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Mating plug

A mating plug, also known as a copulatory plug, is a gelatinous or solid mass formed by coagulated seminal proteins that males deposit in the female reproductive tract during or immediately after copulation, primarily to block further insemination by rival males and thereby increase the depositor's paternity share under promiscuous mating conditions.^[1] These structures are widespread across animal taxa, including insects like Drosophila melanogaster, nematodes such as Caenorhabditis remanei, rodents like the bank vole (Myodes glareolus), and even some cephalopods and arachnids, reflecting convergent evolution driven by sexual selection.^[2]^[3]^[1]

Formation and Composition

Mating plugs typically arise from the rapid coagulation of ejaculate components, often involving specialized proteins from male accessory glands or seminal vesicles; for instance, in rodents, transglutaminase enzymes cross-link proteins to form a durable barrier, while in Drosophila, proteins like PEBme from the ejaculatory bulb solidify within minutes to retain the ejaculate.^[1]^[2] In nematodes, the plug is a polymerizing gelatinous secretion from a dedicated male gland applied directly to the vulva post-insemination.^[3] Plug size and durability often correlate with male traits like seminal vesicle mass, influencing their effectiveness in sperm competition.^[1]

Functions and Evolutionary Significance

Beyond serving as a mechanical barrier to inhibit rival sperm, mating plugs can promote the transport and storage of the male's own sperm, and even confer female benefits such as increased offspring production (e.g., ~29% more hatchlings in plugged C. remanei females) or pathogen protection.^[1]^[3] In Drosophila, plugs prevent ejaculate loss and support fertility by enabling proper sperm storage, with experimental removal leading to reduced reproductive success.^[2] Evolutionarily, these adaptations highlight male strategies to mitigate sperm competition in polyandrous species, though plugs may also evolve mutualistic roles benefiting both sexes, as evidenced by their persistence across diverse phyla.^[3]^[1]

Overview

Definition

A mating plug is a gelatinous or solid mass of seminal fluid deposited by the male in, on, or around the female's genitalia or reproductive tract immediately after copulation, which hardens to form a physical barrier that blocks further sperm entry from subsequent matings.^[1] Historically, the term has been referred to as a copulatory plug in various vertebrates and invertebrates, emphasizing its role in post-copulatory interactions.^[4] In certain Lepidoptera species, it is specifically known as a sphragis, an often externalized and elaborate plug secreted by the male to seal the female's genitalia.^[5] Key characteristics of mating plugs include their function as a temporary or semi-permanent seal, with durability ranging from hours to days depending on the species, and variations in size from small internal coagulations to large external structures that can cover much of the female's abdomen.^[5]^[1] These plugs may briefly prevent female remating to favor the depositing male's paternity.^[1]

Biological Role

The mating plug serves a primary biological role in preventing sperm competition by physically obstructing the female's genital opening, thereby reducing the entry of rival sperm into the reproductive tract. In species such as the fruit fly Drosophila melanogaster, the plug forms a barrier that delays the ejection of the male's ejaculate, allowing more time for his sperm to be stored in the female's spermathecae and minimizing dilution or displacement by subsequent matings.^[6] Similarly, in mammals like house mice (Mus musculus), the copulatory plug blocks the vaginal opening, inhibiting insemination by rival males and enhancing the first male's fertilization success even in vasectomized scenarios where no sperm is transferred.^[7] A key function of the mating plug is mate guarding, which decreases the likelihood of female remating and thereby secures paternity for the depositing male. By altering female physiology and behavior, the plug reduces short-term sexual receptivity; for instance, in D. melanogaster, females mated to males unable to form plugs exhibit significantly higher remating rates compared to those with intact plugs, as observed in behavioral assays where plug-deficient matings led to increased female acceptance of subsequent courtship.^[6] In rodents such as bank voles (Myodes glareolus), retained plugs correlate with lower second-male sperm presence in the uterus, demonstrating effective post-copulatory guarding under promiscuous conditions.^[1] Secondary roles of the mating plug include facilitation of sperm storage in certain species and potential chemical signaling through retained secretions. In D. melanogaster, the plug acts as a scaffold that promotes efficient sperm retention and storage by preventing premature loss of the ejaculate, with mutants lacking key plug proteins showing reduced sperm counts in female storage organs over time.^[8] Additionally, by holding seminal fluid proteins in place, the plug may enable chemical signaling that triggers female post-mating responses, such as elevated oviposition or reduced receptivity, though direct evidence for signaling via plug-specific components remains limited.^[6]

Physical Properties

Composition

Mating plugs are primarily composed of seminal proteins and coagulating fluids derived from male reproductive accessory glands, which solidify to form a barrier in the female reproductive tract. In insects such as Drosophila melanogaster, the plug consists of multiple male accessory gland (MAG) proteins, including a 38 kDa autofluorescent protein known as PEB-me from the ejaculatory bulb and fibrinogen-like proteins that facilitate coagulation.^[9]^[10] In mosquitoes like Anopheles gambiae, transglutaminase 3 (AgTG3) similarly cross-links seminal proteins to form the plug structure.^[11] In reptiles, particularly garter snakes (Thamnophis sirtalis parietalis), mating plugs are gelatinous masses formed from renal or cloacal secretions deposited post-insemination, lacking the protein-heavy composition seen in insects but serving a comparable occlusive function.^[12] These plugs are thick and amorphous, potentially incorporating lipid elements from glandular fluids, though detailed biochemical profiles remain less studied compared to arthropods.^[13] In mammals, such as house mice (Mus domesticus), copulatory plugs arise from coagulation of seminal vesicle proteins, including transglutaminase 4 (TGM4) and seminal vesicle secretory protein 2 (SVS2), which enable rapid hardening within the vaginal-cervical region.^[14] Proteomic surveys have detected over 60 proteins associated with these plugs, predominantly from seminal fluid, highlighting their role in structural integrity.^[15] Microscopically, insect and mammalian plugs exhibit a dense, solidified matrix that initially permits sperm transit before fully barring subsequent access, as observed in dissected reproductive tracts.^[10] Analytical approaches, including tandem mass spectrometry on isolated plugs, have been instrumental in elucidating these enzymatic drivers like transglutaminases across taxa.^[10]^[11]

Formation Mechanism

The formation of a mating plug typically involves the deposition of seminal fluid during copulation, which coagulates rapidly within the female reproductive tract through enzymatic reactions to create a physical barrier.^[1] In many species, this process begins immediately upon ejaculation, with proteins from the male's accessory glands cross-linking to solidify the material, often within seconds to minutes after insemination.^[1] For instance, in rodents such as house mice, proteins secreted from the seminal vesicles and coagulating gland mix during ejaculation and harden via transglutaminase enzymes to form a cohesive plug in the vaginal canal.^[16] Similarly, in fruit flies (Drosophila melanogaster), male seminal fluid proteins like Acp36DE and Ebp are ejaculated into the female bursa, where they coagulate to encapsulate sperm, with the process completing shortly after copulation ends.^[17] Male contributions to plug formation are primarily through specialized glands that produce the coagulating components. In mammals, the seminal vesicles supply the bulk of the proteins (e.g., SVS4 in rodents), while prostate-derived enzymes facilitate cross-linking; larger glands correlate with more robust plugs.^[1] In arthropods, males transfer seminal fluid from accessory glands containing proteins that interact with the female tract to promote solidification, though female reproductive glands also contribute proteolytic enzymes that influence the plug's initial structure.^[17] Reptiles exhibit variation, as seen in garter snakes (Thamnophis sirtalis), where the renal sexual segment—a modified kidney portion—produces gelatinous material that is extruded via the hemipenis at the end of copulation, forming a plug in the cloaca without relying on traditional accessory glands.^[18] The timing of solidification is species-specific but generally rapid to ensure immediate functionality. In insects like Drosophila, the plug solidifies within minutes post-ejaculation, aiding sperm transfer before potential ejection.^[17] Rodent plugs harden almost instantly upon deposition, remaining intact for hours depending on environmental factors.^[16] In reptiles, such as garter snakes, the plug material is deposited over about 2 minutes at copulation's conclusion and fully hardens within 6 hours.^[18] Removal or dissolution of the plug occurs through natural enzymatic breakdown in the female tract or mechanical ejection, with durations ranging from hours to days. In Drosophila, female glands secrete enzymes (e.g., send1) that dissolve the plug, typically within 3 hours, facilitating sperm storage and subsequent ejection.^[17] Rodent plugs are enzymatically degraded over several hours, though they can be dislodged mechanically by subsequent males via intromission.^[1] In garter snakes, plugs persist for about 2 days before enzymatic dissolution and expulsion, with warmer conditions accelerating the process.^[18] These mechanisms ensure the plug's temporary nature, balancing male and female reproductive interests.

Taxonomic Distribution

In Arthropods

Mating plugs are highly prevalent among insects, occurring in various orders including Hymenoptera, Diptera, and Lepidoptera, where they serve to block subsequent inseminations and reduce sperm competition.^[9] Entomological studies indicate that such structures are documented in numerous species across these groups, reflecting their adaptive significance in diverse mating systems.^[19] They are also reported in arachnids, particularly spiders, where males may deposit plugs to prevent remating or protect sperm; for example, in the spider Neriene emphana, plugs function to inhibit sperm leakage and desiccation.^[20] In Hymenoptera, particularly in social bees like the honeybee Apis mellifera, the mating plug, known as the "mating sign," forms from the male's endophallus, which detaches and remains in the queen's genital tract after copulation, temporarily sealing it.^[21] This structure, composed of chitinous parts and mucus, facilitates multiple matings by subsequent drones while marking the queen.^[22] In Diptera, such as fruit flies (Drosophila melanogaster), the plug is a temporary gelatinous mass derived from seminal fluid proteins secreted by the male accessory glands, which coagulates in the female's bursa copulatrix to delay remating for several hours.^[17] This adaptation helps retain sperm but dissolves relatively quickly, allowing for potential polyandry.^[2] Within Lepidoptera, mating plugs vary markedly; in many butterfly species, males produce a permanent external structure called a sphragis, which scales and seals the female's abdomen, preventing further copulations for life.^[5] Surveys have recorded sphragides or related plugs in at least 273 species across families like Papilionidae and Nymphalidae, highlighting their widespread occurrence in this order.^[5] In contrast to the transient plugs in Diptera, these lifelong barriers underscore intense sexual conflict in lepidopteran mating dynamics.^[23]

In Other Taxa

Mating plugs occur in nematodes, such as Caenorhabditis remanei, where males produce a gelatinous secretion from a specialized gland that polymerizes on the female vulva post-insemination, benefiting female fecundity by increasing hatchling production.^[3] In cephalopods, structures resembling mating plugs are formed by everted spermatophores in species like the arrow squid (Doryteuthis plei), which block the female's seminal receptacle to prevent further insemination by rivals.^[24]

In Reptiles

Mating plugs, also known as copulatory plugs, are documented in various squamate reptiles, particularly snakes and to a lesser extent lizards, where they serve to seal the female's cloaca following copulation. In snakes, these structures are relatively common, especially in species exhibiting high levels of sperm competition such as garter snakes (Thamnophis spp.) and some vipers, where they physically block the oviductal openings to inhibit subsequent inseminations by rival males.^[12] In lizards, plugs are rarer but have been observed in species like the Iberian rock lizard (Lacerta monticola), though their prevalence across squamates remains lower than in snakes, with reports in a limited number of taxa.^[25]^[26] Formation of these plugs occurs during or immediately after copulation, when the male everts one of his paired hemipenes to deposit the material directly into the female's cloaca. Unlike in mammals or arthropods, squamate reptiles lack dedicated accessory sex glands; instead, the gelatinous plug material is produced by the renal sexual segment (RSS) of the male's kidney, which secretes a viscous, proteinaceous fluid rich in lipids that solidifies upon deposition.^[26] This process typically takes about 2 minutes at the end of copulation in species like the red-sided garter snake (Thamnophis sirtalis parietalis), where the plug forms as a cohesive blob that adheres firmly to the cloacal walls.^[18] The plugs generally persist for 1 to 7 days, with duration influenced by environmental factors such as temperature—shorter in warmer conditions due to faster degradation—and species-specific traits, often lasting around 2 days in garter snakes.^[18]^[12] While effective as a temporary barrier against remating, they can impose costs on females, including physical discomfort from the hardened mass and potentially elevated predation risk in species with communal mating aggregations. In red-sided garter snakes, for instance, plugs reduce the likelihood of multiple matings within communal dens, where intense male competition occurs, thereby enhancing the first male's paternity share.^[18] In the Iberian rock lizard, however, plugs do not reliably prevent insemination by rivals, as subsequent males can displace them, highlighting variability in their efficacy across reptilian taxa.^[25]

In Mammals

In mammals, mating plugs are most prominently observed in rodents, particularly species such as house mice (Mus domesticus) and rats (Rattus norvegicus), where they manifest as vaginal plugs formed primarily from secretions of the seminal vesicles.^[1] These secretions, rich in proteins like SVS4, coagulate in the female's reproductive tract due to cross-linking by transglutaminase enzymes (TGM4) derived from the prostate.^[1] The process begins immediately upon ejaculation, with the seminal fluid solidifying rapidly within the vagina to create a hardened barrier, typically within minutes post-copulation.^[14] This coagulation mechanism serves to seal the vaginal canal temporarily, often persisting for 24-48 hours, thereby influencing post-copulatory reproductive dynamics in these species.^[14] Laboratory studies on house mice demonstrate that the presence of these plugs significantly enhances the first male's paternity success by inhibiting rival sperm entry; for instance, in competitive mating scenarios, intact plugs result in the first male siring nearly 95% of offspring, compared to 0% when plugs fail to form.^[27] Mating plugs are rare outside of rodents among mammals and are not a universal feature. They occur occasionally in certain primates, such as ring-tailed lemurs (Lemur catta), where males deposit gelatinous plugs that can be displaced during subsequent matings, reflecting adaptations in polygynandrous systems.^[28]^[29] However, such structures are absent or inconsistent in most other mammalian orders, highlighting their specialized evolutionary occurrence primarily within rodent lineages.^[28]

Evolutionary Aspects

Adaptive Value

Mating plugs provide significant adaptive value to males by enhancing paternity assurance in species where females mate promiscuously, thereby reducing the costs associated with sperm competition from rival males. In such contexts, plugs physically obstruct the female genital tract, impeding subsequent inseminations and allowing the first male's sperm a competitive advantage. For instance, in house mice (Mus domesticus), the absence of a copulatory plug results in the first male losing nearly all paternity to subsequent mates, demonstrating the plug's role in securing substantial reproductive success.^[27] Similarly, evolutionary models indicate that plugs evolve as a male strategy to limit female remating, particularly under conditions of low mating attempts per female and male-biased sex ratios, where high plug efficacy maximizes fertilization shares.^[30] From the female perspective, mating plugs impose potential costs such as delayed remating opportunities and reduced receptivity, which may limit access to diverse sperm for genetic benefits or increase vulnerability to injury during plug removal attempts. However, plugs can also confer benefits by optimizing the timing of mate choice, allowing females to avoid excessive harassment or suboptimal pairings. In the nematode Caenorhabditis remanei, for example, females bearing plugs produce more offspring than those without, suggesting a net fitness gain through enhanced sperm storage or protection.^[31] These dual effects highlight plugs as a sexually antagonistic trait, where female resistance behaviors, such as attempts to dislodge plugs, evolve in response to male-imposed constraints on remating. For instance, in the spider Micaria sociabilis, females exhibit behaviors that influence plug formation and persistence.^[32] Trade-offs in plug use are evident across species, balancing male gains against female-imposed counteradaptations, with fitness models quantifying male paternity increases from plugs as ranging substantially depending on ecological factors like sperm limitation. In competitive scenarios, plugs can yield paternity shares that shift dramatically in favor of the plugging male, often by 50% or more relative to unplugged matings, though female behaviors like plug ejection mitigate these advantages.^[16] Overall, the evolution of mating plugs is driven by sexual selection, with studies across arthropods and mammals supporting their emergence as a response to postcopulatory competition.^[33]

Comparative Analysis

Mating plugs exhibit convergent evolution across distantly related taxa, serving a similar function in blocking female remating or sperm displacement despite differences in composition and formation. For instance, in insects such as Drosophila, plugs are formed from seminal proteins that coagulate in the female reproductive tract, while in reptiles like garter snakes (Thamnophis sirtalis), they consist of gelatinous secretions from the male cloaca that harden post-copulation. This independent evolution highlights a shared selective pressure under sperm competition, with plugs arising multiple times in nematodes, insects, arachnids, reptiles, and mammals.^[34] Variations in mating plug durability and persistence occur across taxa, ranging from temporary structures that dissolve relatively quickly to more permanent barriers. In mammals, plugs are often temporary and dissolvable, as seen in rodents where enzymatic degradation allows for potential remating after hours or days, whereas in primates like chimpanzees, they form robust, longer-lasting coagula correlated with higher promiscuity levels. In contrast, butterflies (Lepidoptera) produce enduring sphragides, externalized keratin-like plugs secreted by males, often incorporating scales from the male, that permanently seal the female genitalia without impeding oviposition, ensuring paternity in species with intense male-male competition.^[34] Phylogenetic patterns reveal that mating plugs are more prevalent in taxa characterized by high female promiscuity, where they function to mitigate sperm competition risks. Reviews across diverse animal groups, including arthropods, reptiles, and mammals, indicate that plug formation correlates with polyandrous mating systems, enhancing male reproductive success by reducing subsequent inseminations. For example, in primates, plug robustness increases with estimated promiscuity rates, while in insects, plugs are common in species with multiple matings per female.^[34] Significant gaps persist in understanding mating plugs in certain vertebrate lineages, particularly birds and amphibians, where such structures are rare or undocumented. In birds, despite widespread promiscuity in many species, copulatory plugs appear absent, with alternative mechanisms like cloacal pecking or sperm ejection dominating post-copulatory interactions.^[35] Similarly, in amphibians, plugs are sporadically reported but largely unstudied, potentially due to external fertilization in many taxa limiting the need for internal barriers.^[36]

References

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Revealing mechanisms of mating plug function under sexual selection
Oct 19, 2020 · Mating plugs are produced by many sexually reproducing animals and are hypothesized to promote male fertilization success under promiscuous mating.
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Don't pull the plug! the Drosophila mating plug preserves fertility
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Definition: A gelatinous secretion used in the mating of some species. It is deposited by a male into a female genital tract and later hardens into a plug or ...
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Aug 12, 2016 · For example, the copulatory plug may contribute to copulatory stimulation (#3), which may induce contractions that promote sperm transport (#2) ...Missing: definition | Show results with:definition
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A number of functions have been attributed to copulatory plugs, including the inhibition of female remating and the promotion of ejaculate movement. Here we ...
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Obp56g is involved in mating plug formation, ejaculate retention, and sperm storage. Increased egg laying and decreased remating are two phenotypes of the PMR ...
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Dec 22, 2009 · The Mating Plug Is Composed of Multiple MAG Proteins. To identify MAG proteins that are transferred to females during copulation, we examined ...
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Formation of the “mating plug” by cross-linking Plugin is necessary for efficient sperm storage by females. AgTG3 has a similar degree of sequence identity (∼30 ...
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The honey bee's mating is spectacular because a drone 'comet' pursues the queen, the drone dies after mating, and the drone's phallus detaches and may burst.
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