Monogyny

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Monogyny is a specialised mating system in which a male can only mate with one female throughout his lifetime, but the female may mate with more than one male. In this system, the males generally provide no paternal care. [1] In many spider species that are monogynous, the males have two copulatory organs, which allows them to mate a maximum of twice throughout their lifetime. [2] As is commonly seen in honeybees, ants and certain spider species, a male may put all his energy into a single copulation, knowing that this will lower his overall fitness. During copulation, monogynous males have adapted to cause self genital damage or even death to increase their chances of paternity.

Contents

Definition and distinction

Monogyny is one of several mating systems observed in nature, in which a male mates only once; females, however, may mate with multiple males. It is important to emphasize the distinctions between monogyny and polyandry, and monogyny and monogamy. Polyandry is a mating system by which a female mates with more than one male; the male, in turn, can also mate with more than one female. In a monogamous setting, both male and female consent to having only one mate at any one time and thus mate only with that partner for that time period. Hence, monogyny is sometimes referred to as male monogamy because the male only mates with one female. [2]

Examples

The mating system of monogyny is most common in ants, honeybees, and spiders.

In colony species

In species of ants and honeybees, there is only one female queen who mates with all the males in her colony; the males attend to the queen and mate only with her. There are circumstances, however, where a colony can become queenless, and therefore certain males must adapt to this surrounding in order to increase paternity. In ants and honeybees, there are two different types of monogynous settings. Type A are monogynous, queenright colonies where the queen is the mated female and everyone else is unmated. Type B are monogynous, worker-reproductive colonies where there is no queen, but rather there are gamergates, which are mated workers who take on a queen-like role. [3] The queen is normally the only egg producer. However, when a colony becomes queenless, some workers which have intact, undeveloped ovaries may develop them and thus become capable of laying more eggs. [4] So in certain colonies, a singly mated worker called a gamergate reproduces as the functional queen in that colony. [5] These workers are termed "totipotent"; that is, they are able to change and adapt to a different surrounding in which they no longer have a queen.

In spiders

Males in certain species of spiders often employ drastic methods to be paternally successful. Monogyny in spiders culminates in extreme traits, such as dramatic male self-sacrifice and emasculation of the male by the female during copulation. [6] Since males only mate with one female in a monogynous setting, each individual male must do whatever it takes to increase his particular paternity success, even if it means sacrificing himself. Male redback spiders twist their abdomens onto the fangs of their mates during copulation and, if cannibalized (65% of matings), increase their paternity relative to males that are not cannibalized. [7] In this way, males of the redback spiders in a monogynous setting increase their chance of paternity by actually surrendering themselves to be cannibalized by the female.

Male sacrifice tactics

Genital plugging

The benefits of mate guarding and securing paternity are higher than searching for many mates in a monogynous system. A male securing his paternity becomes a male's first priority during reproduction. One way they mate guard is by creating a physical barrier to turn away any other males. The male can cause severe physical damage to themselves by breaking off their pedipalps in order to plug the genital opening of the female. Males of Argiope bruennichi remove their pedipalp into the females and thus reduce the risk of sperm competition. Males can also remove the sperm of a previous mate from the female and deposit their own sperm, increasing their likelihood of success in that copulation. In the golden orb spider, the male may sacrifice both of his copulatory organs in one mating in order to turn away any wandering males. [8] In other cases, we see the casting off of other body parts such as the anterior legs in the golden orb spider when the male is attacked by an aggressive female. By doing this, he can continue to mate with her while she eats his legs and does not eat him whole. [8]

Self sacrifice and cannibalism

Copulation in a monogynous male is a sacrificial system. They not only cause genital damage to themselves but, in many cases, die during copulation spontaneously such as Argiope aurantia or are cannibalized by the female. This can be observed in many spider species, such as the red back spider which consumes the male either during or right after copulation if the male is not quick enough to escape. [7] The size and age of the female play a role in whether or not the male is able to escape. They usually are not successful in the attempt to escape if the female is older and heavier making her much more dominant than the male. Another factor in the survival or demise of the male is the duration of the copulation. If there is a high copulation time the chances of him being eaten are much higher. If the copulation has a duration of ten seconds or more, the chances of him being eaten are much greater than those that jump off before ten seconds. [7] Monogyny increases a male's chance of paternity when there is a male biased ratio in the population. When males make up a large majority of the population, the likelihood of finding multiple females is slim. Thus the males will mate with the first female they encounter. Mate guarding her from other males is more beneficial than looking for another female because the odds of meeting another female in a male biased population are against him. [1]

Costs and benefits

From a male standpoint, evolutionary theory suggests that the focus of mating is to enhance paternity in order to produce viable offspring. Therefore, sexual selection theory would suggest that a male should attempt to mate with several females. [2] This means that if a male wants to ensure that he will be paternally successful, he should mate with more than one female. When the sex ratio is male biased, however, male monogamy (monogyny) would arise as a means of increasing paternity and producing offspring; in other words, if the setting contains a sex ratio of all male to one female, then monogyny would arise as a means to produce offspring. This model predicts that a male-biased sex ratio is required for monogyny to evolve. [9]

Male adaptation

Males can adapt in order to increase paternity in a monogynous setting. An example of this would be the formation of gamergates in a queenless colony of honeybees and/or ants. Another example would be male-sacrifice in order to increase paternity in certain species of spiders. The costs of increasing paternity in a monogynous setting are great for the males; in certain species of spiders the male will surrender himself to be cannibalized in order to increase paternity. In this respect, the benefit for the female is that she will receive the chance to eat if she is hungry; the cost for the male is the loss of life to increase his paternity.

In certain species, male adaptation will include the process of pedipalp damage. Males in species of the golden orb weaver, for instance, can protect their paternity by obstructing the female's genital openings with fragments of their copulatory organs. The male will actively participate in damaging his genitals by breaking off parts of his copulatory organs during mating and obstructing the female's genital openings in order to be paternally successful. [10]

Evolutionary significance

Male animals, especially in species where males provide little or no parental investment (time and energy invested in current offspring at the expense of future offspring), are generally expected to maximize their fitness by mating with several females. [10] In certain monogynous settings, however, paternal investment by the male is greater than that of males in other mating systems because the benefits of paternal protection exceed those of searching for additional mates. [8] Paternal investment includes even dramatic examples such as the remarkable adaptation of male sacrifice via sexual cannibalism and the ability to inflict genital damage on oneself to increase paternity success. In these circumstances, selection may favor extreme mechanisms of paternity protection that amount to a maximal investment in a single mating.

There are also circumstances in which monogyny evolves when males do not provide any paternal investment. Researchers have focused on sexual behaviour in systems where males have low paternal investment but frequently mate only once in their lifetimes, after which they are often killed by the female. Mating effort is high for these males. In particular, time and energy costs or risks incurred by males in securing a given mating could decrease the relative number of males available for mating; this type of mating is called non-promiscuous. [1] Researchers have focused on species of web-building spiders with males that show high levels of non-promiscuous mating effort but apparently low paternal investment. The mechanism of male monogamy (monogyny) in these species is indisputably the most extreme form of non-promiscuous mating effort. [1]

Related Research Articles

<i>Argiope bruennichi</i> Species of orb-weaver spider

Argiope bruennichi, commonly known as the wasp spider, is a species of orb-weaver spider found across Central and Northern Europe, several regions of Asia, plus parts of the Middle east, North Africa and the Azores. Like many other members of the same genus Argiope, this species features distinctive yellow, white and black markings on its abdomen.

Monogamous pairing in animals refers to the natural history of mating systems in which species pair bond to raise offspring. This is associated, usually implicitly, with sexual monogamy.

<span class="mw-page-title-main">Spider cannibalism</span> Spiders consuming all or part of another individual of the same species as food

Spider cannibalism is the act of a spider consuming all or part of another individual of the same species as food. It is most commonly seen as an example of female sexual cannibalism where a female spider kills and eats a male before, during, or after copulation. Cases of non-sexual cannibalism or male cannibalism of females both occur but are notably rare.

<i>Metellina segmentata</i> Species of spider

Metellina segmentata is a spider in the family Tetragnathidae with a Palaearctic distribution. This spider's name is often shortened to Meta segmentata, and some even call it Araneus segmentatus simply meaning, orb weaving spiders. It is primarily found in Europe, with the highest number in the United Kingdom, but the species has also been introduced to Canada.

<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, several insect and crustacean clades, gastropods, and some snake species. 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.

<span class="mw-page-title-main">Parental care</span> Behavior in animals of taking care of offspring

Parental care is a behavioural and evolutionary strategy adopted by some animals, involving a parental investment being made to the evolutionary fitness of offspring. Patterns of parental care are widespread and highly diverse across the animal kingdom. There is great variation in different animal groups in terms of how parents care for offspring, and the amount of resources invested by parents. For example, there may be considerable variation in the amount of care invested by each sex, where females may invest more in some species, males invest more in others, or investment may be shared equally. Numerous hypotheses have been proposed to describe this variation and patterns in parental care that exist between the sexes, as well as among species.

<i>Unicorn</i> (spider) Genus of spiders

Unicorn ("one horn", in Latin) is a genus of goblin spiders from South America, containing seven species that occur predominantly in high elevation, semi-desert regions of Bolivia, Chile, and Argentina. Individuals are relatively large for goblin spiders, measuring up to 3.0 mm (0.12 in) in body length. The genus name refers to a characteristic pointed projection between the eyes and jaws of males. In at least one species, broken-off tips of the male pedipalps have been found within the genitalia of females, postulated as a means of sperm competition. Unicorn possesses several traits that suggest it is a relatively "primitive" member of the Oonopidae, and is classified with other similar, soft-bodied goblin spiders in the subfamily Sulsulinae.

Female copulatory vocalizations, also called female copulation calls or coital vocalizations, are produced by female primates, including human females, and female non-primates. Copulatory vocalizations usually occur during copulation and are hence related to sexual activity. Vocalizations that occur before intercourse, for the purpose of attracting mates, are known as mating calls.

Formally, a nuptial gift is a material presentation to a recipient by a donor during or in relation to sexual intercourse that is not simply gametes in order to improve the reproductive fitness of the donor. Often, such a gift will improve the fitness of the recipient as well. This definition implies neutral gifts, costly gifts and beneficial gifts regarding the fitness of the recipient.

<i>Pisaurina mira</i> Species of spider

Pisaurina mira, also known as the American nursery web spider, is a species of spider in the family Pisauridae. They are often mistaken for wolf spiders (Lycosidae) due to their physical resemblance. P. mira is distinguished by its unique eye arrangement of two rows. 

<i>Carabus insulicola</i> Species of beetle

Carabus insulicola is a species of black-colored beetle from the family Carabidae native to Japan. They are also known as ground beetles, and are oval shaped and elongated. They are black with a green metallic hue and vertical stripes running down their backs. The length of a fully grown beetle ranges from 27 to 31 mm. They have three pairs of legs and two pairs of wings. The outer wings are greatly degenerated, making them unable to fly. However, their relatively long legs allow them to walk and run fast. They have prominent mandibles that allow them to capture and eat prey.

<span class="mw-page-title-main">Gamergate (ant)</span> Reproductively viable female worker ant

A gamergate is a mated worker ant that can reproduce sexually, i.e., lay fertilized eggs that will develop as females. In the vast majority of ant species, workers are sterile and gamergates are restricted to taxa where the workers have a functional sperm reservoir ('spermatheca'). In some species, gamergates reproduce in addition to winged queens, while in other species the queen caste has been completely replaced by gamergates. In gamergate species, all workers in a colony have similar reproductive potentials, but as a result of physical interactions, a dominance hierarchy is formed and only one or a few top-ranking workers can mate and produce eggs. Subsequently, however, aggression is no longer needed as gamergates secrete chemical signals that inform the other workers of their reproductive status in the colony.

<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 surviving only a few matings and consequently having short life-spans.

<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, the adzuki bean weevil, 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.

<span class="mw-page-title-main">Palpal bulb</span> Part of a pedipalp of a male spider

The two palpal bulbs – also known as palpal organs and genital bulbs – are the copulatory organs of a male spider. They are borne on the last segment of the pedipalps, giving the spider an appearance often described as like wearing boxing gloves. The palpal bulb does not actually produce sperm, being used only to transfer it to the female. Palpal bulbs are only fully developed in adult male spiders and are not completely visible until after the final moult. In the majority of species of spider, the bulbs have complex shapes and are important in identification.

<span class="mw-page-title-main">Nephilidae</span> Spider family

Nephilidae is a spider family commonly referred to as golden orb-weavers. The various genera in Nephilidae were formerly placed in Tetragnathidae and Araneidae. All nephilid genera partially renew their webs.

<i>Philodromus cespitum</i> Species of spider

Philodromus cespitum is a species of running crab spider in the family Philodromidae. It is found in North America, Europe, North Africa, and parts of the Middle East and Asia. P. cespitum is a foliage-dweller, and is the most abundant species found in European fruit orchards. It acts as a biological control by preying on orchard pests. P. cespitum is a diurnal ambush hunter and preys on aphids, insects, and occasionally competitor spider species. Males court females by tapping on the females’ bodies with their forelegs. They then insert a genital plug into the female during copulation. Unlike in many other spider species, subsequent males can mate with plugged females by removing part of the plug prior to copulation. Males discriminate among females based on virginity and plug size, and can determine these factors using the females’ draglines and plug samples.

Agelenopsis pennsylvanica, commonly known as the Pennsylvania funnel-web spider or the Pennsylvania grass spider, is a species of spider in the family Agelenidae. The common name comes from the place that it was described, Pennsylvania, and the funnel shape of its web. Its closest relative is Agelenopsis potteri.

<i>Pardosa pseudoannulata</i> Species of arachnid

Pardosa pseudoannulata, a member of a group of species referred to as wolf-spiders, is a non-web-building spider belonging to the family Lycosidae. P. pseudoannulata are wandering spiders that track and ambush prey and display sexual cannibalism. They are commonly encountered in farmlands across China and other East Asian countries. Their venom has properties that helps it function as an effective insecticide, and it is, therefore, a crucial pesticide control agent.

<i>Larinia jeskovi</i> Species of arachnid

Larinia jeskovi is a species of the family of orb weaver spiders and a part of the genus Larinia. It is distributed throughout the Americas, Africa, Australia, Europe, and Asia and commonly found in wet climes such as marshes, bogs, and rainforests. Larinia jeskovi have yellow bodies with stripes and range from 5.13 to 8.70 millimeters in body length. They build their webs on plants with a small height above small bodies of waters or wetlands. After sunset and before sunrise are the typical times they hunt and build their web. Males usually occupy a female's web instead of making their own. The mating behavior is noteworthy as male spiders often mutilate external female genitalia to reduce sperm competition while female spiders resort to sexual cannibalism to counter such mechanisms. The males also follow an elaborate courtship ritual to attract the female. The bite of Larinia jeskovi is not known to be of harm to humans.

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