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Androgenesis

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Androgenesis is a system of asexual reproduction that requires the presence of eggs and occurs when a zygote is produced with only paternal nuclear genes. During standard sexual reproduction, one female and one male parent each produce haploid gametes (such as a sperm or egg cell, each containing only a single set of chromosomes), which recombine to create offspring with genetic material from both parents. However, in androgenesis, there is no recombination of maternal and paternal chromosomes, and only the paternal chromosomes are passed down to the offspring (the inverse of this is gynogenesis, where only the maternal chromosomes are inherited, which is more common than androgenesis).[1] The offspring produced in androgenesis will still have maternally inherited mitochondria, as is the case with most sexually reproducing species.

One of two things can occur to produce offspring with exclusively paternal genetic material: the maternal nuclear genome can be eliminated from the zygote, or the female can produce an egg with no nucleus, resulting in an embryo developing with only the genome of the male gamete.

Androgenesis blurs the lines between sexual and asexual reproduction–it is not strictly a form of asexual reproduction because both male and female gametes are required. However, it is not strictly a form of sexual reproduction because the offspring have uniparental nuclear DNA that has not undergone recombination, and the proliferation of androgenesis can lead to exclusively asexually reproducting species.[1]

Androgenesis occurs in nature in many organisms. like plants,[2] invertebrates (for example, clams,[3] stick insects,[4] some ants,[5] bees,[2] flies[6] and parasitic wasps[2]) and vertebrates (mainly amphibians[7] and fish[2][8]). The Androgenesis has been observed in roosters[9][10] and genetically modified laboratory mice.[11]

Elimination of the maternal nuclear genome

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When androgenesis occurs via elimination of the maternal nuclear genome, the elimination takes place after fertilisation. The nuclei of the two gametes fuse as normal, but immediately afterwards the male nuclear genome then eliminates the female nuclear genome, leaving a fertilized ovum with only the nuclear genome of the male parent. If viable, the resulting offspring is a clone or sub-clone of the sperm or pollen parent.[12]

Elimination of the maternal nuclear genome is evolutionarily advantageous for the male parent, because all offspring produced have the entirely paternally-inherited alleles: in contrast, a male parent that reproduces sexually without androgenesis only passes down half its genetic material to each of its offspring. A male allele promoting the elimination of the female gametic nucleus therefore has a high fitness advantage and can spread through a population and even reach fixation.[12] However, this may be part of the reason androgenesis is very rarely observed in nature: despite being advantageous to the individual producing offspring, it is deleterious to the population as a whole: if an androgenesis-inducing allele reaches high frequencies, egg-producing individuals become rare. Because both egg- and sperm-producers are necessary for androgenesis, if the sex ratio becomes highly unbalanced and there are too few egg-producers, the population is driven to extinction.[12] However, in hermaphrodites (species where a single individual produces both male and female gametes), this is less of a problem since there is no sex ratio.

Female production of a non-nuclear egg

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Androgenesis can also occur through female production of an egg without a nucleus. Upon fertilization with pollen or sperm, there is no maternal nucleus to expel, and a zygote is produced that derives its nuclear genome entirely from its paternal parent. It is unclear why production of non-nucleate eggs would have evolved, because there is no fitness advantage to the egg parent: none of its nuclear genes are being passed onto its offspring. Therefore, any female allele causing non-nucleate egg production would be highly disadvantageous. This form of androgenesis could spread through genetic drift, or if there is some unknown benefit to the egg parent. Species in which non-nucleate egg production occurs are less likely to go extinct than species where the maternal nuclear genome is eliminated. This is because females producing non-nucleate eggs are disfavored by natural selection, so their proportion in a population will remain low.[12]

Male apomixis

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Other type of androgenesis is the male apomixis or paternal apomixis is a reproductive process in which a plant develops from a sperm cell (male gamete) without the participation of a female cell (ovum). In this process, the zygote is formed solely with genetic material from the father, resulting in offspring genetically identical to the male organism.[13][14][15] This has been noted in many plants like Nicotiana, Capsicum frutescens, Cicer arietinum, Poa arachnifera, Cupressus sempervirens, Solanum verrucosum, Phaeophyceae,[16] Pripsacum dactyloides, Zea mays,[2] and occurs as the regular reproductive method in Cupressus dupreziana.[13] This contrasts with the more common apomixis, where development occurs without fertilization, but with genetic material only from the mother.

There are also clonal species that reproduce through vegetative reproduction like Lomatia tasmanica,[17] Lagarostrobos franklinii,[17] Elodea canadensis[18] and Pando,[19] where the genetic material is exclusively male.

Obligate androgenesis

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Although the most common term to refer to totally asexual reproduction in males is Paternal Apomixis, the term Obligated Androgenesis is more used in animals.

Obligate androgenesis is the process in which males are able to produce offspring exclusively through male genetic material, where mating with females of related species is not necessary to produce offspring, which leads to these species being able to survive in the absence of females. They are also capable of interbreeding with sexual and other androgenetic lineages in a phenomenon known as "egg parasitism." This method of reproduction is relatively rare as it has been found in several species of clams of the genus Corbicula[3] and recently in the all male fish specie Squalius alburnoides.[8][20]

Ploidy in androgenesis

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Individuals produced through androgenesis can be either haploid or diploid (having one or two sets of chromosomes, respectively), depending on the species. Diploidy occurs through either the fusion of two haploid sperm cells or the duplication of chromosomes from one haploid sperm cell. In both cases the offspring experience a loss of genetic variation: individuals with the genome of 2 fused sperm cells will suffer from inbreeding depression, and individuals with the genome of a duplicated sperm will be fully homozygous. In species with male heterogamety (males have XY or XO chromosomes and females have XX, like in most mammals), the doubling of male chromosomes will cause all offspring to be female: if the sperm carries an X chromosome, the embryo must be XX, and if it carries a Y or O, the embryo will be YY or OO, and unviable. With sperm fusion, a quarter of fertilized eggs will be female (XX), half will be male (XO or XY), and a quarter will be non-viable (YY or OO).[12]

Androgenesis is more common in haplo-diploid species, a species where sex is determined by ploidy, males generally develop from an unfertilized egg and females from a fertilized egg, than in diploid species (where all sexes are diploid). This is because with haplo-diploids, there is no requirement of the doubling of chromosomes from a haploid gamete, so that no embryos are lost due to YY or OO chromosomes.[12]

Androgenesis in non-gonochoristic species

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Androgenesis is more likely to persist in hermaphrodites than in species with two distinct sexes (gonochorists) because all individuals have the ability to produce ovum, so the spread of androgenesis-promoting alleles causing egg-producers to become scarce is not an issue. Androgenesis is also seen more frequently in species that already have uncommon modes of reproduction such as hybridogenesis and parthenogenesis, and is sometimes seen in interspecies hybridization.[12]

Induced androgenesis

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Humans sometimes induce androgenesis to create clonal lines in plants (specifically crops), fish, and silkworms. A common method of inducing androgenesis is through irradiation. The egg cells can have their nuclei inactivated by gamma ray, UV, or X-ray radiation before being fertilized with sperm or pollen. A 2015 study was successful in producing zebrafish adrogenones by cold-shocking just fertilized eggs, which prevents the first cleavage event that doubles the chromosome number after parthenogenesis, and then heat-shocking them to double their chromosome number.[21]

See also

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References

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  1. ^ a b Pigneur, L.-M.; Hedtke, S. M.; Etoundi, E.; Van Doninck, K. (2012). "Androgenesis: a review through the study of the selfish shellfish Corbicula spp". Heredity. 108 (6): 581–591. doi:10.1038/hdy.2012.3. ISSN 1365-2540. PMC 3356815.
  2. ^ a b c d e Schwander, Tanja; Oldroyd, Benjamin P (28 Sep 2008). "Androgenesis: where males hijack eggs to clone themselves".
  3. ^ a b Hedtke, Shannon M.; Stanger-Hall, Kathrin; Baker, Robert J.; Hillis, David M. (May 2008). "All-Male Asexuality: Origin and Maintenance of Androgenesis in the Asian Clam Corbicula". Evolution. 62 (5): 1119–1136. doi:10.1111/j.1558-5646.2008.00344.x. PMID 18266987.
  4. ^ Tinti, Fausto; Scali, Valerio (November 1992). "Genome exclusion and gametic dapi—dna content in the hybridogenetic Bacillus rossius—grandii benazzii complex (insecta phasmatodea)". Molecular Reproduction and Development. 33 (3): 235–242. doi:10.1002/mrd.1080330302. PMID 1449790.
  5. ^ Fournier, Denis; Estoup, Arnaud; Orivel, Jérôme; Foucaud, Julien; Jourdan, Hervé; Breton, Julien Le; Keller, Laurent (June 2005). "Clonal reproduction by males and females in the little fire ant". Nature. 435 (7046): 1230–1234. doi:10.1038/nature03705. PMID 15988525.
  6. ^ Komma, D J; Endow, S A (5 December 1995). "Haploidy and androgenesis in Drosophila". Proceedings of the National Academy of Sciences. 92 (25): 11884–11888. doi:10.1073/pnas.92.25.11884. PMC 40507. PMID 8524868.
  7. ^ "All-male hybrids of a tetrapod Pelophylax esculentus share its origin and genetics of maintenance". 28 Sep 2024.
  8. ^ a b Matos, I.; Machado, M.P.; Sucena, é.; Collares-Pereira, M.J.; Schartl, M.; Coelho, M.M. (2010). "Evidence for Hermaphroditism in the Squalius alburnoides Allopolyploid Fish Complex". Sexual Development. 4 (3): 170–175. doi:10.1159/000313359.
  9. ^ "Sigue causando asombro el gallo que puso huevos". 12 Nov 2024.
  10. ^ "Rooster who is now laying eggs". 12 Nov 2024.
  11. ^ Ledford, Heidi (2023). "Making mice with two dads: this biologist rewrote the rules on sexual reproduction". Nature. 624 (7992): 499. Bibcode:2023Natur.624..499L. doi:10.1038/d41586-023-03922-6. PMID 38093054.
  12. ^ a b c d e f g Schwander, Tanja; Oldroyd, Benjamin P. (2016-10-19). "Androgenesis: where males hijack eggs to clone themselves". Philosophical Transactions of the Royal Society B: Biological Sciences. 371 (1706): 20150534. doi:10.1098/rstb.2015.0534. ISSN 0962-8436. PMC 5031619. PMID 27619698.
  13. ^ a b Christian Pichot; Benjamin Liens; Juana L. Rivera Nava; Julien B. Bachelier; Mohamed El Maâtaoui (January 2008). "Cypress Surrogate Mother Produces Haploid Progeny From Alien Pollen". Genetics. 178 (1): 379–383. doi:10.1534/genetics.107.080572. PMC 2206086. PMID 18202380.
  14. ^ Christian Pichot; Bruno Fady; Isabelle Hochu (2000). "Lack of mother tree alleles in zymograms of Cupressus dupreziana A. Camus embryos". Annals of Forest Science. 57 (1): 17–22. Bibcode:2000AnFSc..57...17P. doi:10.1051/forest:2000108.
  15. ^ Pichot, C.; El Maataoui, M.; Raddi, S.; Raddi, P. (2001). "Conservation: Surrogate mother for endangered Cupressus". Nature. 412 (6842): 39. doi:10.1038/35083687. PMID 11452293. S2CID 39046191.
  16. ^ Heesch, Svenja; Serrano-Serrano, Martha; Barrera-Redondo, Josué; Luthringer, Rémy; Peters, Akira F; Destombe, Christophe; Cock, J Mark; Valero, Myriam; Roze, Denis; Salamin, Nicolas; Coelho, Susana M (July 2021). "Evolution of life cycles and reproductive traits: Insights from the brown algae". Journal of Evolutionary Biology. 34 (7): 992–1009. doi:10.1111/jeb.13880.
  17. ^ a b "The Oldest Soul". 10 Nov 2024.
  18. ^ "No sex at all? Extremely low genetic diversity in Gagea spathacea (Liliaceae) across Europe". 10 Nov 2024.
  19. ^ DeWoody, Jennifer; Rowe, Carol A.; Hipkins, Valerie D.; Mock, Karen E. (2008). ""Pando" Lives: Molecular Genetic Evidence of a Giant Aspen Clone in Central Utah". Western North American Naturalist. 68 (4): 493–497. doi:10.3398/1527-0904-68.4.493. S2CID 59135424.
  20. ^ FishBase (en inglés)
  21. ^ Hou, Jilun; Fujimoto, Takafumi; Saito, Taiju; Yamaha, Etsuro; Arai, Katsutoshi (2015-08-20). "Generation of clonal zebrafish line by androgenesis without egg irradiation". Scientific Reports. 5 (1): 13346. doi:10.1038/srep13346. ISSN 2045-2322. PMC 4542340.