Female sperm storage

Last updated
Sperm storage organs in the fruit fly Drosophila melanogaster. Female was first mated with GFP-male and then re-mated with RFP-male. D.melanogaster Female Sperm Storage.jpg
Sperm storage organs in the fruit fly Drosophila melanogaster . Female was first mated with GFP-male and then re-mated with RFP-male.

Female sperm storage is a biological process and often a type of sexual selection in which sperm cells transferred to a female during mating are temporarily retained within a specific part of the reproductive tract before the oocyte, or egg, is fertilized. This process takes place in some species of animals, but not in humans[ citation needed ]. The site of storage is variable among different animal taxa and ranges from structures that appear to function solely for sperm retention, such as insect spermatheca [1] and bird sperm storage tubules (bird anatomy), [2] [3] to more general regions of the reproductive tract enriched with receptors to which sperm associate before fertilization, such as the caudal portion of the cow oviduct containing sperm-associating annexins. [4] Female sperm storage is an integral stage in the reproductive process for many animals with internal fertilization. It has several documented biological functions including:

Contents

Increased diversity of offspring

One important advantage female insects that store sperm gain is increased genetic diversity in their offspring. There are many ways that females can alter offspring genetics to increase their success and diversity. An example of how this can be accomplished is in female Scathophaga that preferentially fertilize eggs to survive in different environments. Since many environments require different traits for success, females are somehow able to match sperm (acquired from multiple mates) that have the best genes for whichever environment in which they will develop. [20] Many of the different properties of the environment, including temperature and thermal properties affect the female's sperm choice. [21] Studies have also shown that ovipositing is nonrandom and females lay eggs with varying PGM(phosphoglucomutase) genotypes in different environments in order to optimize offspring success. Females are acutely aware to their environment and manipulate the genetic diversity of their offspring in appropriate ways to ensure their success.

Another way sperm-storing females can alter the diversity of their offspring is controlling the relatedness to the males that provide them with sperm. Inbreeding depression can have a deleterious impact on populations of organisms and is due to mating of closely related individuals. To combat this effect, female insects appear to be able to sort out the sperm of relatives from the sperm of non-relatives to choose the best option to fertilize their eggs. Female crickets are able to preferentially store sperm of multiple unrelated males to that of their siblings; this results in more of the offspring having unrelated parentage. Being able to choose between sperm after coupling might be advantageous to females because choosing between mates precopulation may be more costly, or it may just be too difficult to tell males apart before mating. [22] Females possess remarkable abilities to select sperm to store and to fertilize their eggs that will make their offspring diverse. Though it has been shown that a majority of female insect species can store sperm, specific examples that have been studied could include field crickets, [22] dung flies [21] and Mediterranean fruit flies. [23] Females largely benefit from this mechanism, but males often can experience low fitness because their paternity is not secure.

Sperm stored often determines which male ends up fertilizing the most eggs. An example of this is seen in Red Flour Beetles, where most of the sperm is stored in the first mating. Another male can remove previously stored sperm to better chances of successful mating.

Antagonistic coevolution

Spiny genitalia, such as of this bean weevil, may help to remove sperm from the sperm storage structures Callosobruchus analis penis.jpg
Spiny genitalia, such as of this bean weevil, may help to remove sperm from the sperm storage structures

Antagonistic coevolution is the relationship between males and females where sexual morphology changes over time to change with the opposite's sex traits in order to achieve the maximum reproductive success. [24] One such development is alternative sperm storage sites, such as seminal receptacles, spermathecae, and pseudospermathecae, that are complex and extremely variable to allow for more choice in sperm selection. [25] In some cases, sperm storage sites can produce proteases that break down various proteins in male seminal fluid resulting in female selection in sperm. [26]

Like females, males have developed responses to counter evolutionary adaptations of the opposite sex. Responses in insects can vary in both genitalia and sperm structures, along with variations in behavior. Spiny male genitalia help to anchor the male to the female during copulation and remove sperm of previous males from female storage structures. [27] Males have also developed alternative ways to copulate. In the case of the bed bug, males traumatically inseminate females, which allows faster passage of sperm to female sperm storage sites. [28] The sperm are received by the mesospermalege and eventually reach the spermathecae, also referred to as seminal conceptacles.

At the microscopic level, Drosophila males have differing sperm tail lengths that correspond to various sizes of female seminal receptacles. [29] Longer male sperm tail length has shown a greater reproductive success with a larger female seminal receptacle while sperm with short tail lengths have been found to be more successful in smaller seminal receptacles.

Cryptic female choice

The ability to store and separate sperm from multiple males enables females to manipulate paternity by choosing which sperm fertilize their eggs, a process known as cryptic female choice. Evidence for this ability exists in many different taxa, including birds, reptiles, gastropods, arachnids, and insects. [30] [31] [32] [33] [20] In combining long-term sperm storage with polyandrous behavior, female members of the tortoise family Testudinidae have access to sperm from a range of genetically different males and can potentially influence a clutch’s paternity during each fertilization event, not just through her mating choices alone. As a result of clutches with greater variation in paternal genes and increased sperm competition, females can maximize both the genetic quality and number of offspring. [34]

Cryptic choice allows females to preferentially choose sperm. Females are thus able to mate multiple times and allocate sperm to their eggs according to paternal phenotype, or according to other characteristics. In some cases, such as in the yellow dung fly, certain male traits will affect the fitness of eggs laid in particular environmental conditions. Females can choose sperm based on male quality as a function of its interaction with the environment. [21] In other species, such as the fly Dryomyza anilis , females preferentially choose sperm from one storage location over another. Males of this species have developed behaviors, such as abdominal tapping, to increase their number of sperm stored in the favored storage site. [35] Evidence for this pattern of storage, cryptic choice, and male behavior also exists in the flour beetle Tribolium castaneum. [36] Some species, such as Egernia striolata , not only utilize sperm storage selection to improve fitness of their offspring, but to give them the upper hand in the event of sexual conflict. [37]

Mechanisms

Female muscular contractions

Muscle contraction as a means of moving spermatozoa through the reproductive system into and out of the storage structures has been examined in Diptera, Orthoptera, and Lepidoptera as well as in the species Rhodnius prolixus and the boll weevil. In R. prolixus, rhythmic peristaltic contractions of the oviduct cause contractions of the bursa copulatrix and spermatheca movement. This movement of the spermatheca results in spermatozoa migration into the spermathecal duct and into the spermatheca reservoir. [38] [39] [40] In the boll weevil, contractions are also used to move sperm from the spermathecae so they can fertilize the egg. [41] It has been observed in locusts, that the nervous system initiates female reproductive muscular contractions. [42] In some species, such as R. prolixus, the contractions that move spermatozoa into sperm storage are initiated by a male secretion in the ejaculate. [38] Male secretions, such as the glycoprotein ACP36D in Drosophila , can also play a role in preparing the female reproductive system for sperm storage. It causes changes in uterine shape allowing spermatozoa access to the sperm storage organs. [43]

Female insect nervous system

The female insect nervous system affects many of the processes involved in sperm storage. The nervous system may signal for muscular contractions, fluid absorption, and hormone release, all of which aid in moving the sperm into the storage organs. [44] When the nervous system of female fruit flies (Drosophila melanogaster) was replaced with a masculinized nervous system through genetic manipulation, sperm storage was affected suggesting that the female nervous system is unique and required to store sperm properly. [45]

The nervous system is responsible for several fertilization methods. In the migratory locust (Locusta migratoria), the presence of an egg in the genital chamber results in an increase of spermathecal contractions. As a result, sperm is released to fertilize the egg. A neural loop (from the VIIIth ganglion through the N2B nerve to N2B2, N2B3, N2B4, and N2B6b nerves) is then activated to direct the sperm to fertilize the egg via muscular contractions. [44] In the Caribbean fruit fly (Anastrepha suspensa), both the spermathecae and their ducts are innervated by an abdominal ganglion located under the first abdominal sternite. [46] This location suggests that the sperm receptacle can compress and influence the amount of sperm taken in or released by the female fly. [46]

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of flies, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<span class="mw-page-title-main">Sperm competition</span> Reproductive process

Sperm competition is the competitive process between spermatozoa of two or more different males to fertilize the same egg during sexual reproduction. Competition can occur when females have multiple potential mating partners. Greater choice and variety of mates increases a female's chance to produce more viable offspring. However, multiple mates for a female means each individual male has decreased chances of producing offspring. Sperm competition is an evolutionary pressure on males, and has led to the development of adaptations to increase male's chance of reproductive success. Sperm competition results in a sexual conflict between males and females. Males have evolved several defensive tactics including: mate-guarding, mating plugs, and releasing toxic seminal substances to reduce female re-mating tendencies to cope with sperm competition. Offensive tactics of sperm competition involve direct interference by one male on the reproductive success of another male, for instance by mate guarding or by physically removing another male's sperm prior to mating with a female. For an example, see Gryllus bimaculatus.

<span class="mw-page-title-main">Internal fertilization</span> Union of an egg and sperm to form a zygote within the female body

Internal fertilization is the union of an egg and sperm cell during sexual reproduction inside the female body. Internal fertilization, unlike its counterpart, external fertilization, brings more control to the female with reproduction. For internal fertilization to happen there needs to be a method for the male to introduce the sperm into the female's reproductive tract.

<span class="mw-page-title-main">Spermatheca</span> Insect female reproductive organ

The spermatheca, also called receptaculum seminis, is an organ of the female reproductive tract in insects, e.g. ants, bees, some molluscs, oligochaeta worms and certain other invertebrates and vertebrates. Its purpose is to receive and store sperm from the male or, in the case of hermaphrodites, the male component of the body. Spermathecae can sometimes be the site of fertilisation when the oocytes are sufficiently developed.

<span class="mw-page-title-main">Hemipenis</span> Male sex organ in squamate reptiles

A hemipenis is one of a pair of intromittent organs of male squamates. Hemipenes are usually held inverted within the body, and are everted for reproduction via erectile tissue, much like that in the human penis. They come in a variety of shapes, depending on species, with ornamentation such as spikes.

<span class="mw-page-title-main">Haplodiploidy</span> Biological system where sex is determined by the number of sets of chromosomes

Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. Haplodiploidy is sometimes called arrhenotoky.

<span class="mw-page-title-main">Sexual conflict</span> Term in evolutionary biology

Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females, due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.

<i>Scathophaga stercoraria</i> Species of fly

Scathophaga stercoraria, commonly known as the yellow dung fly or the golden dung fly, is one of the most familiar and abundant flies in many parts of the Northern Hemisphere. As its common name suggests, it is often found on the feces of large mammals, such as horses, cattle, sheep, deer, and wild boar, where it goes to breed. The distribution of S. stercoraria is likely influenced by human agriculture, especially in northern Europe and North America. The Scathophaga are integral in the animal kingdom due to their role in the natural decomposition of dung in fields. They are also very important in the scientific world due to their short life cycles and susceptibility to experimental manipulations; thus, they have contributed significant knowledge about animal behavior.

<span class="mw-page-title-main">Red flour beetle</span> Species of beetle

The red flour beetle is a species of beetle in the family Tenebrionidae, the darkling beetles. It is a worldwide pest of stored products, particularly food grains, and a model organism for ethological and food safety research.

<span class="mw-page-title-main">Mating plug</span> Gelatinous secretion used in the mating of some species

A mating plug, also known as a copulation plug, sperm plug, vaginal plug, or sphragis, is a gelatinous secretion used in the mating of some species. It is deposited by a male into a female genital tract, such as the vagina, and later hardens into a plug or glues the tract together. While females can expel the plugs afterwards, the male's sperm still gets a time advantage in getting to the egg, which is often the deciding factor in fertilization.

<span class="mw-page-title-main">Reproductive system of gastropods</span>

The reproductive system of gastropods varies greatly from one group to another within this very large and diverse taxonomic class of animals. Their reproductive strategies also vary greatly.

Bateman's principle, in evolutionary biology, is that in most species, variability in reproductive success is greater in males than in females. It was first proposed by Angus John Bateman (1919–1996), an English geneticist. Bateman suggested that, since males are capable of producing millions of sperm cells with little effort, while females invest much higher levels of energy in order to nurture a relatively small number of eggs, the female plays a significantly larger role in their offspring's reproductive success. Bateman's paradigm thus views females as the limiting factor of parental investment, over which males will compete in order to copulate successfully.

Sexual antagonistic co-evolution is the relationship between males and females where sexual morphology changes over time to counteract the opposite's sex traits to achieve the maximum reproductive success. This has been compared to an arms race between sexes. In many cases, male mating behavior is detrimental to the female's fitness. For example, when insects reproduce by means of traumatic insemination, it is very disadvantageous to the female's health. During mating, males will try to inseminate as many females as possible, however, the more times a female's abdomen is punctured, the less likely she is to survive. Females that possess traits to avoid multiple matings will be more likely to survive, resulting in a change in morphology. In males, genitalia is relatively simple and more likely to vary among generations compared to female genitalia. This results in a new trait that females have to avoid in order to survive.

Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.

A nuptial gift is a nutritional gift given by one partner in some animals' sexual reproduction practices.

<span class="mw-page-title-main">Sexual selection in mammals</span> Mode of natural selection

Sexual selection in mammals is a process the study of which started with Charles Darwin's observations concerning sexual selection, including sexual selection in humans, and in other mammals, consisting of male–male competition and mate choice that mold the development of future phenotypes in a population for a given species.

<span class="mw-page-title-main">Sexual selection in amphibians</span> Choice of and competition for mates

Sexual selection in amphibians involves sexual selection processes in amphibians, including frogs, salamanders and newts. Prolonged breeders, the majority of frog species, have breeding seasons at regular intervals where male-male competition occurs with males arriving at the waters edge first in large number and producing a wide range of vocalizations, with variations in depth of calls the speed of calls and other complex behaviours to attract mates. The fittest males will have the deepest croaks and the best territories, with females making their mate choices at least partly based on the males depth of croaking. This has led to sexual dimorphism, with females being larger than males in 90% of species, males in 10% and males fighting for groups of females.

Cryptic female choice is a form of mate choice which occurs both in pre and post copulatory circumstances when females in certain species use physical or chemical mechanisms to control a male's success of fertilizing their ova or ovum; i.e. by selecting whether sperm are successful in fertilizing their eggs or not. It occurs in internally-fertilizing species and involves differential use of sperm by females when sperm are available in the reproductive tract.

<span class="mw-page-title-main">Polyandry in animals</span> Class of mating system in non-human species

In behavioral ecology, polyandry is a class of mating system where one female mates with several males in a breeding season. Polyandry is often compared to the polygyny system based on the cost and benefits incurred by members of each sex. Polygyny is where one male mates with several females in a breeding season . A common example of polyandrous mating can be found in the field cricket of the invertebrate order Orthoptera. Polyandrous behavior is also prominent in many other insect species, including the red flour beetle and the species of spider Stegodyphus lineatus. Polyandry also occurs in some primates such as marmosets, mammal groups, the marsupial genus' Antechinus and bandicoots, around 1% of all bird species, such as jacanas and dunnocks, insects such as honeybees, and fish such as pipefish.

Genetic incompatibility describes the process by which mating yields offspring that are nonviable, prone to disease, or genetically defective in some way. In nature, animals can ill afford to devote costly resources for little or no reward, ergo, mating strategies have evolved to allow females to choose or otherwise determine mates which are more likely to result in viable offspring.

References

  1. ↑ Klowden MJ. 2003. Spermatheca. In Resh VH and Cardé RT (eds.): Encyclopedia of Insects. San Diego, CA: Academic Press. 1266.
  2. ↑ Liem KL, Bemis WE, Walker WF & Grande L. 2001. Functional Anatomy of the Vertebrates, an Evolutionary Perspective Archived 2021-12-26 at the Wayback Machine 3rd ed. Belmont, CA: Brooks/Cole – Thomson Learning. Pp703.
  3. ↑ Birkhead TR. 1998. Sperm Competition in Birds: mechanisms and function. In Birkhead TR & Møller AP (eds.) 1998. Sperm Competition and Sexual Selection. San Diego, CA: Academic Press. Pp. 826.
  4. ↑ Ignotz, George G; Cho, Margaret Y; Suarez, Susan S (2007). "Annexins Are Candidate Oviductal Receptors for Bovine Sperm Surface Proteins and Thus May Serve to Hold Bovine Sperm in the Oviductal Reservoir1". Biology of Reproduction. 77 (6): 906–13. doi: 10.1095/biolreprod.107.062505 . PMID   17715429.
  5. 1 2 3 Suarez, SS (2002). "Formation of a Reservoir of Sperm in the Oviduct". Reproduction in Domestic Animals. 37 (3): 140–3. doi:10.1046/j.1439-0531.2002.00346.x. PMID   12071887.
  6. ↑ Suarez, S. S (2008). "Control of hyperactivation in sperm". Human Reproduction Update. 14 (6): 647–57. doi: 10.1093/humupd/dmn029 . PMID   18653675.
  7. ↑ Allen, A. K; Spradling, A. C (2007). "The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function". Development. 135 (2): 311–21. doi: 10.1242/dev.015156 . PMID   18077584.
  8. ↑ Hunter, R. H. F; Leglise, P. C (1971). "Polyspermic Fertilization Following Tubal Surgery in Pigs, with Particular Reference to the Role of the Isthmus". Reproduction. 24 (2): 233–46. CiteSeerX   10.1.1.1028.5312 . doi:10.1530/jrf.0.0240233. PMID   5102536.
  9. ↑ Kardong KV. 2009. Vertebrates: Comparative Anatomy, Function, Evolution. 5th ed. Boston, MA: McGraw Hill. Pp 779.
  10. ↑ Birkhead, T. R; Møller, A. P (1993). "Sexual selection and the temporal separation of reproductive events: Sperm storage data from reptiles, birds and mammals". Biological Journal of the Linnean Society. 50 (4): 295–311. doi:10.1111/j.1095-8312.1993.tb00933.x.
  11. ↑ Holt, William V (2011). "Mechanisms of Sperm Storage in the Female Reproductive Tract: An Interspecies Comparison". Reproduction in Domestic Animals. 46: 68–74. doi: 10.1111/j.1439-0531.2011.01862.x . PMID   21884282.
  12. ↑ Ridley, M (1988). "Mating Frequency and Fecundity in Insects". Biological Reviews. 63 (4): 509–49. doi:10.1111/j.1469-185X.1988.tb00669.x. S2CID   85110084.
  13. ↑ Den Boer, S. P. A; Baer, B; Dreier, S; Aron, S; Nash, D. R; Boomsma, J. J (2009). "Prudent sperm use by leaf-cutter ant queens". Proceedings of the Royal Society B: Biological Sciences. 276 (1675): 3945–53. doi:10.1098/rspb.2009.1184. JSTOR   30245087. PMC   2825782 . PMID   19710057.
  14. ↑ Antolin MF & Henk AD. 2003. Sex Determination. In Resh VH and Cardé RT (eds.): Encyclopedia of Insects. San Diego, CA: Academic Press. 1266.
  15. ↑ Werren, J. H (1980). "Sex Ratio Adaptations to Local Mate Competition in a Parasitic Wasp". Science. 208 (4448): 1157–9. Bibcode:1980Sci...208.1157W. doi:10.1126/science.208.4448.1157. PMID   17783073. S2CID   28151928.
  16. ↑ King, P. E (1961). "A Possible Method of Sex Ratio Determination in the Parasitic Hymenopteran Nasonia vitripennis". Nature. 189 (4761): 330–1. Bibcode:1961Natur.189..330K. doi:10.1038/189330a0. S2CID   4181967.
  17. ↑ Birkhead TR & Møller AP (eds.) 1998. Sperm Competition and Sexual Selection. San Diego, CA: Academic Press. Pp. 826.
  18. ↑ Eberhard WG. 1996. Female Control: Sexual Selection and Cryptic Female Choice. Princeton, NJ: Princeton University Press. Pp 501.
  19. ↑ Leonard J. & Cordoba-Aguilar A. 2010. The Evolution of Primary Sexual Characters in Animals (pp. 1–52). Oxford: Oxford University Press.
  20. 1 2 Ward, Paul I (2000). "Cryptic Female Choice in the Yellow Dung Fly Scathophaga Stercoraria (L.)". Evolution. 54 (5): 1680–6. doi:10.1111/j.0014-3820.2000.tb00712.x. PMID   11108595. S2CID   86351582.
  21. 1 2 3 Ward, Paul I; Vonwil, Judith; Scholte, Ernst-Jan; Knop, Eva (2002). "Field experiments on the distributions of eggs of different phosphoglucomutase (PGM) genotypes in the yellow dung fly Scathophaga stercoraria (L.)". Molecular Ecology. 11 (9): 1781–5. Bibcode:2002MolEc..11.1781W. doi:10.1046/j.1365-294X.2002.01558.x. PMID   12207727. S2CID   1292185.
  22. 1 2 Bretman, Amanda; Newcombe, Devi; Tregenza, TOM (2009). "Promiscuous females avoid inbreeding by controlling sperm storage". Molecular Ecology. 18 (16): 3340–5. Bibcode:2009MolEc..18.3340B. doi:10.1111/j.1365-294X.2009.04301.x. PMID   19694961. S2CID   21936522.
  23. ↑ Taylor, Phillip W; Yuval, Boaz (1999). "Postcopulatory sexual selection in Mediterranean fruit flies: Advantages for large and protein-fed males". Animal Behaviour. 58 (2): 247–254. doi:10.1006/anbe.1999.1137. PMID   10458875. S2CID   13919705.
  24. ↑ Rowe, Locke; Arnqvist, Göran (2002). "Sexually Antagonistic Coevolution in a Mating System: Combining Experimental and Comparative Approaches to Address Evolutionary Processes". Evolution. 56 (4): 754–67. doi: 10.1111/j.0014-3820.2002.tb01386.x . PMID   12038533. S2CID   221736131.
  25. ↑ Marchini, Daniela; Bene, Giovanna Del; Dallai, Romano (2009). "Functional morphology of the female reproductive apparatus of Stephanitis pyrioides (Heteroptera, Tingidae): A novel role for the pseudospermathecae". Journal of Morphology. 271 (4): 473–82. doi:10.1002/jmor.10811. PMID   19941380. S2CID   7316706.
  26. ↑ Prokupek, Adrianne; Hoffmann, Federico; Eyun, Seong-il; Moriyama, Etsuko; Zhou, Min; Harshman, Lawrence (2008). "An Evolutionary Expressed Sequence Tag Analysis of Drosophila Spermatheca Genes". Evolution. 62 (11): 2936–47. doi: 10.1111/j.1558-5646.2008.00493.x . PMID   18752616. S2CID   33477158.
  27. ↑ Ronn, J; Katvala, M; Arnqvist, G (2007). "Coevolution between harmful male genitalia and female resistance in seed beetles". Proceedings of the National Academy of Sciences. 104 (26): 10921–5. Bibcode:2007PNAS..10410921R. doi: 10.1073/pnas.0701170104 . PMC   1904142 . PMID   17573531.
  28. ↑ Siva-Jothy, M. T; Stutt, A. D (2003). "A matter of taste: Direct detection of female mating status in the bedbug". Proceedings of the Royal Society B: Biological Sciences. 270 (1515): 649–52. doi:10.1098/rspb.2002.2260. PMC   1691276 . PMID   12769466.
  29. ↑ Miller, G. T; Pitnick, S (2002). "Sperm-Female Coevolution in Drosophila". Science. 298 (5596): 1230–3. Bibcode:2002Sci...298.1230M. doi:10.1126/science.1076968. PMID   12424377. S2CID   46698905.
  30. ↑ Wagner, R. H; Helfenstein, F; Danchin, E (2004). "Female choice of young sperm in a genetically monogamous bird". Proceedings of the Royal Society B: Biological Sciences. 271 (Suppl 4): S134–7. doi:10.1098/rsbl.2003.0142. PMC   1810032 . PMID   15252964.
  31. ↑ Moore, Jennifer A; Daugherty, Charles H; Godfrey, Stephanie S; Nelson, Nicola J (2009). "Seasonal monogamy and multiple paternity in a wild population of a territorial reptile (tuatara)". Biological Journal of the Linnean Society. 98 (1): 161–70. doi: 10.1111/j.1095-8312.2009.01271.x .
  32. ↑ Beese, K; Armbruster, G. F. J; Beier, K; Baur, B (2009). "Evolution of female sperm-storage organs in the carrefour of stylommatophoran gastropods". Journal of Zoological Systematics and Evolutionary Research. 47 (5): 208–11. doi: 10.1111/j.1439-0469.2008.00491.x .
  33. ↑ Welke, Klaas; Schneider, Jutta M (2009). "Inbreeding avoidance through cryptic female choice in the cannibalistic orb-web spider Argiope lobata". Behavioral Ecology. 20 (5): 1056–62. doi: 10.1093/beheco/arp097 .
  34. ↑ Holt, W.V; Lloyd, R.E (2010). "Sperm storage in the vertebrate female reproductive tract: How does it work so well?". Theriogenology. 73 (6): 713–22. doi:10.1016/j.theriogenology.2009.07.002. PMID   19632711.
  35. ↑ Bussière, L. F; Demont, M; Pemberton, A. J; Hall, M. D; Ward, P. I (2010). "The assessment of insemination success in yellow dung flies using competitive PCR". Molecular Ecology Resources. 10 (2): 292–303. doi: 10.1111/j.1755-0998.2009.02754.x . PMID   21565024. S2CID   10879957.
  36. ↑ Bloch Qazi, M. C (2003). "A potential mechanism for cryptic female choice in a flour beetle". Journal of Evolutionary Biology. 16 (1): 170–6. doi: 10.1046/j.1420-9101.2003.00501.x . PMID   14635892. S2CID   5636469.
  37. ↑ Riley, Julia L; Stow, Adam; Bolton, Peri E; Dennison, Siobhan; Byrne, Richard; Whiting, Martin J (2021-08-19). "Sperm Storage in a Family-Living Lizard, the Tree Skink (Egernia striolata)". Journal of Heredity (esab048). doi:10.1093/jhered/esab048. ISSN 0022-1503.
  38. 1 2 Davey, KG (1958). "The migration of spermatozoa in the female of Rhodnius prolixus". Journal of Experimental Biology. 35: 694–701. doi:10.1242/jeb.35.3.694.
  39. ↑ Nonidez, José F (1920). "The Internal Phenomena of Reproduction in Drosophila". The Biological Bulletin. 39 (4): 207–30. doi: 10.2307/1536488 . JSTOR   1536488.
  40. ↑ Omura, S (1935). "Structure and function of the female genital system of Bombyx mori with special reference to the mechanism of fertilization" (PDF). Journal of the Faculty of Agriculture. 40 (3): 111–31.
  41. ↑ Villavaso, Eric J (1975). "Functions of the spermathecal muscle of the boll weevil, Anthonomus grandis". Journal of Insect Physiology. 21 (6): 1275–8. doi:10.1016/0022-1910(75)90099-2.
  42. ↑ Clark, Julie; Lange, Angela B (2001). "Evidence of a neural loop involved in controlling spermathecal contractions in Locusta migratoria". Journal of Insect Physiology. 47 (6): 607–616. doi:10.1016/S0022-1910(00)00149-9. PMID   11249949.
  43. ↑ Avila, F. W; Wolfner, M. F (2009). "Acp36DE is required for uterine conformational changes in mated Drosophila females". Proceedings of the National Academy of Sciences. 106 (37): 15796–800. doi: 10.1073/pnas.0904029106 . JSTOR   40484802. PMC   2747198 . PMID   19805225.
  44. 1 2 Clark, Julie; Lange, Angela B (2001). "Evidence of a neural loop involved in controlling spermathecal contractions in Locusta migratoria". Journal of Insect Physiology. 47 (6): 607–616. doi:10.1016/s0022-1910(00)00149-9. PMID   11249949.
  45. ↑ Arthur, B; Hauschteck-Jungen, E; Nothiger, R; Ward, P. I (1998). "A female nervous system is necessary for normal sperm storage in Drosophila melanogaster: A masculinized nervous system is as good as none". Proceedings of the Royal Society B: Biological Sciences. 265 (1407): 1749–53. doi:10.1098/rspb.1998.0498. JSTOR   51255. PMC   1689365 .
  46. 1 2 Fritz, Ann H (2002). "A Single, Abdominal Ganglion in Anastrepha suspensa (Diptera: Tephritidae) and Its Innervation of the Female Sperm Storage Organs". Annals of the Entomological Society of America. 95 (1): 103–8. doi: 10.1603/0013-8746(2002)095[0103:asagia]2.0.co;2 .
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.