scholarly journals Sperm Numbers as a Paternity Guard in a Wild Bird

Cells ◽  
2022 ◽  
Vol 11 (2) ◽  
pp. 231
Author(s):  
Melissah Rowe ◽  
Annabel van Oort ◽  
Lyanne Brouwer ◽  
Jan T. Lifjeld ◽  
Michael S. Webster ◽  
...  

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.

2021 ◽  
Author(s):  
Jake Galvin ◽  
Erica Larson ◽  
Sevan Yedigarian ◽  
Mohammad Rahman ◽  
Kirill Borziak ◽  
...  

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.


2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Lennart Winkler ◽  
Anna K. Lindholm ◽  
Steven A. Ramm ◽  
Andreas Sutter

AbstractThe vast variation observed in genital morphology is a longstanding puzzle in evolutionary biology. Studies showing that the morphology of the mammalian baculum (penis bone) can covary with a male’s paternity success indicate a potential impact of baculum morphology on male fitness, likely through influencing sperm competition outcomes. We therefore measured the size (measurements of length and width) and shape (geometric morphometric measurements) of the bacula of male house mice used in previously published sperm competition experiments, in which two males mated successively with the same female in staged matings. This enabled us to correlate baculum morphology with sperm competition success, incorporating potential explanatory variables related to copulatory plugs, male mating behavior and a selfish genetic element that influences sperm motility. We found that a wider baculum shaft increased a male’s paternity share when mating first, but not when mating second with a multiply-mating female. Geometric morphometric shape measurements were not clearly associated with fertilization success for either male. We found limited evidence that the effect of baculum morphology on male fertilization success was altered by experimental removal of the copulatory plug. Furthermore, neither genetic differences in sperm motility, nor covariation with male mating behavior mediated the effect of baculum morphology on male fertilization success. Taken together with previous findings, the mating-order effects we found here suggest that baculum-mediated stimulation by the first male might be particularly important for fertilization.


2005 ◽  
Vol 83 (12) ◽  
pp. 1638-1642 ◽  
Author(s):  
Albrecht I Schulte-Hostedde ◽  
Gary Burness

Sperm competition results in the evolution of ejaculate characteristics such as high sperm density, high motility, and fast sperm swimming speed. A fundamental assumption of sperm competition theory is that ejaculates with high motility and fast-swimming sperm have an advantage with respect to fertilization success. We tested this assumption by studying the fertilization dynamics of alternative mating tactics (cuckolders and parentals) of male bluegill (Lepomis macrochirus Rafinesque, 1819). Sneakers (cuckolders) have faster swimming sperm and a higher proportion of motile sperm immediately following sperm activation than do parentals; however, these variables decline more quickly over time in sneaker sperm than in the sperm of parental males. We used a controlled fertilization experiment to test the prediction that parental males will have higher fertilization success than sneakers late in the sperm activation cycle because of the reduced rate of decline in ejaculate quality over time. We found that as the time from sperm activation increases parental sperm fertilizes more eggs than the sperm of sneakers. Our results support the idea that fertilization success is higher when ejaculates contain a higher proportion of either motile sperm or faster swimming sperm, all else being equal. In addition, after controlling for time from sperm activation, we found a significant bias in fertilization success toward parental males, suggesting that cryptic female choice might play a role in fertilization dynamics.


Parasitology ◽  
2014 ◽  
Vol 141 (7) ◽  
pp. 934-939
Author(s):  
D. ANDREOU ◽  
D. P. BENESH

SUMMARYSimultaneous hermaphrodites maximize their fitness by optimizing their investment into male or female functions. Allocation of resources to male function (tissues, traits, and/or behaviours increasing paternity) is predicted to increase as density, and the associated level of sperm competition, increases. We tested whether the simultaneous hermaphroditic cestode Schistocephalus solidus uses cues of potential partner densities in its fish intermediate host to improve its male reproductive success in the final host. We had two worms, one originating from a multiple infection in the fish intermediate host and one from a single infection, sequentially compete to fertilize the eggs of a third worm. The fertilization rates of the two competitors nearly always differed from the 50–50 null expectation, sometimes considerably, implying there was a ‘winner’ in each experimental competition. However, we did not find a significant effect of density in the fish host (single vs multiple) or mating order on paternity. Additional work will be needed to identify the traits and environmental conditions that explain the high variance in male reproductive success observed in this experiment.


2013 ◽  
Vol 280 (1772) ◽  
pp. 20132047 ◽  
Author(s):  
Jonathan P. Evans ◽  
Patrice Rosengrave ◽  
Clelia Gasparini ◽  
Neil J. Gemmell

Disentangling the relative roles of males, females and their interactive effects on competitive fertilization success remains a challenge in sperm competition. In this study, we apply a novel experimental framework to an ideally suited externally fertilizing model system in order to delineate these roles. We focus on the chinook salmon, Oncorhynchus tshawytscha , a species in which ovarian fluid (OF) has been implicated as a potential arbiter of cryptic female choice for genetically compatible mates. We evaluated this predicted sexually selected function of OF using a series of factorial competitive fertilization trials. Our design involved a series of 10 factorial crosses, each involving two ‘focal’ rival males whose sperm competed against those from a single ‘standardized’ (non-focal) rival for a genetically uniform set of eggs in the presence of OF from two focal females. This design enabled us to attribute variation in competitive fertilization success among focal males, females (OF) and their interacting effects, while controlling for variation attributable to differences in the sperm competitive ability of rival males, and male-by-female genotypic interactions. Using this experimental framework, we found that variation in sperm competitiveness could be attributed exclusively to differences in the sperm competitive ability of focal males, a conclusion supported by subsequent analyses revealing that variation in sperm swimming velocity predicts paternity success. Together, these findings provide evidence that variation in paternity success can be attributed to intrinsic differences in the sperm competitive ability of rival males, and reveal that sperm swimming velocity is a key target of sexual selection.


2016 ◽  
Vol 283 (1843) ◽  
pp. 20161883 ◽  
Author(s):  
Viola Pavlova ◽  
Jacob Nabe-Nielsen ◽  
Rune Dietz ◽  
Christian Sonne ◽  
Volker Grimm

Polar bears ( Ursus maritimus ) from East Greenland and Svalbard exhibited very high concentrations of polychlorinated biphenyls (PCBs) in the 1980s and 1990s. In Svalbard, slow population growth during that period was suspected to be linked to PCB contamination. In this case study, we explored how PCBs could have impacted polar bear population growth and/or male reproductive success in Svalbard during the mid-1990s by reducing the fertility of contaminated males. A dose–response relationship linking the effects of PCBs to male polar bear fertility was extrapolated from studies of the effects of PCBs on sperm quality in rodents. Based on this relationship, an individual-based model of bear interactions during the breeding season predicted fertilization success under alternative assumptions regarding male–male competition for females. Contamination reduced pregnancy rates by decreasing the availability of fertile males, thus triggering a mate-finding Allee effect, particularly when male–male competition for females was limited or when infertile males were able to compete with fertile males for females. Comparisons of our model predictions on age-dependent reproductive success of males with published empirical observations revealed that the low representation of 10–14-year-old males among breeding males documented in Svalbard in mid-1990s could have resulted from PCB contamination. We conclude that contamination-related male infertility may lead to a reduction in population growth via an Allee effect. The magnitude of the effect is largely dependent on the population-specific mating system. In eco-toxicological risk assessments, appropriate consideration should therefore be given to negative effects of contaminants on male fertility and male mating behaviour.


2021 ◽  
Author(s):  
Upama Aich ◽  
Megan Head ◽  
Rebecca Fox ◽  
Michael D Jennions

Older males often perform poorly under post-copulatory sexual selection. It is unclear, however, whether reproductive senescence is due to male age itself or the accumulated costs of the higher lifetime mating effort that is usually associated with male age. To date, very few studies have accounted for male mating history when testing for the effect of male age on sperm traits, and none test how age and past mating history influence paternity success under sperm competition. Here, we experimentally manipulate male mating history to tease apart its effects from that of age on ejaculate traits and paternity in the mosquitofish, Gambusia holbrooki. We found that old, naive males had more sperm than old, experienced males, while the reverse was true for young males. In contrast, neither male age nor mating history affected sperm velocity. Finally, using artificial insemination to experimentally control the number of sperm per male, we found that old males sired significantly more offspring than young males independent of their mating history. Our results highlight that the general pattern of male reproductive senescence described in many taxa may often be affected by two naturally confounding factors, male mating history and sperm age, rather than male age itself.


Behaviour ◽  
1990 ◽  
Vol 113 (1-2) ◽  
pp. 57-80 ◽  
Author(s):  
Christopher W. Petersen

AbstractThe hermaphroditic reef fish Serranus fasciatus exhibits three types of social systems. The size of a social group is correlated with the local density of conspecifics. At very low densities, isolated pairs of individuals reciprocally spawn with each other, achieving equal current reproductive success. At intermediate group sizes, harems form, with the largest individual typically losing all of its female function and becoming a functional male. In harems, subordinate hermaphrodites obtain little male reproductive success through streaking, an alternative male mating tactic. The lone pure male maintains almost total monopolization of male reproductive success in harems, apparently due to aggressive domination of subordinates. At high group sizes, the ability of the male to monopolize all of the matings in a social group decreases, and some of the larger hermaphrodites obtain some male-role reproductive success by pair spawning with smaller subordinate hermaphrodites while continuing to spawn as females with the male. Mating partners stay relatively constant through time, resulting in a pattern of small 'sub-harems' within harems. These mating tactics are consistent with the hypothesis that dominant individuals increase their current reproductive success in this species by restricting male mating opportunities of conspecifics. Subordinate individuals spawn as males when the dominant is unable to restrict interactions between hermaphrodites that are potential mates, or when they successfully streak. The increased male reproductive success of hermaphrodites in isolated pairs and complex harems compared with hermaphrodites in harems appears to be important in maintaining a hermaphroditic subordinate phenotype in this largely non-reciprocating species.


1995 ◽  
Vol 350 (1334) ◽  
pp. 391-399 ◽  

Atlantic salmon ( Salmo salar ) males mature as either tiny precocious parr before seaward migration, or as older and larger anadromous males. Anadromous males dominate the spawning redds and aggressively defend females against parr intrusions. Parr gain fertilizations by sneaking in to ejaculate while anadromous males and females spawn. Such differences in mating advantage generate asymmetries in risk of sperm competition between the male strategies. Theoretical sperm competition models predict that males typically mating in disfavoured roles (here, the parr strategy) should be selected to offset this disadvantage by investing more into spermatogenesis to achieve fertilization success. First, we present a theoretical model which analyses gametic expenditure for salmon parr and anadromous male reproductive strategies. We then use the natural variance in mating pattern within this species to compare empirically how males invest in spermatogenesis. A range of reproductive traits were measured for both male strategies. Absolutely, anadromous males have larger testes and produce greater numbers of sperm than parr males. However, results show that parr invest relatively more heavily into total spermatogenesis, and have a larger gonosomatic index than anadromous males. Relative to body size, parr produced greater numbers of sperm and volumes of stripped ejaculate. There was no difference in sperm length between the two male strategies. However, more sperm were motile in parr ejaculates, and these sperm lived longer than anadromous male sperm. Our findings may explain how male parr, under elevated risks of sperm competition and occupying a disfavoured mating role (parr weigh only 0.15% of the average body mass of anadromous males) achieve disproportionately high fertilization success.


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