Polyandry in nature

This article is about polyandry in non-human species. For polyandry in humans, see Polyandry.

In zoology, polyandry is a mating system involving a female and two or more males. Most broadly, polyandry refers to sexual relations with multiple males.

Mating system

The queen bee is usually the only female bee within a hive reproducing with drones, which often come from various hives. She mothers most or all offspring within a given hive.

In the field of behavioural ecology polyandry is a type of breeding adaptation in which one female mates with many males. Another opposite[1] breeding system to this is polygyny in which one male mates with many females (e.g., lions, deer, some primates, and many systems where there is an alpha male).

Polyandry is positively correlated with testicle-to-body weight across taxa (see Sperm competition).[2] Human testicles are lighter than those of chimpanzees—including the highly promiscuous bonobo chimpanzees—but heavier than those of gorillas and orangutans.[3][4]

A common example of polyandrous mating can be found in the Field Cricket Gryllus bimaculatus of the invertebrate order Orthoptera (containing crickets, grasshoppers, and groundhoppers). Females in this species will mate with any male close to them, including siblings. Widely shown in frogs (Agile frogs, Rana dalmatina), polyandry was also documented in polecat (Mustela putorius) and other mustelids.

Many reptile species also demonstrate polyandry, especially among members of the tortoise family (Testudinidae). Through polyandry and long-term sperm storage, recent studies have found evidence for the ability of female tortoises to produce clutches of eggs that demonstrate multiple paternity.[5][6] Predictably, these hatchlings showed an increase in genetic variability compared to those sired by a single male.[6] Potential for multiple paternity within a clutch is primarily a result of sperm storage across reproductive cycles, since studies have confirmed the presence of multiple males’ sperm in the female tortoise reproductive tract simultaneously.[6] As a result of clutches with greater variation in paternal genes and increased sperm competition, females can maximize both the genetic quality and number of offspring.[7] Multiple paternities within a single clutch is therefore considered an effective strategy to increase the reproductive success and fitness of female tortoises.[5]

Some taxa with high social organization are eusocial, meaning that a single female (e.g., the queen bee) or caste produces offspring while the other organisms (e.g., worker bees) cooperate in caring for the young. Examples of mammalian eusociality include Damaraland mole-rats and naked mole-rats,[8][9] among whom polyandry is the norm and polygyny has never been observed.[10] Female mole-rats compete for the status of Queen or “alpha female” (see Naked mole-rat#Queen and gestation).

Commonly in canine[11] and feline[12] reproduction, plural ova are fertilized during the same instance of estrus by various males each, so that a single litter of puppies or kittens may have more than one father. This is called heteropaternal superfecundation; very rare in human reproduction, but is documented. In one study on humans, the frequency was 2.4% among dizygotic twins whose parents were involved in paternity suits.[13]

Many of the theories attempting to explain concealed ovulation in humans and other organisms rely on premises of polyandry.

According to Gordon G. Gallup, human penile shape is indicative of an evolutionary history of polyandry. Male humans evolved to have a wedge- or spoon-shaped glans and to perform repeated thrusting motions during copulation in order to draw foreign semen back away from the cervix and thus to compete with sperm of other males.[14]

Related to sexual conflict, Thierry Lodé[15] found possible evolutionary explanations for polyandry including mate competition and inbreeding avoidance.

Polyandry also occurs in some primates such as marmosets, mammal groups, the marsupial genus' Antechinus and bandicoots, whales,[17][18] around 1% of all bird species, such as jacanas and dunnocks, insects such as honeybees, and fish such as pipefish. Even female camels mate with multiple males.

In New World monkeys

Some New World monkeys, such as Goeldi's Marmoset, have been observed living in polyandrous groups. Although groups may contain more than one female, the dominant female suppresses ovulation in subordinates, causing her to be the only one capable of reproduction. A Goeldi's Marmoset female regularly births more than one offspring, and her eggs are separately fertilized by more than one male. Paternal investment is high among Goeldi's Marmosets, and males often carry infants on their backs even if they are not the father of the infant. It has been suggested that multiple male mates were related, and therefore cooperation in caring for each other's young is adaptive; however, researchers tagged and tracked Goeldi's Marmosets over time, and noticed that unrelated males migrated to new groups to cooperate with nonrelatives as well as with relatives to care for young. It has also been suggested that females select cooperative males, and that the multiple offspring of Goeldi's Marmosets require paternal care for survival.

Current research suggests that polyandry is the dominant social structure in the Callitrichidae subfamily of New World monkeys.

The callitrichidae family includes marmosets and tamarins, two groups of small New World monkeys found in South America. Wild groups usually consist of three to ten individuals, with one reproductively active female, one or more reproductive males, and several nonreproductive helpers that can be either male or female. Interestingly, cooperative polyandry is not the only mating system found in these primates. Polyandrous, monogamous, and polygynous groups can be found within the same population, and a group can even change mating systems, making it the most flexible mating system of any non-human primate.[19] Unlike most primates who typically give birth to single young, twins are the average litter size for tamarins and marmosets. The entire group participates in raising the offspring, sharing the responsibilities of infant carrying, feeding, and grooming. The presence of nonreproductive helpers appears to be the most important factor in determining which mating system is used, as ecological and environmental variability have not been found to have a significant impact. Goldizen (1987) proposed the hypothesis that monogamy in callitrichidae should develop only in groups with nonreproductive helpers to help raise the young, and in the absence of these helpers, both polyandrous males and females would have higher reproductive success than those in lone monogamous pairs. Indeed, in studies of Saguinus fuscicollis, common name saddle-back tamarin, no monogamous lone pairs have ever been seen to attempt a breeding cycle.[20]

Sociobiology

The term has gained some currency in sociobiology, where it refers, analogously, to a mating system in which one female forms more or less permanent bonds to more than one male. It can take two different forms. In one, typified by the Northern Jacana[21] and some other ground-living birds, the female takes on much the same role as the male in a polygynous species, holding a large territory within which several males build nests. Subsequently, the female lays eggs in all the nests, and plays little part in parental care. In the other form, typified by the Galápagos Hawk, a group of two or more males (which may or may not be related) and one female collectively care for a single nest. The latter situation more closely resembles typical human fraternal polyandry.

Although polecats are chiefly polygynous, females can show polyandry, and the sexual conflict aspect of the mating system can change with environmental conditions. Sexual conflict may result in sexually antagonistic co-evolution or “sexual conflict”, in which one sex evolves a “manipulative” character which is countered by a “resistance” trait in the other sex.

These two forms reflect different resource situations: polyandry with shared parental care is more likely in very difficult environments, where the efforts of more than two parents are needed to give a reasonable chance of rearing young successfully.

Honeybees are said to be polyandrous because a queen typically mates with multiple males, even though mating is the only interaction that they have (the males die off, while the queen uses stored sperm for eggs she fertilizes). Utetheisa ornatrix also demonstrate a polyandrous mating system, where females mate with multiple males. On average, females mate with four to five males over their lifespan of three to four weeks but can mate with and receive up to thirteen spermatophores. This allows for increased paternal investment through the content of the spermatophores given to females.[22]

Polyandry in primates, mammals and other animals is usually correlated with reduced or reverse sexual dimorphism—females larger than males. When males of a species are much larger than females, polygyny is usually practiced. As size difference decreases, or the females are larger than males, a species is more likely to practice monogamy or polyandry. The great apes (gorillas, orangutans, chimpanzees, and bonobos) are dimorphic, the greatest disparity occurring in gorillas. Chimpanzees and bonobos have promiscuous societies in which the female mates with multiple males and vice versa. Should only a few females come into estrous, the males of the group will mate with only a few females, creating a fluid form polyandry. However, in chimpanzees, should the alpha male be powerful enough, he will discourage the other males from soliciting a female in estrous and vice versa, effectively establishing a loosely maintained form of polygyny. Chimpanzees and bonobos exhibit slight sexual dimorphism, the latter being matriarchal despite the females' smaller size. Gorillas practice true polygyny with one much larger male travelling with several females and their children. He alone will mate with his female companions. Though orangutans are solitary, it has been found that several females will build their nests within an adult male's territory and will mate more often with this one male than with others, thus demonstrating a form of polygyny. Male and female gibbons (lesser apes) are similar in size and form monogamous pairs. Human males and females are less dimorphic in body size than the other great apes, and engage in polyandry, promiscuity, polygyny, and monogamy, the latter two being the most common.[23][24] Conversely, birds of prey - which show distinct reverse sexual dimorphism—tend to be monogamous for long periods or mate for life; some species like the Snail kite will choose new mates every year, polygyny is noted in many Harriers and polyandry has been observed in the Harris' Hawk (notable for being the only bird of prey to regularly live and hunt in family and social groups[25]) and the aforementioned Galapagos hawk.[26]

Paternal investment is often high in polyandrous species.

See also

References

  1. ↑ Evolutionary anthropology of the human family; In C. A. Salmon and T. K. Shackelford (Eds.), The Oxford Handbook of Evolutionary Family Psychology. New York: Oxford University Press.
  2. ↑ Karim Vahed1, Darren J. Parker, James D. J. Gilbert. "Larger testes are associated with a higher level of polyandry, but a smaller ejaculate volume, across bushcricket species (Tettigoniidae)". Biology Letters. November 10, 2010.
  3. ↑ Harcourt, A.H., Harvey, P.H., Larson, S.G., & Short, R.V. 1981. Testis weight, body weight and breeding system in primates, Nature 293: 55-57
  4. ↑ Shackelford, T. K.; Goetz, A. T. (2007). "Adaptation to Sperm Competition in Humans". Current Directions in Psychological Science 16: 47. doi:10.1111/j.1467-8721.2007.00473.x.
  5. ↑ 5.0 5.1 Johnston, E., Rand, M., and Zweifel, S. 2006. Detection of multiple paternity and sperm storage in a captive colony of the central Asian tortoise, Testudo horsfieldii. Canadian Journal of Zoology 84:520-526.
  6. ↑ 6.0 6.1 6.2 Davy C., Edwards T., Lathrop A., Bratton M., Hagan M., Henen B., Nagy K., Stone J., Hillard L., and Murphy R. 2011. Polyandry and multiple paternities in the threatened Agassiz’s desert tortoise, Gopherus agassizii. Conservation Genetics 12:1313-1322.
  7. ↑ Moon J., McCoy E., Mushinsky H., and Karl S. 2006. Multiple paternity and breeding system in the gopher tortoise, Gopherus polyphemus. The Journal of Heredity 97:150–157.
  8. ↑ Jarvis, Jennifer (May 1981). "Eusociality in a Mammal: Cooperative Breeding in Naked Mole-Rat Colonies". Science 212 (4494): 571–573. doi:10.1126/science.7209555. JSTOR 1686202.
  9. ↑ Burda, H. Honeycutt, R. L, Begall, S., Locker-Grutjen, O & Scharff A. (2000) Are naked and common mole-rats eusocial and if so, why? Behavioral ecology and sociobiology 47(5) 293-303 Abstract
  10. ↑ Bray, TC; Bloomer, P; O'Riain, MJ; Bennett, NC (2012). "'How Attractive Is the Girl Next Door? An Assessment of Spatial Mate Acquisition and Paternity in the Solitary Cape Dune Mole-Rat, Bathyergus suillus". PLoS ONE 7 (6): e39866. doi:10.1371/journal.pone.0039866.
  11. ↑ Coren, Stanley. "Why Are Some Litter Pups Uniform in Appearance While Others Are Mismatched?". Psychology Today. August 29, 2011.
  12. ↑ "Prolific Cats: The Estrous Cycle" (PDF). Veterinary Learning Systems. Retrieved 19 June 2009.
  13. ↑ Wenk RE, Houtz T, Brooks M, Chiafari FA. (1992). "How frequent is heteropaternal superfecundation?". Acta geneticae medicae et gemollologiae 41 (1): 43–7. PMID 1488855.
  14. ↑ Gordon, G. Gallup Jr.; Burch, Rebecca L.; Zappieri, Mary L.; Parvez, Rizwan A.; Stockwell, Malinda L.; Davis, Jennifer A. (2003). "The human penis as a semen displacement device" (PDF). Evolution and Human Behavior 24: 277–289. doi:10.1016/S1090-5138(03)00016-3.
  15. ↑ T Lodé La guerre des sexes chez les animaux, Paris: Eds O. Jacob, 2006, ISBN 2-7381-1901-8 (French)
  16. ↑ Klemme, Ines; Ylönen, Hannu. "Polyandry enhances offspring survival in an infanticidal species". August 12, 2009. doi: 10.1098/rsbl.2009.0500 Biology Letters 23 February 2010 vol. 6 no. 1 24-26
  17. ↑ "Blue Whale". Discovery Channel Blue Ocean.
  18. ↑ "Milk". Modern Marvels. Season 14. 2008-01-07. The History Channel.
  19. ↑ Terborgh, John; Goldizen, Ann Wilson (1985). "On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis)". Behavioral Ecology and Sociobiology 16 (4): 293. doi:10.1007/BF00295541.
  20. ↑ Goldizen, Anne Wilson (1987). "Facultative polyandry and the role of infant-carrying in wild saddle-back tamarins (Saguinus fuscicollis)". Behavioral Ecology and Sociobiology 20 (2): 99. doi:10.1007/BF00572631.
  21. ↑ Jenni, Donald A.; Gerald Collier (1972). "Polyandry in the American Jaçana (Jacana spinosa)". The Auk 89 (4): 743–765. doi:10.2307/4084107.
  22. ↑ Bezzerides, Alexander, and Thomas Eisener. "Apportionment of Nuptial Alkaloidal Gifts by a Multiply-mated Female Moth (Utetheisa Ornatrix): Eggs Individually Receive Alkaloid from More than One Male Source." Chemoecology 12.4 (2002): 213-18. Print.
  23. ↑ de Waal, Frans (1998). Chimpanzee Politics: Power and Sex among Apes. Johns Hopkins University Press, USA.
  24. ↑ Goodall, Jane. (1993). The Chimpanzees of Gombe: Patterns of Behavior. Harvard University Press, USA.
  25. ↑ Cook, William E. (1997). Avian Desert Predators. ISBN 3-540-59262-8.
  26. ↑ "Birds of prey - reproduction". webcitation.org: SeaWorld. Archived from the original on 11 April 2011. Retrieved 11 April 2011.