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Nuptial gifts are food items or inedible tokens that are transferred to females by males during courtship or copulation. Inedible tokens may include items such as a fragment of leaf or twig, a seed tuft, or a silk balloon. [1] In many species of animals, including birds, insects and spiders, this takes the form of a food item that is transferred by a male to a female just prior to copulation. [2] In many species of animals, including birds, insects and spiders, this takes the form of food that is actively provided by the male in a behaviour known as courtship feeding.[3][4] In some species of insects such as katydids, the nuptial gift is packaged with the sperm of the male. The package is an edible spermatophore. These extra nutrients in the sperm are assimilated by the female and are thought to enhance the fitness of the offspring produced, thus increasing the probability that a male passes on its genes. Nuptial gifts may therefore be classified into oral and seminal gifts.[5] Nuptial gifts may also be tokens that do not have any direct value as food but may serve as an indicator of male fitness.[6][7][8]

Occurrence

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Nuptial gifts are common in insects and other invertebrates, such as butterflies, fruit flies and katydids. They are less common in spiders. Also the spider species Pisaura mirabilis is known for nuptial gift giving.[9] In many species of insects, birds and mammals, males acquire and donate food to females either before, during, or after copulation (termed mate provisioning, courtship feeding, nuptial gift giving, or meat-for-sex). Males may relinquish body parts, produce glandular secretions, or share prey or other food to gain fitness benefits via natural and sexual selection. [10]

Courtship feeding is particularly common among many bird species.[11]

Pisaura mirabilis on Plantago lanceolata

In spiders, nuptial gifts in the form of prey are restricted to a few species from two families belonging to the superfamily Lyvosoidea: Pisauridae and Trechalcidae. In both families, the male courts the female by offering a prey wrapped in silk and mating occurs while the female consumes the gift. In the species Pisaura mirabilis (Pisauridae) the gift functions as a mating effort that increases male mating success. The nuptial gift consists of a prey the male has caught and wrapped up in silk. The male offers this gift during courtship, and if the female accepts the invitation she grabs the wrapped prey. While the female is eating, the male inserts the mating organ and sperm is transferred. [12]

A similar function was recently suggested for the trechaleid spider, Paratrechalea ornata. In both species, males can obtain mating without a gift, but male mating success increases dramatically when a gift is offered. In P.mirabilis, the male pushes up the female during mating and performs alternate pedipalp insertions into the female sperm storage organs place ventrally on the abdomen. After each insertion the male returns to a face-to-face position with the female, grabbing the gift in the chelicerae. Females often control mating duration and they often attempt to run away with the gift upon terminating the copulation. [13]

Females are less likely to succeed in stealing a wrapped rather than an unwrapped gift due to the silk wrapping of the gift. The silk wrapping facilitates male handling and control over the gift, as it facilitates a stronger hold of the silk covered package versus and unwrapped insect. Male spiders have a unique opportunity for gift manipulation through the gift wrapping trait, for example by preventing female assessment of the gift content. By disguising the gift content, males may deceive females to copulate, while the female attempts to consume the gift. In P. ornata, males were observed wrapping prey carrion and occasionally inedible items such as plant seeds. In P. mirabilis, males have been reported to carry gifts containing empty arthropod exoskeletons or plant parts, gifts of no nutritional value.[13]

Paratrechalea ornata
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In the spider species Paratrechalea ornata, a Neotropical spider belonging to the Trechaleidae spider family, nuptial gift behavior was recently seen. Paratrechalea ornata males may present either a wrapped or an unwrapped nuptial prey gift. Prey wrapping seems to be triggered by perception of cues on the female's silk and increases in frequency according to the male's age. [14]

The male great grey shrike, a raptor-like passerine bird, gives prey (rodents, birds, lizards, or large insects) to females immediately before copulation. Shrikes are well known for impaling prey on thorns and sharp sprigs. Great grey shrike females select a mate according to the size of prey impaled, with larders thus serving as an extended phenotype of a male. If the amount of food stored by the males can drive female mate choice, food provided before within and extra pair copulations by males may also influence the female's decision to copulate.[15]

Wedding Rings

Nuptial gift also occurs in humans. Depending on the culture, males are known to exchange gifts to females or the family of the female prior to marriage. Many human societies have a bride price which males pay, usually to a woman’s father, to secure a partner. For marriages in many modern western countries, men offer women diamond rings when making marriage proposals. These arrangements entail a longterm commitment to the monopolization of reproductive currencies by each partner.[16] Among humans, men also often show generous behavior to women as a mating strategy. For example, in a study by Saad and Gill, participants took part in a two-person ultimatum game, in which one was the allocator and the other the recipient and the allocator had to split a given sum of money with the recipient. The recipient could either accept or reject the offer. If accepted, both players received their respective splits, if rejected neither of them got anything. The results showed that men made more generous offers when pitted against a woman as opposed to a man. Women, on the other hand, made equal offers independently of the sex of the recipient. [17]

Decorated Crickets
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In decorated crickets, Gryllodes sigillatus (Orthoptera: Gryllidae), the nuptial food gift is a spermatophylax, a large, gelatinous, sperm-free mass that surrounds a smaller, sperm-containing ampulla. Together, the spermatophylax and the ampulla constitute the male’s spermatophore, which is transferred to the female during copulation and remains attached outside her body at the base of her ovipositor. After mating, the female detaches the spermatophylax from the ampulla and feeds on it while the ampulla remains attached and is emptied of sperm. [18] Once the female has consumed or discarded the spermatophylax, she removes the sperm ampulla, terminating sperm transfer. Female cooperation is required for successful spermatophore transfer, and thus, males cannot impose copulations on females. [19]

Six-spot Burnet

Nuptial gifts are widespread in insects, and comprise food items or glandular products offered as paternal investment in offspring and/or to promote mating. Female Zygaena may use this gift for her own defense and to protect her eggs. [20]


Scorpionfly
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Scorpionfly with prey

In the scorpionfly (Panorpa cognata), males offer a salivary secretion as a nuptial gift before copulation. Exchange of the salivary secretion takes place after prolonged courtship interactions. The nuptial gift is more likely to be accepted by the female if premating duration is long. Males in poor condition with a limited supply of saliva may deliberately delay initiating copulations to decrease the probability that their costly gift is rejected and, thus, wasted. Males in good condition with ample mating resources, on the other hand, may afford the risk of wasting a salivary mass and therefore take every opportunity to mate. [21]

Bushcricket males offer a spermatophylax that contains ampulla. The nuptial gift is also protein rich, which the females ingest into their reproductive tract. The size of the nuptial gifts positively influences the females refractory period and the males reproduction success. The size of the gift depends on the ampulla and serves as a sperm protection. In bushcrickets "Ephippiger ephippiger" the females prefer older males, who have larger spermophores and better nutritional value during mating. The nutritional value is related to the female's metabolism, which stands as a benefit for females feeding on the semaphores. Sometimes males produce lower dosages of sperm with a lower nutritional value the fourth time they mate.[22]


Evolution, costs and benefits

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Male sperm offers many nutrients to increase a female's lifetime and egg production. These nutrients include acids or sodium. Male sperm also protects females and their eggs from predators. The females would also gain a net benefit form a males sperm. Female recipients are supposed to produce bigger offspring than those females who did not receive nuptial gifts. Historically, nuptial gifts were seen as nutritional substances given to females from males during mating.[23] The male benefits from a net fitness. Although the gifts are costly to find or produce, the gifts will increase attraction and copulation with other females. Nuptial gifts can benefit a male by increasing his paternity share when females are promiscuous. In some insects, nuptial gifts allow the male to copulate longer and transfer more sperm to the female.[5] In fruit flies, katydids, and scorpion flies, nuptial gifts contain substances that reduce a female’s receptivity to additional matings. While nuptial gifts also may boost female fecundity, from a male’s perspective, such investment will only be beneficial if it increases the number of his own offspring.[8]

In species where males provide females with a nuptial gift during mating, there is a particular scope for males to manipulate females to acquire matings and prolong copulation to enhance their fertilization success. Female choice for males with nuptial gifts could lead to the evolution of male deception by the use of toke gifts. For instance, males can decrease the costs of mating by re-using gifts or by offering worthless gifts. Males of some dance flies may deceive females by offering inadequate or false gifts. Although males that offer inedible gifts run a higher risk of being rejected and may suffer from shorter mating periods compared to males offering edible gifts the chance of acquiring an extra mating should make deception an attractive strategy for males. Hence, males of the dance fly Rhamphomyia sulcata that use inedible token gifts to obtain mates are as successful as males offering small genuine gifts. [13]

When nuptial gifts are given it increases copulations and searches to find females to mate with. Albo and Costa conducted an experiment with Paratrechala ornata spiders to determine the function of the nuptial gift. Two groups of males were exposed to virgin females, 23 males with no nuptial gift (prey) and 21 males with a nuptial gift (prey). Mating ovulation were recorded and the researchers found that males that gave a nuptial gift had better mating success, longer copulations, and longer palpal insertions than those who did not give an nuptial gift. Longer copulations were associated with earlier egg sac construction and oviposition. The researchers' findings suggest that nuptial gift giving represents male mating effort for P. ornata. Nuptial gifts would allow males to control copulation duration and to accelerate female oviposition, improving sperm supply and paternity, and minimizing possible costs of remating with polyandrous individuals.[13]

References

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  1. ^ LeBas, Natasha R.; and Hockham, Leon R. (2008). "An Invasion of Cheats: The Evolution of Worthless Nuptial Gifts". Current Biology. 15 (1): 64–67. {{cite journal}}: |access-date= requires |url= (help); |format= requires |url= (help); Check date values in: |accessdate= (help); Text "http://www.sciencedirect.com/science/article/pii/S0960982204010218" ignored (help)CS1 maint: multiple names: authors list (link)
  2. ^ Alcock, John. Animal Behavior: An Evolutionary Approach (9th ed.). Retrieved April 25, 2012. p.550
  3. ^ Lack, D. (1940). "Courtship feeding in birds" (PDF). Auk. 57: 169–178.
  4. ^ Logue, DM (2007). "A Greater Ani (Crotophaga major) gives a nuptial gift while copulating" (PDF). Ornitologia Neotropical. 18: 311–312.
  5. ^ a b Gwynee, Darry T (2008). "Sexual Conflict over Nuptial Gifts in Insects" (PDF). Annual Review of Entomology. 53: 83–101. doi:10.1146/annurev.ento.53.103106.093423.
  6. ^ LeBas, NR; Hockham LR (2005). "An Invasion of Cheats: The Evolution of Worthless Nuptial Gifts Current Biology" (PDF). Current Biology. 15: 64–67. doi:10.1016/j.cub.2004.12.043. {{cite journal}}: Cite has empty unknown parameter: |1= (help)CS1 maint: multiple names: authors list (link)
  7. ^ Vahed, K. (1998). The function of nuptial feeding in insects: A review of empirical studies. Biol. Rev. 73, 43–78.
  8. ^ a b Lewis, S.; South, A.; Burns, R.; Al-Wathiqui, N. (2011). "Nuptial gifts" (PDF). Current Biology. 21 (17): R644–R645. doi:10.1016/j.cub.2011.05.046. PMID 21920290.
  9. ^ Hansen, Line Spinner; Gonzáles, Sofia Fernández; Toft, Søren; Bilde, Trine (2008). "Thanatosis as an adaptive male mating strategy in the nuptial gift–giving spider Pisaura mirabilis". Behavioral Ecology. 19 (3): 546–551. doi:10.1093/beheco/arm165.
  10. ^ Stevens, Jeffrey R. ; and Gilby, Ian C. (2004). "A conceptual framework for nonkin food sharing: timing and currency of benefits" (PDF). Animal Behaviour. 64 (4): 603–614. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)
  11. ^ Lack, David (April 1940). "Courtship Feeding in Birds". The Auk. 57 (2): 169–178. JSTOR 4078744.
  12. ^ Stålhandske , Pia (2001). "Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection". Behavioral Ecology. 12 (6): 691–697. {{cite journal}}: |access-date= requires |url= (help); |format= requires |url= (help); Check date values in: |accessdate= (help); Unknown parameter |http://beheco.oxfordjournals.org/content/12/6/691.full?sid= ignored (help)
  13. ^ a b c d Albo et al.: Worthless donations: male deception and female counter play in a nuptial gift-giving spider. BMC Evolutionary Biology 2011 11:329.Submit
  14. ^ Albo et al.: Worthless donations: male deception and female counter play in a nuptial gift-giving spider. BMC Evolutionary Biology 2011 11:329. Submit
  15. ^ Tryjanowski,Piotr; and Hromada , Martin (2005). "Do males of the great grey shrike, Lanius excubitor, trade food for extrapair copulations?" (PDF). Animal Behaviour. 69 (3): 529–533. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)
  16. ^ Kruger, Daniel J. (2008). "Young Adults Attempt Exchanges in Reproductively Relevant Currencies" (PDF). Evolutionary Psychology. 6 (1): 204–212. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)
  17. ^ Buunk, Abraham P. ; and Massar, Karlijn . (2012). "Intrasexual competition among males: Competitive towards men, prosocial towards women" (PDF). Personality and Individual Differences. 52 (7): 818–821. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)
  18. ^ Gordon, Darcy G.; and Gershman, Susan N. ; and Sakaluk, Scott K. (2012). "Glycine in nuptial food gifts of decorated crickets decreases female sexual receptivity when ingested, but not when injected" (PDF). Animal Behaviour. 83 (2): 369–375. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)
  19. ^ Zagrobelny, Mika; and Birger, Lindberg Møller (2011). "Cyanogenic glucosides in the biological warfare between plants and insects: The Burnet moth-Birdsfoot trefoil model system" (PDF). Animal Behaviour. 72 (13): 1585–1592. Retrieved May 03,2012. {{cite journal}}: Check |url= value (help); Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)
  20. ^ Ivy, Tracie M.; and Gershman, ; and Sakaluk, Scott K. (2007). "Sequential mate choice in decorated crickets: females use a fixed internal threshold in pre- and postcopulatory choice" (PDF). Phytochemistry. 74 (4): 1065–1072. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)
  21. ^ Engqvist, Leif (2009). "Should I stay or should I go? Condition- and status-dependent courtship decisions in the scorpionfly Panorpa cognata" (PDF). Animal Behaviour. 78 (2): 491–497. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)
  22. ^ Wedell, Nina (1993). "Spermatophore size in bushcrickets: Comparative evidence for nuptial gifts as a sperm protection device" (PDF). Evolution. 47 (4): 1203–1212. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)
  23. ^ Albo, María J. ; and Cpsta, Fernando G. (2010). "Nuptial gift-giving behaviour and male mating effort in the Neotropical spider Paratrechalea ornata (Trechaleidae)" (PDF). Animal Behaviour. 79 (5): 1031–1036. Retrieved April 29,2012. {{cite journal}}: Check date values in: |accessdate= (help)CS1 maint: multiple names: authors list (link)