scholarly journals Collective sperm movements in Peromyscus mice are shaped by phylogenetic history and post-copulatory sexual selection

2020 ◽  
Author(s):  
Kristin A. Hook ◽  
W. David Weber ◽  
Heidi S. Fisher

AbstractIn some species, sperm form motile, coordinated groups as they migrate through the female reproductive tract. Collective sperm migration is posited to have evolved to improve sperm swimming performance, and thus may be beneficial in a competitive context, but limited evidence supports this theory. Here we investigate sperm aggregation across closely-related species of Peromyscus mice that naturally vary by mating system. We find that phylogenetic history predicts the likelihood that sperm will aggregate but that variation in aggregate size negatively associates with relative testis size, suggesting that sperm competition has a stabilizing effect on this trait. Moreover, we show that sperm aggregation is not kinematically beneficial for all species, and we hypothesize that swimming performance is dependent on the orientation and composition of sperm groups. To test this, we compared sperm from the two sister-species that aggregate most frequently and find that sperm of the species that evolved under intense sperm competition forms aggregates with efficient geometry more frequently than sperm from its monogamous congener. Together, our results are consistent with the hypothesis that sperm aggregation evolved to improve motility in a competitive context; however, when monogamy evolved secondarily, relaxed sexual selection allowed for less efficient strategies to persist.

Author(s):  
Patricia L.R. Brennan ◽  
Dara N. Orbach

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.


Cells ◽  
2021 ◽  
Vol 10 (9) ◽  
pp. 2279
Author(s):  
Kristin A. Hook ◽  
Lauren M. Wilke ◽  
Heidi S. Fisher

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.


2007 ◽  
Vol 274 (1612) ◽  
pp. 983-988 ◽  
Author(s):  
Paul F Rugman-Jones ◽  
Paul E Eady

Conspecific sperm precedence (CSP) has been identified as an important post-copulatory, pre-zygotic mechanism that can act to reduce gene flow between populations. The evolution of CSP is thought to have arisen as a by-product of male and female coevolution in response to intraspecific post-copulatory sexual selection. However, little is known about the mechanisms that generate CSP. When Callosobruchus subinnotatus females copulate with both C. subinnotatus and Callosobruchus maculatus males, regardless of mating order, the majority of eggs are fertilized by conspecific sperm. The low number of heterospecific fertilizations does not result from general differences in the viability of sperm in the female reproductive tract, as heterospecific sperm fertilized equivalent numbers of eggs as conspecific sperm in the absence of sperm competition. Instead, CSP results from disadvantages to heterospecific sperm that are manifest only when in competition with conspecific sperm. CSP in C. subinnotatus appears to result from two, not mutually exclusive, mechanisms. First, conspecific sperm are better able to displace heterospecific sperm from female storage. Second, conspecific sperm achieve disproportionately higher numbers of fertilizations relative to their proportional representation in the fertilization set. Thus, we provide evidence of differential sperm use from the female spermatheca.


2020 ◽  
Vol 375 (1813) ◽  
pp. 20200071 ◽  
Author(s):  
Martin D. Garlovsky ◽  
Leeban H. Yusuf ◽  
Michael G. Ritchie ◽  
Rhonda R. Snook

Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here , we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue ‘Fifty years of sperm competition’.


Author(s):  
Zachariah Wylde ◽  
Angela Crean ◽  
Russell Bonduriansky

Abstract Ejaculate traits can be sexually selected and often exhibit heightened condition-dependence. However, the influence of sperm competition risk in tandem with condition-dependent ejaculate allocation strategies is relatively unstudied. Because ejaculates are costly to produce, high-condition males may be expected to invest more in ejaculates when sperm competition risk is greater. We examined the condition-dependence of ejaculate size by manipulating nutrient concentration in the juvenile (larval) diet of the neriid fly Telostylinus angusticollis. Using a fully factorial design we also examined the effects of perceived sperm competition risk (manipulated by allowing males to mate first or second) on the quantity of ejaculate transferred and stored in the three spermathecae of the female reproductive tract. To differentiate male ejaculates, we fed males nontoxic rhodamine fluorophores (which bind to proteins in the body) prior to mating, labeling their sperm red or green. We found that high-condition males initiated mating more quickly and, when mating second, transferred more ejaculate to both of the female’s posterior spermathecae. This suggests that males allocate ejaculates strategically, with high-condition males elevating their ejaculate investment only when facing sperm competition. More broadly, our findings suggest that ejaculate allocation strategies can incorporate variation in both condition and perceived risk of sperm competition.


Behaviour ◽  
2006 ◽  
Vol 143 (5) ◽  
pp. 643-658 ◽  
Author(s):  
Ludovic Arnaud ◽  
Giorgina Bernasconi ◽  
Yves Brostaux ◽  
Eric P. Meyer

AbstractIn polyandrous insects, postcopulatory sexual selection is a pervasive evolutionary force favouring male and female traits that allow control of offspring paternity. Males may influence paternity through adaptations for sperm competition, and females through adaptations facilitating cryptic female choice. Yet, the mechanisms are often complex, involving behaviour, physiology or morphology, and they are difficult to identify. In red flour beetles (Tribolium castaneum), paternity varies widely, and evidence suggests that both male and female traits influence the outcome of sperm competition. To test the role of spermathecal morphology and of sperm storage processes on the outcome of sperm competition, we mated each of 26 virgin females with two males, one of which carrying a phenotypic marker to assign offspring paternity. We manipulated the interval between mating with the first and the second male, to create different conditions of sperm storage (overlapping and non-overlapping) in the female reproductive tract. To investigate the role of sperm storage more closely, we examined the relationship between paternity and spermathecal morphology in a subset of 14 experimental females. In addition, we also characterized variation in spermathecal morphology in three different strains, wildtype, Chicago black and Reindeer. No significant influence of the intermating interval was found on the paternity of the focal male, although the direction of the difference was in the expected direction of higher last male paternity for longer intervals. Moreover, paternity was not significantly associated with spermathecal morphology, although spermathecal volume, complexity, and tubule width varied significantly and substantially among individuals in all investigated strains.


2018 ◽  
Vol 855 ◽  
pp. 408-420 ◽  
Author(s):  
G. Cupples ◽  
R. J. Dyson ◽  
D. J. Smith

Very low Reynolds number propulsion is a topic of enduring interest due to its importance in biological systems such as sperm migration in the female reproductive tract. Motivated by the fibrous nature of cervical mucus, several recent studies have considered the effect of anisotropic rheology; these studies have generally employed the classical swimming sheet model of G. I. Taylor. The models of Cupples et al. (J. Fluid Mech. vol. 812, 2017, pp. 501–524) and Shi & Powers (Phys. Rev. Fluids vol. 2, 2017, 123102) consider related problems which in a common limit (passive, slightly anisotropic) make different predictions regarding how swimming speed depends on alignment angle. In the present paper we find that this discrepancy is due to missing terms in the analysis of Cupples et al., and that when these terms are correctly included, the models agree in their common limit. We further explore the predictions of the corrected model for both passive and active cases; it is found that for certain combinations of alignment angle and activity parameter, propulsion is halted; in other cases the small amplitude asymptotic expansion is no longer valid, motivating future numerical study.


Author(s):  
Leigh W. Simmons

Darwin viewed sexual selection as a process that ended with mate acquisition, assuming that females are fundamentally monogamous, mating with just one male. ‘Sexual selection after mating’, however, shows this assumption to be false. Sexual selection continues long after the physical act of mating is over, as sperm compete inside a female’s reproductive tract and females bias the paternity of their young by selectively using sperm from particular males. Multiple mating by females has turned out to be ubiquitous across animal taxa. The far-reaching evolutionary consequences of sperm competition and cryptic female choice for the evolution of reproductive traits are examined, from the gametes themselves to the adult organisms producing them.


2020 ◽  
Vol 375 (1813) ◽  
pp. 20200079
Author(s):  
Christopher R. Friesen ◽  
Ariel F. Kahrl ◽  
Mats Olsson

Multiple paternity is ubiquitous within the polyphyletic group called ‘reptiles', especially within the lizards and snakes. Therefore, the probability of sperm competition occurring, and being intense, is high. Squamates exhibit a diversity of tactics to ensure fertilization success in the face of sperm competition. The duration of female sperm storage, which can be many months and even years in some species, remains an enigma. Here, we emphasize some mechanisms that might affect patterns of paternity, the source and function of ejaculates and features of the female reproductive tract that may aid in long-term sperm storage. In doing so, we present a new analysis of the relationship between sperm size, the strength of sperm competition and the duration of female sperm storage. Lizards and snakes are a diverse group that has provided many excellent models for the study of an array of life-history strategies. However, when it comes to postcopulatory sexual selection, there is much left to discover. This article is part of the theme issue ‘Fifty years of sperm competition'.


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