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Gamergate (ant)

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For other uses, see Gamergate.

Lateral view of an Ophthalmopone berthoudi worker, the ant for which the term gamergate was originally coined[note 1]

A gamergate (/ˈɡæmərˌɡeɪt/ GAMM-ər-gayt) 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 (usually upon the death of the original foundress), 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 (usually with foreign males) 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.

Depending on the species, there can be one gamergate per colony (monogyny) or several gamergates (polygyny). Most gamergate species have colonies with a few hundred or fewer workers.

Etymology

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Gamergate derives from the Greek words γάμος (gámos) and ἐργάτης (ergátēs) and means 'married worker'. It was coined in 1983 by geneticist William Louis Brown[1] and was first used in scientific literature by entomologists Christian Peeters and Robin Crewe in a 1984 paper published in Naturwissenschaften.[2] The definition typically found in entomological dictionaries is 'mated, egg-laying worker',[3][4] and is drawn from the glossary of Bert Hölldobler and E. O. Wilson's 1990 book, The Ants.[3]

Description

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There are 100–200 different species in which gamergates reproduce (roughly 1% of all ants), most of which fall within the poneromorph subfamilies. Whereas workers (which are all females) in most ant species are morphologically incapable of storing sperm, in gamergate species one or several workers mate and have active ovaries.[5] Gamergate lifespan is short compared to queens in queenright colonies, but gamergates can be replaced by other dominant workers in the colony without risking colony survival. Reproductive investment in gamergate females is thus optimized because non-differentiated gamergates (i.e. reproductively inactive workers) function as laborers.[6]

Caste structure

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Dorsal view of a nonreproductive female Diacamma australe worker, lacking anterior thoracic gemmae (buds).

Within gamergate colonies, all workers are born reproductively viable and are thus potential gamergates. Prior to differentiation as a gamergate, a dominant worker must physically inhibit its sisters. For example, in the case of Diacamma australe, the first female to become reproductively active will clip off the thoracic gemmae of her sisters, thus greatly reducing their sexual attractiveness. In other genera, persistent domination of worker females by gamergates via physical aggression all but ensure that they will not produce male offspring.[7] In Diacamma nilgiri, gamergates use dominance interactions to monopolize reproduction without mutilation of sister workers.[8] The same is true for Streblognathus peetersi, which engage in non-injurious aggression to determine dominance.[2] For most gamergate species, the start of ovarian activity eliminates the need to physically dominate nestmate workers. Instead newly produced pheromones or signaling chemicals ensure that workers remain nonreproductive. Although it is unknown to what degree these chemicals act as pheromones or as signals, support for the signaling hypothesis can be found in the loss of reproductive inhibition of workers as the gamergate grows older and her fecundity diminishes.[7]

Mechanisms of gamergate replacement vary among monogynous and polygynous species. When a gamergate dies, it is usually replaced by a formerly submissive worker who proceeds to mate and begins ovarian activity. A new gamergate often originates from a younger cohort. For example, when the original founding queen dies in a Harpegnathos saltator colony, younger workers begin to fight for dominance and some become the next reproductives.[9] Because reproductively inactive workers are able to activate their ovaries after the death of the gamergate, some gamergate species can be considered cooperative breeders rather than truly eusocial insects.[10]

In colonies with both queens and gamergates, the latter function as secondary reproductives.[5] Research on Amblyoponinae species has shown that there is a fecundity-based hierarchy among gamergates. In Stigmatomma reclinatum, it was found that higher-ranked gamergates had more fully developed oocytes than low-ranked gamergates.[11] In Streblognathus peetersi, only the alpha worker mates and becomes the gamergate; younger workers await a chance to reproduce when the current gamergate exhibits decreased fecundity or dies.[2] Challenges to gamergates from subordinate workers are risky because the gamergate in species like Dinoponera quadriceps may mark the challenger by rubbing special chemicals produced only by the gamergate. These chemicals signal to other workers to immobilize the challenger by biting her appendages and immobilizing her for a few days until her hormonal levels return to normal.[12] Subordinate workers play an important policing role in the selection of future gamergates and are thus able to increase their indirect fitness.[5]

Social structure variation and ecology

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There is much variation in the social structure of ant colonies with gamergates. Some species such as Harpegnathos saltator,[13] Pseudoneoponera tridentata, Gnamptogenys menadensis, and Rhytidoponera confusa have a winged alate queen caste as well as gamergates.[14] Queenless species with only gamergates and workers may have a monogynous structure with a single gamergate or they may have a polygynous structure with multiple gamergates. Examples of monogynous queenless species include Pachycondyla krugeri, P. sublaevis, Diacamma australe, D. rugosum, Dinoponera quadriceps, Platythyrea lamellosa, and Streblognathus aethiopicus.[15] Examples of polygynous queenless species include Ophthalmopone berthoudi, O. hottentota,[16] and all known queenless species of Rhytidoponera.[15] In the queenless Ophthalmopone berthoudi, foreign males visit underground nests to mate with young workers.[17]

Ecologically, gamergate species from different tribes and genera often tend to share certain characteristics. Many gamergate species are solitary generalist foragers living in arid environments.[6] Similar to species with ergatoid queens, the evolution of gamergate reproduction is hypothesized to be associated with a shift to colonial fission. Myrmecologists Christian Peeters and Fuminori Ito have also suggested that "the evolution of gamergate reproduction appears strongly associated with the adaptive benefits of secondary polygyny (e.g. increased colony lifespan and resource inheritance), and it is the preferred option in species having workers able to store sperm."[14]

Classification dispute

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The utility of gamergate as a morphological designation is not without critics. Within the field of myrmecology it is a matter of dispute whether caste should be defined primarily by reproductive role or by physical morphology. Notably, Alfred Buschinger has argued that the term worker should be applied only to those ants who make up the non-reproductive caste and queen should be applied only to reproductively viable female ants regardless of their physical appearance. Hölldobler and Wilson suggest that the two positions can be semantically resolved and that the most fruitful approach would be to keep classification "somewhat loose, incorporating either anatomy or roles in a manner that maximizes convenience, precision, and clarity of expression."[18]

Genera with gamergates

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The existence of gamergates is symplesiomorphic, or ancestral, in ants.[19] They are known to be present in the following genera:

See also

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Notes

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  1. ^ In the original Naturwissenschaften paper where the term "gamergate" was first used, O. berthoudi is referred to by the synonym Pachycondyla berthoudi.
  2. ^ Throughout Ito's 1993 paper for the Journal of Natural History, he refers not to Stigmatomma but to Amblyopone. At the time Stigmatomma was considered to be a synonym of Amblyopone.

References

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  1. ^ Peeters, Christian; Crewe, Robin (1984). "Insemination Controls the Reproductive Division of Labour in a Ponerine Ant". Naturwissenschaften. 71 (1): 50–51. Bibcode:1984NW.....71...50P. doi:10.1007/BF00365989. ISSN 0028-1042. S2CID 43871631.
  2. ^ a b c Véron, Géraldine (February 2005). "La reine des fourmis couronnée au combat". Le Journal du CNRS (181): 50–51. ISSN 0994-7647. Archived from the original on 10 February 2005. Retrieved 9 September 2014.
  3. ^ a b Barrows, Edward M. (2011). "Caste – Gamergate". Animal Behavior Desk Reference: A Dictionary of Animal Behavior, Ecology, and Evolution (Third ed.). CRC Press. p. 75. ISBN 9781439836514.
  4. ^ Gordh, Gordon (2011). "Gamergate". A Dictionary of Entomology. CABI. p. 608. ISBN 9781845935429.
  5. ^ a b c Noël, Carine (6 September 2002). "How queenless ants regulate their conflicts" (Press release). Paris: CNRS. Archived from the original on 2 March 2003. Retrieved 10 September 2014.
  6. ^ a b Choe, Jae C.; Crespi, Bernard J. (1997). "Morphologically 'Primitive' Ants". The Evolution of Social Behaviour in Insects and Arachnids. Cambridge University Press. p. 385. ISBN 9780521589772.
  7. ^ a b Bourke, Andrew F. G. (1995). "7 – Kin Conflict: Reproduction (Part 2 – Queen Policing, Queen Control, and Queen Signaling)". Social Evolution in Ants: Monographs in behavior and ecology. Princeton University Press. pp. 239–240. ISBN 9780691044262.
  8. ^ Cournault, Laurent; Peeters, Christian (2012). "Aggression regulates monogyny in non-mutilating Diacamma ants". Insectes Sociaux. 59 (4): 533–539. doi:10.1007/s00040-012-0251-9. S2CID 16179257.
  9. ^ Gorman, James (27 May 2014). "The Ant Queen Is Dead. Let the Battles Begin". The New York Times. ISSN 0362-4331. Retrieved 12 August 2014.
  10. ^ Crespi, Bernard J. (1996). "9 – Comparative Analysis of the Origins and Losses of Eusociality: Causal Mosaics and Historical Uniqueness (Part 6 – Formicidae)". In Martins, Emília P. (ed.). Phylogenies and the Comparative Method in Animal Behavior. Oxford University Press. p. 272. ISBN 9780195092103.
  11. ^ a b Ito, Fuminori (1993). "Social organization in a primitive ponerine ant: queenless reproduction, dominance hierarchy and functional polygyny in Amblyopone sp. (reclinata group) (Hymenoptera: Formicidae: Ponerinae)". Journal of Natural History. 27 (6): 1315–1324. Bibcode:1993JNatH..27.1315I. doi:10.1080/00222939300770751. ISSN 0022-2933.
  12. ^ Monnin, Thibaud; Ratnieks, Francis L. W.; Jones, Graeme R.; Beard, Richard (5 September 2002). "Pretender punishment induced by chemical signalling in a queenless ant" (PDF). Nature. 419 (6902): 61–65. Bibcode:2002Natur.419...61M. doi:10.1038/nature00932. ISSN 0028-0836. PMID 12214231. S2CID 4372841.
  13. ^ Peeters, Christian; Hölldobler, Bert (November 1995). "Reproductive cooperation between queens and their mated workers: The complex life history of an ant with a valuable nest". Proceedings of the National Academy of Sciences of the United States of America. 92 (24): 10977–10979. Bibcode:1995PNAS...9210977P. doi:10.1073/pnas.92.24.10977. ISSN 0027-8424. PMC 40553. PMID 11607589.
  14. ^ a b Peeters, Christian; Ito, Fuminori (2001). "Colony Dispersal and the Evolution of Queen Morphology in Social Hymenoptera". Annual Review of Entomology. 46: 601–30. CiteSeerX 10.1.1.562.7031. doi:10.1146/annurev.ento.46.1.601. ISSN 0066-4170. PMID 11112181.
  15. ^ a b Peeters, Christian P. (1991). Veeresh, G. K.; Mallik, B. (eds.). Social Insects and the Environment: Proceedings of the 11th International Congress of IUSSI, 1990 (International Union for the Study of Social Insects). Brill Academic Pub. p. 234. ISBN 978-9004093164. Retrieved 12 August 2014.
  16. ^ Peetere, C. P.; Crewe, R. M. (1985). "Queenlessness and reproductive differentiation in Ophthalmopone hottentota". South African Journal of Zoology. 20 (4): 268. doi:10.1080/02541858.1985.11447948.
  17. ^ "Species: Pachycondyla berthoudi". antweb.org. AntWeb. Retrieved 12 August 2014.
  18. ^ Hölldobler, Bert; Wilson, E. O. (1990). "Caste and Division of Labor". The Ants. Harvard University Press. pp. 301 & 305. ISBN 9780674040755.
  19. ^ a b Dietemann, V.; Peeters, C; Hölldobler, B. (2004). "Gamergates in the Australian ant subfamily Myrmeciinae". Naturwissenschaften. 91 (9): 432–435. Bibcode:2004NW.....91..432D. doi:10.1007/s00114-004-0549-1. ISSN 0028-1042. PMID 15278223. S2CID 26161972.
  20. ^ Gobin, B.; Peeters, C.; Billen, J. (September 1998). "Production of trophic eggs by virgin workers in the ponerine ant Gnamptogenys menadensis" (PDF). Physiological Entomology. 23 (4): 329–336. doi:10.1046/j.1365-3032.1998.234102.x. S2CID 83569093. Archived from the original (PDF) on 27 August 2016. Retrieved 26 August 2016.
  21. ^ Peeters, Christian P. (1987). "The Reproductive Division of Labour in the Queenless Ponerine Ant Rhytidoponera sp. 12". Insectes Sociaux. 34 (2): 75–86. doi:10.1007/BF02223826. ISSN 0020-1812. S2CID 26116621.
  22. ^ a b c d e f g h i j k Schmidt, C. A; Shattuck, S. O. (2014). "The Higher Classification of the Ant Subfamily Ponerinae (Hymenoptera: Formicidae), with a Review of Ponerine Ecology and Behavior". Zootaxa. 3817 (1): 1–242. doi:10.11646/zootaxa.3817.1.1. PMID 24943802. S2CID 4540972.
  23. ^ "Genus: Diacamma". antweb.org. AntWeb. Retrieved 12 August 2014.
  24. ^ Haskins, Caryl Parker; Zahl, P. A. (1971). "The reproductive pattern of Dinoponera grandis Roger (Hymenoptera, Ponerinae) with notes on the ethology of the species". Psyche: A Journal of Entomology. 78 (1–2): 1–11. doi:10.1155/1971/914147. ISSN 0033-2615.
  25. ^ Peeters, C.; Fisher, B.L. (14 March 2016). "Gamergates (mated egg-laying workers) and queens both reproduce in Euponera sikorae ants from Madagascar" (PDF). African Entomology. 24 (1): 180–187. doi:10.4001/003.024.0180. S2CID 51851380. Retrieved 26 August 2016.
  26. ^ Peeters, Christian; Hölldobler, Bert (2000). "Sexual reproduction by both queens and workers in the ponerine ant Harpegnathos saltator". Insectes Sociaux. 47 (4): 325–332. doi:10.1007/PL00001724. ISSN 0020-1812. S2CID 8728206.
  27. ^ Peeters, Christian; Crewe, Robin M. (1985). "Worker reproduction in the ponerine ant Ophthalmopone berthoudi: an alternative form of eusocial organization". Behavioral Ecology and Sociobiology. 18 (1): 29–37. Bibcode:1985BEcoS..18...29P. doi:10.1007/BF00299235. ISSN 0340-5443. S2CID 20041163.
  28. ^ Schilder, Klaus; Heinze, Jürgen; Hölldobler, Bert (January 1999). "Colony structure and reproduction in the thelytokous parthenogenetic ant Platythyrea punctata (F. Smith) (Hymenoptera, Formicidae)". Insectes Sociaux. 46 (2): 150–158. doi:10.1007/s000400050126. ISSN 0020-1812. S2CID 13729041.
  29. ^ "Genus: Streblognathus". antweb.org. AntWeb. Retrieved 12 August 2014.
  30. ^ Hölldobler, Bert; Liebig, Jürgen; Alpert, Gary (2002). "Gamergates in the myrmicine genus Metapone (Hymenoptera:Formicidae)". Naturwissenschaften. 89 (7): 305–307. Bibcode:2002NW.....89..305H. doi:10.1007/s00114-002-0329-8. PMID 12216860. S2CID 6945541.
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