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.

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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 the 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 for 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 on whether or not the male was able to escape. They usually were not successful in the attempt to escape if the female was older and heavier making her much more dominant than the male. Another factor on 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 unto 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

<span class="mw-page-title-main">Animal sexual behaviour</span> Sexual behavior of non-human animals

Animal sexual behaviour takes many different forms, including within the same species. Common mating or reproductively motivated systems include monogamy, polygyny, polyandry, polygamy and promiscuity. Other sexual behaviour may be reproductively motivated or non-reproductively motivated.

<span class="mw-page-title-main">Argiope bruennichi</span> Species of orb-weaver spider.

Argiope bruennichi is a species of orb-web spiders distributed throughout Central and Northern Europe, North Africa, parts of Asia, and the Azores archipelago. Like many other members of the genus Argiope, it has strikingly yellow 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.

<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 and crustacean clades. 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.

<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.

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

<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. 

<span class="mw-page-title-main">Worker policing</span> Insects destroying eggs not laid by queen

Worker policing is a behavior seen in colonies of social hymenopterans whereby worker females eat or remove eggs that have been laid by other workers rather than those laid by a queen. Worker policing ensures that the offspring of the queen will predominate in the group. In certain species of bees, ants and wasps, workers or the queen may also act aggressively towards fertile workers. Worker policing has been suggested as a form of coercion to promote the evolution of altruistic behavior in eusocial insect societies.

<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.

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.

<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.

References

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  3. ↑ Ward, P.S. (1983). "Genetic relatedeness and colony organization in a species complex ponerine ants". Genotypic and Phenotypic Composition of Colonies. 12 (4): 285–299. doi:10.1007/BF00302896. JSTOR   4599592. S2CID   24543297.
  4. ↑ Bloch, G. & Hefetz, A. (1999). "Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies". Behavioral Ecology and Sociobiology. 45 (2): 125–135. doi:10.1007/s002650050546. JSTOR   4601585. S2CID   21888119.
  5. ↑ Kikuta, N. & Tsuji, K.. (1999). "Queen and worker policing in the monogynous and monandrous ant, Diacamma sp". Behavioral Ecology and Sociobiology. 46 (3): 180–189. doi:10.1007/s002650050608. S2CID   43077376.
  6. ↑ Michalik, P.; Knoflach, B.; Thaler, K. & Alberti, G. (2010). "Live for the moment—Adaptations in the male genital system of a sexually cannibalstic spider (Theridiidae, Araneae)". Tissue Cell. 42 (1): 32–36. doi:10.1016/j.tice.2009.06.004. PMID   19643451.
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  9. ↑ Schneider, J. & Fromhage, L. (2010). "Monogynous mating strategies in spiders". Animal Behaviour: Evolution and Mechanisms. Springer. pp. 441–464. doi:10.1007/978-3-642-02624-9_15. ISBN   978-3-642-02623-2.
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