits and by using genomic SNP markers. Our results show clear patterns of ancestral adaptations to freshwater and brackish salinities in their sperm performance. Population genomic analyses show that the ancestral ecotypes have generally established themselves in environments that fit their sperm adaptations. Sites close to ports with intense shipping show that both outbreeding and admixture can affect the sperm performance of a population in a given salinity. Rapid adaptation to local conditions is also supported at some sites. Historical and contemporary evolution in the traits of the round goby sperm cells is tightly linked to the population and seascape genomics as well as biogeographic processes in these invasive fishes. Since the risk of a population establishing in an area is related to the genotype by environment match, port connectivity and the ancestry of the round goby population can likely be useful for predicting the species spread. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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16 pages, 1456 KiB

Open AccessArticle

Food Limitation but Not Enhanced Rates of Ejaculate Production Imposes Reproductive and Survival Costs to Male Crickets

by Saoirse McMahon, Magdalena Matzke and Cristina Tuni

Cells 2021, 10(6), 1498; https://doi.org/10.3390/cells10061498 - 15 Jun 2021

Cited by 5 | Viewed by 2753

Abstract

Estimating costs of ejaculate production is challenging. Metabolic investment in ejaculates may come at the expense of other physiological functions and may negatively affect future reproduction and/or survival. These trade-offs are especially likely to occur under constrained resource pools (e.g., poor nutrition). Here, [...] Read more.

Estimating costs of ejaculate production is challenging. Metabolic investment in ejaculates may come at the expense of other physiological functions and may negatively affect future reproduction and/or survival. These trade-offs are especially likely to occur under constrained resource pools (e.g., poor nutrition). Here, we investigated costs of ejaculate production via trade-offs in the field cricket Gryllus bimaculatus. We experimentally increased rates of ejaculate production, while keeping an unmanipulated group, in adult males kept at high and low feeding regimes and tested the effects of our treatments on (i) somatic maintenance (i.e., changes in male body mass), (ii) future reproduction (i.e., the likelihood of producing a spermatophore and the viability of its sperm), and (iii) lifetime survival and longevity. We predicted investment in ejaculates to impinge upon all measured responses, especially in low-fed individuals. Instead, we only found negative effects of food limitation, suggesting low or undetectable costs of spermatophore production. High mating rates may select for males to maximize their capacity of ejaculate production, making ejaculate traits less prone to trade-offs with other fitness-related life history traits. Nevertheless, males were impaired due to nutrient deficiency in producing viable ejaculates, suggesting condition-dependent costs for ejaculate production. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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14 pages, 630 KiB

Open AccessArticle

Longer Sperm Swim More Slowly in the Canary Islands Chiffchaff

by Emily R. A. Cramer, Eduardo Garcia-del-Rey, Lars Erik Johannessen, Terje Laskemoen, Gunnhild Marthinsen, Arild Johnsen and Jan T. Lifjeld

Cells 2021, 10(6), 1358; https://doi.org/10.3390/cells10061358 - 31 May 2021

Cited by 9 | Viewed by 5581

Abstract

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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11 pages, 1290 KiB

Open AccessArticle

Can Sexual Selection Drive the Evolution of Sperm Cell Structure?

by Leigh W. Simmons and Francisco Garcia-Gonzalez

Cells 2021, 10(5), 1227; https://doi.org/10.3390/cells10051227 - 17 May 2021

Cited by 3 | Viewed by 3222

Abstract

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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13 pages, 482 KiB

Open AccessArticle

Weapons Evolve Faster Than Sperm in Bovids and Cervids

by Charel Reuland, Leigh W. Simmons, Stefan Lüpold and John L. Fitzpatrick

Cells 2021, 10(5), 1062; https://doi.org/10.3390/cells10051062 - 29 Apr 2021

Cited by 5 | Viewed by 3138

Abstract

In polyandrous species, males face reproductive competition both before and after mating. Sexual selection thus shapes the evolution of both pre- and postcopulatory traits, creating competing demands on resource allocation to different reproductive episodes. Traits subject to strong selection exhibit accelerated rates of [...] Read more.

In polyandrous species, males face reproductive competition both before and after mating. Sexual selection thus shapes the evolution of both pre- and postcopulatory traits, creating competing demands on resource allocation to different reproductive episodes. Traits subject to strong selection exhibit accelerated rates of phenotypic divergence, and examining evolutionary rates may inform us about the relative importance and potential fitness consequences of investing in traits under either pre- or postcopulatory sexual selection. Here, we used a comparative approach to assess evolutionary rates of key competitive traits in two artiodactyl families, bovids (family Bovidae) and cervids (family Cervidae), where male–male competition can occur before and after mating. We quantified and compared evolutionary rates of male weaponry (horns and antlers), body size/mass, testes mass, and sperm morphometrics. We found that weapons evolve faster than sperm dimensions. In contrast, testes and body mass evolve at similar rates. These results suggest strong, but differential, selection on both pre- and postcopulatory traits in bovids and cervids. Furthermore, we documented distinct evolutionary rates among different sperm components, with sperm head and midpiece evolving faster than the flagellum. Finally, we demonstrate that, despite considerable differences in weapon development between bovids and cervids, the overall evolutionary patterns between these families were broadly consistent. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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20 pages, 7078 KiB

Open AccessArticle

Molecular Evolution of CatSper in Mammals and Function of Sperm Hyperactivation in Gray Short-Tailed Opossum

by Jae Yeon Hwang, Jamie Maziarz, Günter P. Wagner and Jean-Ju Chung

Cells 2021, 10(5), 1047; https://doi.org/10.3390/cells10051047 - 29 Apr 2021

Cited by 11 | Viewed by 5716

Abstract

Males have evolved species-specifical sperm morphology and swimming patterns to adapt to different fertilization environments. In eutherians, only a small fraction of the sperm overcome the diverse obstacles in the female reproductive tract and successfully migrate to the fertilizing site. Sperm arriving at [...] Read more.

Males have evolved species-specifical sperm morphology and swimming patterns to adapt to different fertilization environments. In eutherians, only a small fraction of the sperm overcome the diverse obstacles in the female reproductive tract and successfully migrate to the fertilizing site. Sperm arriving at the fertilizing site show hyperactivated motility, a unique motility pattern displaying asymmetric beating of sperm flagella with increased amplitude. This motility change is triggered by Ca²⁺ influx through the sperm-specific ion channel, CatSper. However, the current understanding of the CatSper function and its molecular regulation is limited in eutherians. Here, we report molecular evolution and conservation of the CatSper channel in the genome throughout eutherians and marsupials. Sequence analyses reveal that CatSper proteins are slowly evolved in marsupials. Using an American marsupial, gray short-tailed opossum (Monodelphis domestica), we demonstrate the expression of CatSper in testes and its function in hyperactivation and unpairing of sperm. We demonstrate that a conserved IQ-like motif in CatSperζ is required for CatSperζ interaction with the pH-tuned Ca²⁺ sensor, EFCAB9, for regulating CatSper activity. Recombinant opossum EFCAB9 can interact with mouse CatSperζ despite high sequence divergence of CatSperζ among CatSper subunits in therians. Our finding suggests that molecular characteristics and functions of CatSper are evolutionarily conserved in gray short-tailed opossum, unraveling the significance of sperm hyperactivation and fertilization in marsupials for the first time. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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23 pages, 1695 KiB

Open AccessArticle

Measuring Pre- and Post-Copulatory Sexual Selection and Their Interaction in Socially Monogamous Species with Extra-Pair Paternity

by Emily Rebecca Alison Cramer

Cells 2021, 10(3), 620; https://doi.org/10.3390/cells10030620 - 11 Mar 2021

Cited by 7 | Viewed by 4455

Abstract

When females copulate with multiple males, pre- and post-copulatory sexual selection may interact synergistically or in opposition. Studying this interaction in wild populations is complex and potentially biased, because copulation and fertilization success are often inferred from offspring parentage rather than being directly [...] Read more.

When females copulate with multiple males, pre- and post-copulatory sexual selection may interact synergistically or in opposition. Studying this interaction in wild populations is complex and potentially biased, because copulation and fertilization success are often inferred from offspring parentage rather than being directly measured. Here, I simulated 15 species of socially monogamous birds with varying levels of extra-pair paternity, where I could independently cause a male secondary sexual trait to improve copulation success, and a sperm trait to improve fertilization success. By varying the degree of correlation between the male and sperm traits, I show that several common statistical approaches, including univariate selection gradients and paired t-tests comparing extra-pair males to the within-pair males they cuckolded, can give highly biased results for sperm traits. These tests should therefore be avoided for sperm traits in socially monogamous species with extra-pair paternity, unless the sperm trait is known to be uncorrelated with male trait(s) impacting copulation success. In contrast, multivariate selection analysis and a regression of the proportion of extra-pair brood(s) sired on the sperm trait of the extra-pair male (including only broods where the male sired ≥1 extra-pair offspring) were unbiased, and appear likely to be unbiased under a broad range of conditions for this mating system. In addition, I investigated whether the occurrence of pre-copulatory selection impacted the strength of post-copulatory selection, and vice versa. I found no evidence of an interaction under the conditions simulated, where the male trait impacted only copulation success and the sperm trait impacted only fertilization success. Instead, direct selection on each trait was independent of whether the other trait was under selection. Although pre- and post-copulatory selection strength was independent, selection on the two traits was positively correlated across species because selection on both traits increased with the frequency of extra-pair copulations in these socially monogamous species. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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14 pages, 785 KiB

Open AccessArticle

The Legacy of Parker, Baker and Smith 1972: Gamete Competition, the Evolution of Anisogamy, and Model Robustness

by Jussi Lehtonen

Cells 2021, 10(3), 573; https://doi.org/10.3390/cells10030573 - 5 Mar 2021

Cited by 1 | Viewed by 3430

Abstract

The evolution of anisogamy or gamete size dimorphism is a fundamental transition in evolutionary history, and it is the origin of the female and male sexes. Although mathematical models attempting to explain this transition have been published as early as 1932, the 1972 [...] Read more.

The evolution of anisogamy or gamete size dimorphism is a fundamental transition in evolutionary history, and it is the origin of the female and male sexes. Although mathematical models attempting to explain this transition have been published as early as 1932, the 1972 model of Parker, Baker, and Smith is considered to be the first explanation for the evolution of anisogamy that is consistent with modern evolutionary theory. The central idea of the model is ingenious in its simplicity: selection simultaneously favours large gametes for zygote provisioning, and small gametes for numerical competition, and under certain conditions the outcome is anisogamy. In this article, I derive novel analytical solutions to a 2002 game theoretical update of the 1972 anisogamy model, and use these solutions to examine its robustness to variation in its central assumptions. Combining new results with those from earlier papers, I find that the model is quite robust to variation in its central components. This kind of robustness is crucially important in a model for an early evolutionary transition where we may only have an approximate understanding of constraints that the different parts of the model must obey. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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12 pages, 1053 KiB

Open AccessArticle

Expression of Mst89B and CG31287 is Needed for Effective Sperm Storage and Egg Fertilization in Drosophila

by Gurman Grewal, Bahar Patlar and Alberto Civetta

Cells 2021, 10(2), 289; https://doi.org/10.3390/cells10020289 - 1 Feb 2021

Cited by 5 | Viewed by 2902

Abstract

In Drosophila, male reproductive fitness can be affected by any number of processes, ranging from development of gametes, transfer to and storage of mature sperm within the female sperm storage organs, and utilization of sperm for fertilization. We have previously identified the [...] Read more.

In Drosophila, male reproductive fitness can be affected by any number of processes, ranging from development of gametes, transfer to and storage of mature sperm within the female sperm storage organs, and utilization of sperm for fertilization. We have previously identified the 89B cytogenetic map position of D. melanogaster as a hub for genes that effect male paternity success when disturbed. Here, we used RNA interference to test 11 genes that are highly expressed in the testes and located within the 89B region for their role in sperm competition and male fecundity when their expression is perturbed. Testes-specific knockdown (KD) of bor and CSN5 resulted in complete sterility, whereas KD of CG31287, Manf and Mst89B, showed a breakdown in sperm competitive success when second to mate (P2 < 0.5) and reduced fecundity in single matings. The low fecundity of Manf KD is explained by a significant reduction in the amount of mature sperm produced. KD of Mst89B and CG31287 does not affect sperm production, sperm transfer into the female bursa or storage within 30 min after mating. Instead, a significant reduction of sperm in female storage is observed 24 h after mating. Egg hatchability 24 h after mating is also drastically reduced for females mated to Mst89B or CG31287 KD males, and this reduction parallels the decrease in fecundity. We show that normal germ-line expression of Mst89B and CG31287 is needed for effective sperm usage and egg fertilization. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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Review

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12 pages, 2056 KiB

Open AccessReview

Atypical Centriolar Composition Correlates with Internal Fertilization in Fish

by Katerina Turner, Nisha Solanki, Hassan O. Salouha and Tomer Avidor-Reiss

Cells 2022, 11(5), 758; https://doi.org/10.3390/cells11050758 - 22 Feb 2022

Cited by 6 | Viewed by 5361

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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22 pages, 6994 KiB

Open AccessReview

Fisher vs. the Worms: Extraordinary Sex Ratios in Nematodes and the Mechanisms that Produce Them

by Justin Van Goor, Diane C. Shakes and Eric S. Haag

Cells 2021, 10(7), 1793; https://doi.org/10.3390/cells10071793 - 15 Jul 2021

Cited by 12 | Viewed by 4274

Abstract

Parker, Baker, and Smith provided the first robust theory explaining why anisogamy evolves in parallel in multicellular organisms. Anisogamy sets the stage for the emergence of separate sexes, and for another phenomenon with which Parker is associated: sperm competition. In outcrossing taxa with [...] Read more.

Parker, Baker, and Smith provided the first robust theory explaining why anisogamy evolves in parallel in multicellular organisms. Anisogamy sets the stage for the emergence of separate sexes, and for another phenomenon with which Parker is associated: sperm competition. In outcrossing taxa with separate sexes, Fisher proposed that the sex ratio will tend towards unity in large, randomly mating populations due to a fitness advantage that accrues in individuals of the rarer sex. This creates a vast excess of sperm over that required to fertilize all available eggs, and intense competition as a result. However, small, inbred populations can experience selection for skewed sex ratios. This is widely appreciated in haplodiploid organisms, in which females can control the sex ratio behaviorally. In this review, we discuss recent research in nematodes that has characterized the mechanisms underlying highly skewed sex ratios in fully diploid systems. These include self-fertile hermaphroditism and the adaptive elimination of sperm competition factors, facultative parthenogenesis, non-Mendelian meiotic oddities involving the sex chromosomes, and environmental sex determination. By connecting sex ratio evolution and sperm biology in surprising ways, these phenomena link two “seminal” contributions of G. A. Parker. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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19 pages, 3320 KiB

Open AccessReview

Co-Adaptation of Physical Attributes of the Mammalian Female Reproductive Tract and Sperm to Facilitate Fertilization

by Chih-Kuan Tung and Susan S. Suarez

Cells 2021, 10(6), 1297; https://doi.org/10.3390/cells10061297 - 24 May 2021

Cited by 22 | Viewed by 8605

Abstract

The functions of the female reproductive tract not only encompass sperm migration, storage, and fertilization, but also support the transport and development of the fertilized egg through to the birth of offspring. Further, because the tract is open to the external environment, it [...] Read more.

The functions of the female reproductive tract not only encompass sperm migration, storage, and fertilization, but also support the transport and development of the fertilized egg through to the birth of offspring. Further, because the tract is open to the external environment, it must also provide protection against invasive pathogens. In biophysics, sperm are considered “pusher microswimmers”, because they are propelled by pushing fluid behind them. This type of swimming by motile microorganisms promotes the tendency to swim along walls and upstream in gentle fluid flows. Thus, the architecture of the walls of the female tract, and the gentle flows created by cilia, can guide sperm migration. The viscoelasticity of the fluids in the tract, such as mucus secretions, also promotes the cooperative swimming of sperm that can improve fertilization success; at the same time, the mucus can also impede the invasion of pathogens. This review is focused on how the mammalian female reproductive tract and sperm interact physically to facilitate the movement of sperm to the site of fertilization. Knowledge of female/sperm interactions can not only explain how the female tract can physically guide sperm to the fertilization site, but can also be applied for the improvement of in vitro fertilization devices. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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Other

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16 pages, 1892 KiB

Open AccessOpinion

How Soon Hath Time… A History of Two “Seminal” Publications

by Geoff A. Parker

Cells 2021, 10(2), 287; https://doi.org/10.3390/cells10020287 - 1 Feb 2021

Cited by 8 | Viewed by 3753

Abstract

This review documents the history of the two papers written half a century ago that relate to this special issue of Cells. The first, “Sperm competition and its evolutionary consequences in the insects” (Biological Reviews, 1970), stressed that sexual selection [...] Read more.

This review documents the history of the two papers written half a century ago that relate to this special issue of Cells. The first, “Sperm competition and its evolutionary consequences in the insects” (Biological Reviews, 1970), stressed that sexual selection continues after ejaculation, resulting in many adaptations (e.g., postcopulatory guarding phases, copulatory plugs, seminal fluid components that modify female reproduction, and optimal ejaculation strategies), an aspect not considered by Darwin in his classic treatise of 1871. Sperm competition has subsequently been studied in many taxa, and post-copulatory sexual selection is now considered an important sequel to Darwinian pre-copulatory sexual selection. The second, “The origin and evolution of gamete dimorphism and the male-female phenomenon” (Journal of Theoretical Biology, 1972) showed how selection, based on gamete competition between individuals, can give rise to anisogamy in an isogamous broadcast spawning ancestor. This theory, which has subsequently been developed in various ways, is argued to form the most powerful explanation of why there are two sexes in most multicellular organisms. Together, the two papers have influenced our general understanding of the evolutionary differentiation of the two forms of gametic cells, and the divergence of sexual strategies between males and females under sexual selection. Full article

(This article belongs to the Special Issue Origin and Evolution of Sperm Cells—An Issue in Honor of Geoff A. Parker)

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