Social status and ejaculate composition in the house mouse Bayram, Helen L; Franco, Catarina; Brownridge, Philip ...
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2020, Letnik:
375, Številka:
1813
Journal Article
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Sperm competition theory predicts that males should tailor ejaculates according to their social status. Here, we test this in a model vertebrate, the house mouse (
), combining experimental data with ...a quantitative proteomics analysis of seminal fluid composition. Our analyses reveal that both sperm production and the composition of proteins found in seminal vesicle secretions differ according to social status. Dominant males invested more in ejaculate production overall. Their epididymides contained more sperm than those of subordinate or control males, despite similar testes size between the groups. Dominant males also had larger seminal vesicle glands than subordinate or control males, despite similar body size. However, the seminal vesicle secretions of subordinate males had a significantly higher protein concentration than those of dominant males. Moreover, detailed proteomic analysis revealed subtle but consistent differences in the composition of secreted seminal vesicle proteins according to social status, involving multiple proteins of potential functional significance in sperm competition. These findings have significant implications for understanding the dynamics and outcome of sperm competition, and highlight the importance of social status as a factor influencing both sperm and seminal fluid investment strategies. This article is part of the theme issue 'Fifty years of sperm competition'.
Male and female genital morphology may have strong effects on fitness in spiders. Females of some species of Leucauge produce mating plugs that partially or totally block the entrances to their ...insemination ducts on the epigynum, forming barriers that reduce the probabilities of future inseminations. While in some species both females and males participate in plug formation, the mating plugs in L. argyra are produced exclusively by females. The epigynum of L. argyra (Walckenaer 1841) is unusual in having a prominent ventral process covered on its anterior side and around its base with long, thick setae. We tested whether male stimulation of these epigynal setae affected female plug formation by removing them from some females but not others. Females lacking setae produced mating plugs immediately after copulation less often than unmanipulated females. However, 24 hr later the mating plugs had disappeared in many females of the treatment group. Setae removal did not affect the amount of sperm stored in the female spermatheca, or the frequency of female attacks. The rate of male genital inflations correlated positively, but mating duration was negatively correlated with sperm stored in female's spermathecae. Females attempted to attack small males more often than large males. These findings contribute to our understanding of the function of the setae associated with the female genitalia, and the effect of their tactile stimulation on plug formation, and transference of spermatozoids.
* Removal of female epigynal setae affects the frequency of female plug formation
* Male size influences female attack decisions during mating
A common male adaptation to prevent sperm competition is the placement of a mating plug. Such plugs are considered as an extreme investment if they comprise parts of the genital systems and render ...the male sterile. Genital mutilation occurs in monogynous spiders of several families and may co‐occur with permanent sperm depletion, meaning that sperm production is terminated once males become mature. Within the orb‐web spider genus Nephila, monogynous mating strategies are considered ancestral, although some species have reverted to a polygynous mating strategy. Although genital mutilation does not occur in these species, permanent sperm depletion (PSD) remained. We compared investment in sperm between an effectively plugging (Nephila fenestrata Thorell, 1859) and a closely‐related nonplugging species Nephila senegalensis (Walckenaer, 1841). Sperm investment should be higher in N. senegalensis because males are able to mate with several females, whereas N. fenestrata males can only achieve a maximum of two copulations, generally performed with the same female. The absence of a plugging mechanism in N. senegalensis and the inability to monopolize females by means of mating plugs results in a higher risk of sperm competition. Thus, we predicted higher investment in sperm producing tissue and larger sperm storage organs in males of N. senegalensis compared to N. fenestrata. We examined the testes and deferent ducts of both species for size and cell‐quality differences using light and transmission electron microscopy and analyzed the volume of the sperm reservoir in the male copulatory organ (i.e. spermophor) using X‐ray microcomputed tomography. In contrast to our prediction, the lumen of testes, deferent ducts, and spermophor of N. senegalensis males were significantly smaller than in N. fenestrata.
The best mating strategy for males differs from that of females, because females gain from mating with several males (polyandry), but males gain from monopolizing the females. As a consequence, males ...have evolved a variety of methods, such as the transfer of inhibitory substances from their accessory glands, to ensure exclusive paternity of the female's offspring, generally with detrimental effects on female fitness. Inhibitory substances have been identified as peptides or other specific molecules. Unfortunately, in social insects male-mating traits are investigated only poorly, although male social insects might have the same fundamental influence on female-mating behavior as found in other species. A recently developed technique for the artificial insemination of bumblebee queens allowed us to investigate which chemical compound in the mating plug of male bumblebees, Bombus terrestris L., prevents females (queens) from further mating. Surprisingly, we found that the active substance is linoleic acid, a ubiquitous and rather unspecific fatty acid. Contrary to mating plugs in other insect species, the bumblebee mating plug is highly efficient and allows the males to determine queen-mating frequencies.
Male genital mutilation is a common mechanism by which males reduce sperm competition by plugging female insemination ducts with different parts of its own genital system. This behavior is frequent ...in many spider families but is uncommon in Haplogynae. The reproductive biology of Dysderoidea is not well studied and the data is fragmentary; male genital mutilation has been reported only for one species of Oonopidae. This study provides evidence of male genital mutilation in Unicorn catleyi Platnick and Brescovit (Araneae: Oonopidae). Pieces of the embolus were found in the female posterior receptaculum. This behavior is a strategy used by the males in order to guarantee their paternity and not for escape from female attacks as has been reported for other species of Araneae, since cannibalism is unlikely in this species. The presence of embolus in the posterior receptaculum suggests this is the first place where sperm is received. The similarity of the female genitalia of U. catleyi to those of Orsolobidae, along with sclerotization of the seminal duct in the male copulatory bulb that is also present in Orchestina, Xiombarg, and Orsolobidae, provide strong evidence of the basal position of this genus in the family Oonopidae.
Male inhibition of female re-mating is common in many insects. Mating plugs, used by males to control female re-mating, have been postulated in several ant species. Recent studies of bumblebees have ...described re-mating inhibition by male accessory gland secretions. Fire ants Solenopsis invicta possess accessory glands containing the same four fatty acids as do the bumblebees. Furthermore it appears that some of these acids are transferred to the female at mating. Thus, it is possible that single mating of fire ant females may be enforced by male mating plugs.
Polyandry in hymenopteran social insects is surprisingly rare, despite its likely colony-level fitness benefits. Ordinarily, a male's fitness will be at odds with that of a colony when the genetic ...representation within it is diluted by multiple mating by the queen. Consequently, males are expected to be under selection to limit female re-mating, for example via secretions of their accessory glands. I hypothesized that if accessory glands in some way regulate female mating frequency, an evolutionary transition from single to multiple mating would likely be accompanied with a change in the morphology of the accessory glands. The accessory gland morphology was examined in the fungus-gardening ants, which have made a single transition from single to multiple mating. The evolution of polyandry within this clade corresponds to the loss of male accessory glands, lending tentative support to the idea that they may be involved in regulating mating frequency. MAG Male accessory gland Male accessory gland
Postcopulatory sexual selection—sperm competition and cryptic female choice—has become a major area of research over the past 40 years. Within this field there are many outstanding questions at every ...level of analysis, from proximate to ultimate. The fitness consequences for both sexes in the period after copulation and before fertilization are considerable, but are obscured within the female reproductive tract. Our understanding of postcopulatory mechanisms is especially sparse in taxa other than birds and insects. Nearly nothing is known in reptiles except that multiple paternity is common and widespread, and often results from long-term sperm storage across breeding seasons. We present some of the very first data on the determinants of fertilization success in the context of sperm competition in reptiles, a group that accounts for 30% of terrestrial vertebrates.
In the first chapter, "Asymmetric gametic isolation between two populations of red-sided garter snakes", we discuss the use of between-population crosses to reveal gametic isolation. The effect of population density and operational sex ratios on mating systems and the speciation process has fueled theoretical debate. We attempted to address these issues using two populations of red-sided garter snakes (Thamnophis sirtalis parietalis) from Manitoba, Canada. Our study populations differ markedly in their density mating aggregations, with a 10-fold difference between them. Using microsatellite markers for paternity analysis of litters produced from within and between population crosses. We found that the population with highest aggregation density, and presumably with the highest level of sexual conflict (i.e., when the evolutionary interests of the sexes differ) over mating, was also the population that exhibited homotypic sperm precedence. The less dense population showed a distinct postcopulatory male-size advantage. We also demonstrated that sperm stored within the female over hibernation can father 20-30% of offspring in a litter.
In the second chapter, "Sperm competition and mate-order effects in red-sided garter snakes", we test whether females use mate-order effects to ensure that a larger (fitter) male will sire her offspring. Does that second male should have precedence in sperm competition? We tested for second-male precedence using singly-mated females that mated with a second male. Average proportion of paternity was shared equally among the first (P₁, i.e., proportion of offspring from a litter fathered by the first male to mate) and second males (P₂) to mate, and stored sperm (Psubscript ss). This may be a case where last male precedence breaks down with more than two males. All females were spring virgins (they had not mated that spring, but may have stored sperm from fall matings); thus sperm stored presumably from fall matings is important in this system. As the interval between matings increased P₁ increased at the expense of Psubscript ss. As the second male to mate's copulation duration increased, P₁ also increased at the expense of P₂. This last result may indicate female influence over sperm transfer during coerced matings.
Copulatory plugs (CPs) are found in many taxa, but the functional significance is debated. Male garter snakes produce a gelatinous copulatory plug during mating that occludes the opening of the female reproductive tract for approximately two days. In chapter three, "Not just a chastity belt: the role of mating plugs in red-sided garter snakes revisited", we experimentally tested the role of the CPs. In snakes, sperm are produced in the testes and delivered through the ductus deferens, and the copulatory plug is thought to be produced by the sexual segment of the kidney and conveyed through the ureter. We manipulated the delivery of the two fluids separately by ligating the ducts. We confirmed that the CP is not formed in ureter-ligated males and that sperm leaks out immediately after copulation. The CP is analogous to a spermatophore. The protein matrix contains most of the sperm which are liberated as the plug dissolves within the female's vaginal pouch.
One of the fundamental principles in sperm competition is that increased sperm numbers increase the odds of winning in competitions for fertilization success and males will adjust their ejaculate relative to competition and the quality of his mate. In chapter four, "Sperm depleted males and the unfortunate females who mate with them", we detect significant among-male variation in the number of sperm ejaculated, and that male mate-order reduces sperm numbers. Male sperm numbers drop significantly from one mating to the next, and this has implications for sperm competiveness, as Thamnophis sirtalis exhibits a disassociated reproductive tactic, in that sperm stores are produced outside the breeding season, and thus cannot be replenished after mating. Interestingly, however, the on average the mobility of the sperm increased for a male's second mating. Therefore, increased sperm quality may compensate for reduced numbers in a competitive context. Further, females increase their remating rate when mating with males that are unable to deliver sperm.
In chapter five, "Sexual conflict during mating in red-sided garter snakes as evidenced by genital manipulation", we revisited the CP in the context of sexual conflict. Sex-differences in optimal copulation duration can be a source of conflict, as increased copulation duration may be advantageous for males as it delays female remating. Males of many species actively guard females to prevent them from remating, and in some cases males produce copulatory plugs to prevent remating. If precopulatory choice is limited at the time of her first mating, conflict may be especially onerous to a female. The size of the plug is influenced by the copulation duration. We experimentally tested the contribution of male and female control over copulation duration. We ablated the largest basal spine on the male's hemipene and found a reduction in copulation duration and an increase in the variation of plug mass. Further, we anesthetized the female's cloaca and found copulation duration increased, which suggests that males benefit from increased copulation duration while females actively try to reduce copulation duration. Therefore, sexual conflict is manifest in divergent copulation duration optima for males and females.
Graduation date: 2013
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