Cryptic female choice

Last updated October 15, 2023

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.

The present understanding of cryptic female choice is largely thanks to the extensive research and analysis done by William G. Eberhard. The term ‘cryptic’ according to Eberhard is meant to describe an internal and thereby hidden choice some female organisms are able to make following insemination with regards to sperm selection.^[1]^: 7–9 In male species with intromittent organs, during copulation, a male inserts his reproductive organ into that of a female's so as to inseminate her with his genetic material. Through the development of mechanisms that either prematurely inhibit copulation or act following male insemination, females are able to prevent undesirable males from successfully fertilizing their eggs.^[1]^: 5 Thus, not every copulatory event is successful – there are many factors that combine to determine whether or not an offspring is created. It is likely that cryptic female choice is a consequence of the conflict between the reproductive desires of males and females.^[1]^: 22 While males commonly increase their reproductive success by maximally fertilizing each female they mate with, females can incur costs to their personal health as a result of such behavior. Cryptic female choice reduces these costs by allowing them to also benefit from and select for favorable matings.

Theory

Females not only exert sexual control but also benefit from exerting such control over male reproductive success. It has been observed that in some species males continue to court females following copulation, which illuminates the fact above. This female control compels males to continue to impress their female counterparts following copulation.^[2] The assumption above can be made because there is an energetic cost for a male to continue to court a female following insemination because he has to invest energy to do so. And, because there is an energetic investment he must benefit in some way. As such, sexual selection does not only act on traits that influence female mate choice of males but it also acts on male traits that determine his success following copulation.

There are circumstances in nature in which a male's interaction with a female is of detriment to her personal well-being and that of her offspring, one such situation, sexual coercion, occurs when a male harasses a female prior to copulation. In such circumstances where the female's lifespan and fertility are compromised, it benefits females to develop evasive mechanisms.^[1]^: 23 In addition, in some species where multiple males inseminate a female, a female is able to select the most desirable sperm for her offspring by rejecting that which she desires less.^[1]^: 233 In both of the aforementioned situations it is a female's reproductive actions that affect male reproductive success following copulation.^[1]^: 3–7 As discussed below, female species that are able to use cryptic choice have developed various mechanisms to manipulate male reproductive success. Species that are able to use cryptic choice only use one of the below mechanisms to do so. Regardless of the mechanism, this ability allows females to respond differently to conspecific males depending on whether the male that inseminates her is favorable to her or not.^[1]^: 5

Mechanisms of cryptic female choice

Many mechanisms exist in the animal world that allow females to practice cryptic female choice by manipulating which reproductive events are successful or not. These choices can occur at varying stages of the reproductive process.

Pre-copulation

Pre-Copulation – female cryptic choice can include physical, anatomical, and chemical barriers that can promote or hinder a male's success in the mating process.^[1]^: 45

Morphology

(Physical/Anatomical): At the pre-copulatory level female cryptic choice consists of the physical and anatomical barriers that females use to decide whether a male is successful or not. This can fall under two subcategories as a result of mating strategies:

Antagonistic coevolution: Among species that mate multiple times, studies have shown much greater divergence in genital morphology than in species who mate singly. The rapid evolution of internal female and male reproductive morphology is due to the high sexual selection pressures characteristic of polygamous populations. In such cases, females can use cryptic female choice in choosing for or resisting males with specific physical or anatomical traits.^[1]^: 22 Duck genitalia and anatomical evolution is a prime example of this male-female conflict through evolution of internal anatomical barriers.^[3]
Coevolution: Female cryptic choice may also act indirectly by choosing for males with subtle secondary sexual traits that may cater to easier insemination and mating. In these instances female cooperation during the mating process is crucial for male success. For example, in the yellow fever mosquito, successful copulation requires a multistep process with a cooperative and receptive female.^[1]^: 97 In the Caribbean fruit fly, males must display a specific calling song to induce female cooperation which allows the male to penetrate the female deeply, increasing his chances of success.^[1]^: 101

In both cases, without the compliance of the female, the male will be unsuccessful in his mating attempt. As such, females can choose for specific male traits by hindering complete intromission or ejaculation during mating.

Chemical

At the pre-copulatory level female cryptic choice can also be employed through chemical means to allow for mating with some males while deceiving other males.

Masking estrus cycle : Female cryptic choice can also occur when females mask their estrus cycle. Specifically in mammals, by hiding the timing of their estrus cycle, females can avoid male control and pursue their own reproductive strategies. This way a female in estrus can sometimes avoid being swamped by competing males or she can prevent male harassment, coercion, or forced mating.^[4]

Insemination

Female cryptic choice can also occur after the male has mated and released his sperm.

Copulation times: A longer copulation time generally means increased mating success for a male. A female may exercise cryptic female choice by determining whether a male can mate for longer or for shorter periods of time, thus increasing or decreasing male insemination success. In hanging flies, females allows males that provide larger nuptial gifts to copulate longer, which increases male fitness.^[1]^: 69 In the tiger beetle, females sometimes forcefully terminate a copulation to deny male insemination.^[1]^: 127
Discard current sperm: During most copulatory events, only a fraction of a male's sperm is usually taken up and stored by the female. In some species, females can sometimes discard sperm by sperm ejection, releasing sperm after mating so that they are free to mate again if another, more preferred male comes along. Females can also sometimes exercise cryptic female choice by mating several times and selectively discarding sperm from certain males while retaining those from preferred males. In Drosophila flies and in field crickets, females mate multiply and select for sperm or spermatophores of certain males.^[1]^: 17, 88
Destroy current sperm: Females can also exercise cryptic female choice by committing spermatocide. They can sometimes destroy stored male sperm through various means, usually chemically (raising pH, hormones, bodily chemical fluids, etc.) after a mating to allow for a second male to successfully inseminate her.

Copulatory plug
Copulatory plug: After inseminating a female, certain species of males will then insert a copulatory plug to prevent females from mating again, or to discourage or prevent other males from displacing their sperm. Some females have the ability to either keep or remove the plug and thus choose which sperm they select to keep. Females can remove this plug so they may successfully re-mate again if a better prospect comes along.^[1]^: 146
Sperm-transplant: Females can also exercise cryptic female choice by preventing the transfer of sperm to a storage organ or fertilization sites. This can occur through various means such as muscular contractions, hormones, nervous control, or bodily fluids or chemicals, etc. In some lab rats females demonstrated their ability to halt sperm transport by re-mating more quickly after certain mating events.^[1]^: 106
Make subsequent sperm transfer more difficult morphologically: Females can sometimes influence ease of sperm transfer during mating. In certain species of arthropods, such as the golden silk spider, some females can change the rate at which the cuticle of their genitalia hardens to manipulate ease of sperm transfer.^[1]^: 179

Fertilization

Females can also exercise cryptic female choice during the fertilization processes.

Sperm bias in storage or transportation

By utilizing sperm storage and transplant, females can exercise cryptic female choice by storing or transplanting sperm to bias sperm success rates towards certain males.^[1]^: 166

Adjacent sperm storage organs: Females can sometimes store sperm in adjacent organs, especially when they mate multiply and thus give unequal preference to certain males. In many polygamous species, males often have the ability to displace a previous male's sperm. In response to this, females retain control of sperm choice by using multiple sperm storage sites to exercise cryptic female choice. By moving sperm to adjacent organs females can prevent particular sperm from being displaced and save the displaced sperm for fertilization. Moving the sperm can also prevent it from continuing on in the fertilization process. In the Dryomiza anilis fly and in the flour beetle, females choose sperm from a number of different storage locations.^[1]^: 169 In the red flour beetle, females often possess several storage receptacles for sperm from different males, and can choose which sperm to utilize for fertilization.^[5]
Sperm transplant: Similar to sperm storage mechanisms of cryptic female choice, females can exercise cryptic female choice by promoting or hindering sperm movement in and out of the reproductive tract into storage structures through muscular contractions.

Failing to prepare uterus for embryo implantation

Females can control hormonal signals that halt embryo preparation to keep sperm from successfully fertilizing the embryo. They can also promote or hinder ovulation as a means of exercising cryptic female choice. By hindering ovulation, a copulatory interaction may be deemed unsuccessful. In rats and golden hamsters, females denied a male's success by failing to prepare their uterus based on male stimulation.^[1]^: 143

Select for or against sperm during hyperactivation

After insemination, male sperm are relatively slow and inert in the reproductive tracts or storage areas of the female and are only activated by calcium ionophores in vitro. Thus by releasing or withholding the necessary ions to activate the sperm, females can promote faster motility of sperm towards the egg for fertilization or hinder it by slowing their motility and allowing them to die before they reach the egg respectively.^[6]

Choosing from among sperm to reach the egg

Female ovarian fluids can promote or hinder sperm especially if they have complementary or uncomplimentary chemical signals. Some females may also physically choose from among spermatophores taken from multiple matings.

Failure to ovulate

Females can sometimes change their differential ovulation responses based on male stimuli to affect male reproductive success. In lions some females will reduce fertility after the male commits infanticide, resulting in low offspring counts after a new male takes over a pride.^[1]^: 135

Gestation

Even after fertilization has occurred, females can exercise cryptic female choice.

Abortion: By aborting the zygote or the fetus through female resistance or acceptance of male induced abortion signals, a female can exercise cryptic female choice. [1] : 162
Reduce rate of offspring produced: Females can sometimes adjust rates of oviposition to determine the number of successful offspring a male's sperm will produce after a mating event. In the leaf-rolling frog, females can delay spawn times which determines the number of final offspring produced from a mating event.^[1]^: 124
Fail to mature eggs: Some females can deny male reproductive success by controlling the development and maturation of eggs in her ovary. In the red garter snake, some females failed to produce eggs after a mating event.^[1]^: 140

Post-birth

Even after birth has occurred, females can manipulate male offspring success.

Invest less in each offspring: by altering rates of investment in an offspring, a female can sometimes exercise cryptic female choice.^[1]^: 184

Examples

Theropithecus gelada BabouinGeladaPortrait.JPG — Theropithecus gelada

The wide variety of species around the world provides us with many examples of each mechanism of cryptic female choice. This section provides a more detailed example of a few of the mechanisms of cryptic female choice seen in particular species.

In the Cassadine Plant Beetle, Chelymorpha alternans, the female has a complexly coiled spermathecal duct that frequently reverses in direction. With this reversal, the female is able to discriminate between males' gentalic sclerite. This is an example of a copulatory mechanism where the female actively hinders a successful mating.^[1]

The Sand Lizard, Lacerta agilis, provides us an example of cryptic female choice during the insemination phase of mating. Females routinely and indiscriminately copulate with several males. The females who mate more often have greater hatching success, lowering the incidence of deformities among offspring, and enhancing survival of free-living offspring. The aforementioned consequences are a result of the females' ability to differentially use the sperm from the least related male. Thus, the males most genetically similar to the female sire less offspring.^[7]

Some species have a sperm transplant mechanism. Crickets are one such species that can prematurely remove spermatophore after copulation, which terminates sperm transfer. In one study, males were randomly assigned to females to create half-sib families to determine the heritability of spermatophore retention time in females. The researchers found that there was additive genetic variance in the timing of spermatophore removal by females. These results suggest that the timing of the spermatophore removal is determined partly by genotype and is independent of the quality of a female's mate. This shows no difference between the fitness of females who freely remove the spermatophore and the fitness of females that are forced to accept complete ejaculates.^[8]

The female spider, Pisaura mirabilis , stores more sperm from males who give a nuptial gift compared to those who share no such gift.^[9] This shows a biased use of stored sperm and hence cryptic female choice in a post-copulatory mechanism.

Theropithecus gelada is a wild primate that demonstrates cryptic female choice through a gestation mechanism. The females have been reported to have a strong Bruce effect. Bruce effect is when the female terminates the pregnancy when she is exposed to an unrelated male.^[10] Female gelada's terminate about 80% of their pregnancies the week after the dominant male has been replaced. This could be because males typically perform infanticide when they take over a new group. Terminating a pregnancy could be a female's way to protect herself and avoid infanticide of her young. Studies have been shown to support the hypothesis that the Bruce effect can be an adaptive strategy for females.^[10]

The Japanese pygmy squid, Idiosepius paradoxus , is yet another example of a species which exhibits cryptic female choice. The males place spermatangia on an external location on the female's body, and the female is able to physically remove spermatangia to select for preferred traits in males, enacting postcopulatory intersexual selection.^[11]^[12]

Species of Harpobittacus, a genus of hanging fly or scorpionfly, are another example. Females exercise post-copulatory control after mating with multiple males by determining rate of fertilization by each male. Females continue to mate with different males until finding one with a large nuptial gift, upon which she enters a period of sexual non-receptivity and begins laying eggs.^[13]

Related Research Articles

In biology, mating is the pairing of either opposite-sex or hermaphroditic organisms for the purposes of sexual reproduction. Fertilization is the fusion of two gametes. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization. Mating may also lead to external fertilization, as seen in amphibians, fishes and plants. For most species, mating is between two individuals of opposite sexes. However, for some hermaphroditic species, copulation is not required because the parent organism is capable of self-fertilization (autogamy); for example, banana slugs.

The Coolidge effect is a biological phenomenon seen in animals, whereby males exhibit renewed sexual interest whenever a new female is introduced, even after sex with prior but still available sexual partners. To a lesser extent, the effect is also seen among females with regard to their mates.

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 physically removing another male's sperm prior to mating with a female. For an example, see Gryllus bimaculatus.

Insemination is the introduction of sperm into a female's reproductive system for the purpose of impregnating, also called fertilizing, the female for sexual reproduction. The sperm is introduced into the uterus of a mammal or the oviduct of an oviparous (egg-laying) animal. In mammals, insemination normally occurs during sexual intercourse or copulation, but insemination can take place in other ways, such as by artificial insemination.

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.

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 spines or hooks. The female homologue is the hemiclitoris.

<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.

<span class="mw-page-title-main">Sexual cannibalism</span> Practice of animals eating their own mating partners

Sexual cannibalism is when an animal, usually the female, cannibalizes its mate prior to, during, or after copulation. It is a trait observed in many arachnid orders and several insect orders. Several hypotheses to explain this seemingly paradoxical behavior have been proposed. The adaptive foraging hypothesis, aggressive spillover hypothesis and mistaken identity hypothesis are among the proposed hypotheses to explain how sexual cannibalism evolved. This behavior is believed to have evolved as a manifestation of sexual conflict, occurring when the reproductive interests of males and females differ. In many species that exhibit sexual cannibalism, the female consumes the male upon detection. Females of cannibalistic species are generally hostile and unwilling to mate; thus many males of these species have developed adaptive behaviors to counteract female aggression.

Idiosepius paradoxus, also known as the northern pygmy squid, is a species of pygmy squid native to the western Pacific Ocean. This species can be found inhabiting shallow, inshore waters around central China, South Korea, and Japan.

Traumatic insemination, also known as hypodermic insemination, is the mating practice in some species of invertebrates in which the male pierces the female's abdomen with his aedeagus and injects his sperm through the wound into her abdominal cavity (hemocoel). The sperm diffuses through the female's hemolymph, reaching the ovaries and resulting in fertilization.

The ocoee salamander is a species of salamander in the family Plethodontidae. This salamander has a variety of colors and patterns, and got its name from Tennessee state wildflower. Its natural habitats are temperate forests, rivers, intermittent rivers, freshwater springs and wet rocks in mountainous areas of the Southeastern United States. It was first described by Nicholls in 1949. They are territorial and feed on small invertebrates. It is widely distributed in the southeastern United States and is listed as "Least Concern" by the International Union for Conservation of Nature.

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.

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, see Mating of gastropods.

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. 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 and bird sperm storage tubules, 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. Female sperm storage is an integral stage in the reproductive process for many animals with internal fertilization. It has several documented biological functions including:

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.

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

Sexual selection in birds concerns how birds have evolved a variety of mating behaviors, with the peacock tail being perhaps the most famous example of sexual selection and the Fisherian runaway. Commonly occurring sexual dimorphisms such as size and color differences are energetically costly attributes that signal competitive breeding situations. Many types of avian sexual selection have been identified; intersexual selection, also known as female choice; and intrasexual competition, where individuals of the more abundant sex compete with each other for the privilege to mate. Sexually selected traits often evolve to become more pronounced in competitive breeding situations until the trait begins to limit the individual's fitness. Conflicts between an individual fitness and signaling adaptations ensure that sexually selected ornaments such as plumage coloration and courtship behavior are “honest” traits. Signals must be costly to ensure that only good-quality individuals can present these exaggerated sexual ornaments and behaviors.

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.

<span class="mw-page-title-main">Sexual selection in spiders</span>

Sexual selection in spiders shows how sexual selection explains the evolution of phenotypic traits in spiders. Male spiders have many complex courtship rituals and have to avoid being eaten by the females, with the males of most species survive a few matings, and having short life spans.

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.

References

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Eberhard, William G. (1996). Female control: sexual selection by cryptic female choice. Princeton, NJ: Princeton Univ. Press. ISBN 9780691010847.
↑ Eberhard, William G (1991). "Copulatory Courtship and Cryptic Female Choice in Insects". Biological Reviews. 66 (1): 1–31. doi:10.1111/j.1469-185X.1991.tb01133.x. S2CID 85822041.
↑ Brennan, Patricia LR; et al. (2007). "Coevolution of male and female genital morphology in waterfowl". PLOS ONE. 2 (5): e418. Bibcode:2007PLoSO...2..418B. doi: 10.1371/journal.pone.0000418 . PMC 1855079 . PMID 17476339.
↑ Reeder, D. M. "The potential for cryptic female choice in primates: behavioral, anatomical, and physiological considerations." Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman (2003): 255-303.
↑ Fedina, Tatyana Yu; Lewis, Sara M. (2004-07-07). "Female influence over offspring paternity in the red flour beetle Tribolium castaneum". Proceedings of the Royal Society of London B: Biological Sciences. 271 (1546): 1393–1399. doi:10.1098/rspb.2004.2731. ISSN 0962-8452. PMC 1691742 . PMID 15306338.
↑ Ziegler, Andreas; Kentenich, Heribert; Uchanska-Ziegler, Barbara (2005). "Female choice and the MHC". Trends in Immunology. 26 (9): 496–502. doi:10.1016/j.it.2005.07.003. PMID 16027037.
↑ Birkhead, T.R. (1998). "Cryptic Female Choice: Criteria for Establishing Female Sperm Choice". Evolution. 52 (4): 1212–1218. doi: 10.1111/j.1558-5646.1998.tb01848.x . JSTOR 2411251. PMID 28565225.
↑ Mautz, B.; Sakaluk, S. (2008). "Heritable variation in the timing of spermatophore removal, a mechanism of post-copulatory female choice in crickets". Journal of Evolutionary Biology. 21 (5): 1366–1370. doi: 10.1111/j.1420-9101.2008.01560.x . PMID 18544069.
↑ Albo, M.; Bilde, T.; Uhl, G. (2013). "Sperm storage is mediated by female favoritism for males who present nuptial gifts". Proceedings of the Royal Society B: Biological Sciences. 280 (1772): 20131735. doi: 10.1098/rspb.2013.1735 . PMC 3813325 . PMID 24266042.
1 2 Roberts, E. K.; Lu, A.; Bergman, T. J.; Beehner, J. C. (23 February 2012). "A Bruce Effect in Wild Geladas". Science. 335 (6073): 1222–1225. Bibcode:2012Sci...335.1222R. doi: 10.1126/science.1213600 . PMID 22362878. S2CID 34095168.
↑ Sato, Noriyosi; Yoshida, Masa-aki; Kasugai, Takashi (2016-11-17). "Impact of cryptic female choice on insemination success: Larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia". Evolution. 71 (1): 111–120. doi:10.1111/evo.13108. ISSN 0014-3820.
↑ Sato, Noriyosi; Kasugai, Takashi; Munehara, Hiroyuki (2013-03-01). "Sperm transfer or spermatangia removal: postcopulatory behaviour of picking up spermatangium by female Japanese pygmy squid". Marine Biology. 160 (3): 553–561. doi:10.1007/s00227-012-2112-5. hdl: 10069/31698 . ISSN 1432-1793.
↑ Thornhill, Randy (December 1983). "Cryptic Female Choice and Its Implications in the Scorpionfly Harpobittacus nigriceps". The American Naturalist. 122 (6): 765–788. doi:10.1086/284170. ISSN 0003-0147.

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[Eberhard-1] 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Eberhard, William G. (1996). Female control: sexual selection by cryptic female choice. Princeton, NJ: Princeton Univ. Press. ISBN 9780691010847.

[2] Eberhard, William G (1991). "Copulatory Courtship and Cryptic Female Choice in Insects". Biological Reviews. 66 (1): 1–31. doi:10.1111/j.1469-185X.1991.tb01133.x. S2CID 85822041.

[3] Brennan, Patricia LR; et al. (2007). "Coevolution of male and female genital morphology in waterfowl". PLOS ONE. 2 (5): e418. Bibcode:2007PLoSO...2..418B. doi: 10.1371/journal.pone.0000418 . PMC 1855079 . PMID 17476339.

[4] Reeder, D. M. "The potential for cryptic female choice in primates: behavioral, anatomical, and physiological considerations." Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman (2003): 255-303.

[5] Fedina, Tatyana Yu; Lewis, Sara M. (2004-07-07). "Female influence over offspring paternity in the red flour beetle Tribolium castaneum". Proceedings of the Royal Society of London B: Biological Sciences. 271 (1546): 1393–1399. doi:10.1098/rspb.2004.2731. ISSN 0962-8452. PMC 1691742 . PMID 15306338.

[6] Ziegler, Andreas; Kentenich, Heribert; Uchanska-Ziegler, Barbara (2005). "Female choice and the MHC". Trends in Immunology. 26 (9): 496–502. doi:10.1016/j.it.2005.07.003. PMID 16027037.

[7] Birkhead, T.R. (1998). "Cryptic Female Choice: Criteria for Establishing Female Sperm Choice". Evolution. 52 (4): 1212–1218. doi: 10.1111/j.1558-5646.1998.tb01848.x . JSTOR 2411251. PMID 28565225.

[8] Mautz, B.; Sakaluk, S. (2008). "Heritable variation in the timing of spermatophore removal, a mechanism of post-copulatory female choice in crickets". Journal of Evolutionary Biology. 21 (5): 1366–1370. doi: 10.1111/j.1420-9101.2008.01560.x . PMID 18544069.

[9] Albo, M.; Bilde, T.; Uhl, G. (2013). "Sperm storage is mediated by female favoritism for males who present nuptial gifts". Proceedings of the Royal Society B: Biological Sciences. 280 (1772): 20131735. doi: 10.1098/rspb.2013.1735 . PMC 3813325 . PMID 24266042.

[Roberts-10] 1 2 Roberts, E. K.; Lu, A.; Bergman, T. J.; Beehner, J. C. (23 February 2012). "A Bruce Effect in Wild Geladas". Science. 335 (6073): 1222–1225. Bibcode:2012Sci...335.1222R. doi: 10.1126/science.1213600 . PMID 22362878. S2CID 34095168.

[:0-11] Sato, Noriyosi; Yoshida, Masa-aki; Kasugai, Takashi (2016-11-17). "Impact of cryptic female choice on insemination success: Larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia". Evolution. 71 (1): 111–120. doi:10.1111/evo.13108. ISSN 0014-3820.

[:14-12] Sato, Noriyosi; Kasugai, Takashi; Munehara, Hiroyuki (2013-03-01). "Sperm transfer or spermatangia removal: postcopulatory behaviour of picking up spermatangium by female Japanese pygmy squid". Marine Biology. 160 (3): 553–561. doi:10.1007/s00227-012-2112-5. hdl: 10069/31698 . ISSN 1432-1793.

[13] Thornhill, Randy (December 1983). "Cryptic Female Choice and Its Implications in the Scorpionfly Harpobittacus nigriceps". The American Naturalist. 122 (6): 765–788. doi:10.1086/284170. ISSN 0003-0147.

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