Parthenogenesis in amphibians

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Parthenogenesis is a form of reproduction where eggs develop without fertilization, resulting in unisexual species. This phenomenon is closely related with reproductive modes such as hybridogenesis, where fertilization occurs, but the paternal DNA is not passed on. Among amphibians, it is seen in numerous frog and salamander species, but has not been recorded in caecilians.

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Artificial parthenogenesis

Pelophylax nigromaculatus has been used in artificial parthenogenesis experiments Rana rugosa by OpenCage.jpg
Pelophylax nigromaculatus has been used in artificial parthenogenesis experiments

Haploid parthenogenesis has been achieved experimentally in amphibians, through approaches that could be considered artificial gynogenesis. Oscar Hertwig first achieved artificial parthenogenesis in frogs in 1911, using eggs fertilized by irradiated sperm. [1] The radiation destroyed the DNA within the sperm, but nearly normal embryos were still produced. Gunther Hertwig repeated this experiment in 1924, using crosses between different frogs. [1] A cross between a toad, Amietophrynus regularis , and a frog, Rana fusca , would not produce a viable embryo, but fertilization of a toad egg by an irradiated frog sperm would produce a haploid larva. [1] Parthenogenesis has also been induced in Pelophylax nigromaculatus by pricking an egg with a needle. [2] This method produced tadpoles which metamorphosed into adult frogs, some of which were albino. [2] Rana japonica , Pelophylax nigromaculatus and Lithobates pipiens have all produced viable haploid adults as a result of artificial parthenogenesis. [1]

Parthenogenesis in nature

Origins

Salamanders are the oldest known parthenogenic vertebrates. [3] Molecular methods date the origins of unisexual salamanders to the Pliocene, from between 3.9 million [4] to approximately 5 million years ago. [5]

All known parthenogenic amphibians have been the result of hybridization events between closely related species. [6] Pelophylax esculentus , the edible frog, is the product of crosses between Pelophylax lessonae and Pelophylax ridibundus . [7] Similarly, Ambystoma laterale , Ambystoma jeffersonianum , Ambystoma texanum and Ambystoma tigrinum have been identified as extant parent species to unisexual salamanders within the same genus. [4] However, mitochondrial evidence suggests that the origins of hybrid Ambystoma , on the maternal line, lie in a relative of Ambystoma barbouri . [5] [7] In spite of this, all extant unisexual species of Ambystoma share no nuclear DNA with Ambystoma barbouri. [5]

Polyploidy in unisexual amphibians

Polyploidy, a numerical change in the number of chromosomes, is common in parthenogenic amphibians. Triploidy (having three sets of chromosomes), tetraploidy (four sets of chromosomes) and pentaploidy (five sets of chromosomes) are common in salamanders. [4] In unisexual salamanders these different levels of polyploidy are a result of multiple hybridization events, involving two to four species. [4] [8] Ambystoma nothagenes is a unisexual, triploid hybrid of Ambystoma laterale , Ambystoma texanum and Ambystoma tigrinum , while hybrids of Ambystoma platineum and Ambystoma texanum have been found to be tetraploid. [9] Most Ambystoma hybrids are described by how many haploid sets of chromosomes they contain from each of their parent species, reflecting their level of ploidy. [4]

Mortality

Embryonic mortality in parthenogenic amphibians is high. Hatching rates for North American salamander species have ranged from 19.5% [10] to 30.5%. [11] It is speculated that intergenomic exchanges, like crossing over during meiosis, may play a role. Intergenomic exchanges are often lethal due to the fact that chromosomes in unisexual species are homeologous (similar, but less so than homologous chromosomes from within a species). [3] Homologous chromosomes are largely identical, in this case as a result of the chromosome replication. [3]

Modes of parthenogenesis and parthenogenetic-like reproduction in amphibians

Gynogenesis

Gynogenesis is a form of parthenogenesis where an egg begins to divide only after being pricked by a sperm cell, but without the genetic material of the sperm being used. [8] There are two known mechanisms of gynogenesis. The first is an endomitotic event prior to meiosis, where the number of chromosomes in a cell doubles without cell division taking place. [3] After meiosis each egg has the same ploidy (number of chromosomes) as the mother. This particular parthenogentic mechanism has been observed in unisexual Ambystoma species [8] as well as Glandirana rugosa . [12] The second potential mechanism is apomixis, which produces a complete set of chromosomes through mitotic replication. [8] This method has not been observed in any amphibious species. [8] Courtship behavior between females of the same species has been observed in Ambystoma platineum , and has been posited to induce either oviposition of ovulation, though the precise utility of the behavior is unknown. [13]

Mole salamander

Unisexual female mole salamanders of the genus Ambystoma are frequent in the region of the North American Great Lakes. [14] These salamanders emerged about 5 million years ago and are the oldest known unisexual vertebrate lineage. [15] The unisexual female Ambystoma can sometimes undergo genome exchange with males from sympatric sexual species. [15]

Hybridogenesis

In hybridogenesis, females of a unisexual species mate with a male of a related species and utilize their genetic material in order to produce offspring. However, in spite of this requirement, the genetic material of the male is not passed on to the next generation. [8] Just prior to meiosis, during mitotic division, spindle fibers attach to the maternal chromosomes, leaving the paternal chromosomes in the cytoplasm. [16] The paternal chromosomes are therefore excluded from nascent eggs, without recombination having typically occurred. [8] In some cases, such as Pelophylax esculentus, there is also endomeiosis prior to cell division, which means that the maternal chromosomes are duplicated and each egg contains identical pairs of chromosomes. [8] Hybridogenesis can be described as a parthenogenetic-like mode of reproduction, since there is no continuing heredity in the paternal line . [8] It has been documented in the European water frog complex of the genus Pelophylax , which includes three hybridogenic forms.

Kleptogenesis

Kleptogenesis is a sexually parasitic form of reproduction in unisexual organisms, that is often associated with species that are also capable of gynogenetic reproduction. [8] In this reproductive mode unisexual females mate with sympatric males of related species, and genetic material in the paternal line recombines with the maternal DNA and thus is passed on. This mode of reproduction can be seen in numerous, though not all, species of unisexual salamander, particularly salamanders in the genus Ambystoma, [3] and is implicated in the exceptional genetic diversity that exists in those animals. [7]

Related Research Articles

<span class="mw-page-title-main">Asexual reproduction</span> Reproduction without a sexual process

Asexual reproduction is a type of reproduction that does not involve the fusion of gametes or change in the number of chromosomes. The offspring that arise by asexual reproduction from either unicellular or multicellular organisms inherit the full set of genes of their single parent and thus the newly created individual is genetically and physically similar to the parent or an exact clone of the parent. Asexual reproduction is the primary form of reproduction for single-celled organisms such as archaea and bacteria. Many eukaryotic organisms including plants, animals, and fungi can also reproduce asexually. In vertebrates, the most common form of asexual reproduction is parthenogenesis, which is typically used as an alternative to sexual reproduction in times when reproductive opportunities are limited. Komodo dragons and some monitor lizards can reproduce asexually.

<span class="mw-page-title-main">Meiosis</span> Cell division producing haploid gametes

Meiosis (; from Ancient Greek μείωσις 'lessening', is a special type of cell division of germ cells in sexually-reproducing organisms that produces the gametes, the sperm or egg cells. It involves two rounds of division that ultimately result in four cells, each with only one copy of each chromosome. Additionally, prior to the division, genetic material from the paternal and maternal copies of each chromosome is crossed over, creating new combinations of code on each chromosome. Later on, during fertilisation, the haploid cells produced by meiosis from a male and a female will fuse to create a zygote, a cell with two copies of each chromosome again.

<span class="mw-page-title-main">Reproduction</span> Biological process by which new organisms are generated from one or more parent organisms

Reproduction is the biological process by which new individual organisms – "offspring" – are produced from their "parent" or parents. There are two forms of reproduction: asexual and sexual.

<span class="mw-page-title-main">Vertebrate</span> Subphylum of chordates with backbones

Vertebrates are deuterostomal animals with bony or cartilaginous axial endoskeleton — known as the vertebral column, spine or backbone — around and along the spinal cord, including all fish, amphibians, reptiles, birds and mammals. The vertebrates consist of all the taxa within the subphylum Vertebrata and represent the overwhelming majority of the phylum Chordata, with currently about 69,963 species described.

<span class="mw-page-title-main">Fertilisation</span> Union of gametes of opposite sexes during the process of sexual reproduction to form a zygote

Fertilisation or fertilization, also known as generative fertilisation, syngamy and impregnation, is the fusion of gametes to give rise to a zygote and initiate its development into a new individual organism or offspring. While processes such as insemination or pollination, which happen before the fusion of gametes, are also sometimes informally referred to as fertilisation, these are technically separate processes. The cycle of fertilisation and development of new individuals is called sexual reproduction. During double fertilisation in angiosperms, the haploid male gamete combines with two haploid polar nuclei to form a triploid primary endosperm nucleus by the process of vegetative fertilisation.

<span class="mw-page-title-main">Apomixis</span> Replacement of the normal sexual reproduction by asexual reproduction, without fertilization

In botany, apomixis is asexual development of seed or embryo without fertilization. However, other definitions include replacement of the seed by a plantlet or replacement of the flower by bulbils.

<span class="mw-page-title-main">Mole salamander</span> Genus of amphibians

The mole salamanders are a group of advanced salamanders endemic to North America. The group has become famous due to the presence of the axolotl, widely used in research due to its paedomorphosis, and the tiger salamander which is the official amphibian of many US states, and often sold as a pet.

<span class="mw-page-title-main">Edible frog</span> Species of amphibian

The edible frog is a species of common European frog, also known as the common water frog or green frog.

<span class="mw-page-title-main">Karyogamy</span> Fusion of the nuclei of two haploid eukaryotic cells

Karyogamy is the final step in the process of fusing together two haploid eukaryotic cells, and refers specifically to the fusion of the two nuclei. Before karyogamy, each haploid cell has one complete copy of the organism's genome. In order for karyogamy to occur, the cell membrane and cytoplasm of each cell must fuse with the other in a process known as plasmogamy. Once within the joined cell membrane, the nuclei are referred to as pronuclei. Once the cell membranes, cytoplasm, and pronuclei fuse, the resulting single cell is diploid, containing two copies of the genome. This diploid cell, called a zygote or zygospore can then enter meiosis, or continue to divide by mitosis. Mammalian fertilization uses a comparable process to combine haploid sperm and egg cells (gametes) to create a diploid fertilized egg.

<span class="mw-page-title-main">Blue-spotted salamander</span> Species of amphibian

The blue-spotted salamander is a mole salamander native to the Great Lakes states and northeastern United States, and parts of Ontario and Quebec in Canada. Their range is known to extend to James Bay to the north, and southeastern Manitoba to the west.

<span class="mw-page-title-main">Fish reproduction</span> Reproductive physiology of fishes

Fish reproductive organs include testes and ovaries. In most species, gonads are paired organs of similar size, which can be partially or totally fused. There may also be a range of secondary organs that increase reproductive fitness. The genital papilla is a small, fleshy tube behind the anus in some fishes, from which the sperm or eggs are released; the sex of a fish can often be determined by the shape of its papilla.

<span class="mw-page-title-main">Thelytoky</span> Type of parthenogenesis in which females are produced from unfertilized eggs

Thelytoky is a type of parthenogenesis and is the absence of mating and subsequent production of all female diploid offspring as for example in aphids. Thelytokous parthenogenesis is rare among animals and reported in about 1,500 species, about 1 in 1000 of described animal species, according to a 1984 study. It is more common in invertebrates, like arthropods, but it can occur in vertebrates, including salamanders, fish, and reptiles such as some whiptail lizards.

<span class="mw-page-title-main">Polar body</span> Byproduct of oogenesis

A polar body is a small haploid cell that is formed at the same time as an egg cell during oogenesis, but generally does not have the ability to be fertilized. It is named from its polar position in the egg.

<span class="mw-page-title-main">Parthenogenesis</span> Asexual reproduction without fertilization

Parthenogenesis is a natural form of asexual reproduction in which growth and development of an embryo occur directly from an egg, without need for fertilization. In animals, parthenogenesis means development of an embryo from an unfertilized egg cell. In plants, parthenogenesis is a component process of apomixis. In algae, parthenogenesis can mean the development of an embryo from either an individual sperm or an individual egg.

<span class="mw-page-title-main">Sexual reproduction</span> Biological process

Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete with a single set of chromosomes combines with another gamete to produce a zygote that develops into an organism composed of cells with two sets of chromosomes (diploid). This is typical in animals, though the number of chromosome sets and how that number changes in sexual reproduction varies, especially among plants, fungi, and other eukaryotes.

<span class="mw-page-title-main">Klepton</span> Species that requires input from another biological taxon to complete its reproductive cycle

In biology, a klepton and synklepton is a species that requires input from another biological taxon to complete its reproductive cycle. Specific types of kleptons are zygokleptons, which reproduce by zygogenesis; gynokleptons which reproduce by gynogenesis, and tychokleptons, which reproduce by a combination of both systems.

Parthenogenesis is a mode of asexual reproduction in which offspring are produced by females without the genetic contribution of a male. Among all the sexual vertebrates, the only examples of true parthenogenesis, in which all-female populations reproduce without the involvement of males, are found in squamate reptiles. There are about 50 species of lizard and 1 species of snake that reproduce solely through parthenogenesis. It is unknown how many sexually reproducing species are also capable of parthenogenesis in the absence of males, but recent research has revealed that this ability is widespread among squamates.

<span class="mw-page-title-main">Hybridogenesis in water frogs</span>

The fertile hybrids of European water frogs reproduce by hybridogenesis (hemiclonally). This means that during gametogenesis, they discard the genome of one of the parental species and produce gametes of the other parental species. The first parental genome is restored by fertilization of these gametes with gametes from the first species. In all-hybrid populations of the edible frog Pelophylax kl. esculentus, however, triploid hybrids provide this missing genome.

Gynogenesis, a form of parthenogenesis, is a system of asexual reproduction that requires the presence of sperm without the actual contribution of its DNA for completion. The paternal DNA dissolves or is destroyed before it can fuse with the egg. The egg cell of the organism is able to develop, unfertilized, into an adult using only maternal genetic material. Gynogenesis is often termed "sperm parasitism" in reference to the somewhat pointless role of male gametes. Gynogenetic species, "gynogens" for short, are unisexual, meaning they must mate with males from a closely related bisexual species that normally reproduces sexually.

Androgenesis 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, 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 offspring produced in androgenesis will still have maternally inherited mitochondria, as is the case with most sexually reproducing species.

References

  1. 1 2 3 4 Mittwoch, Ursula (1972). "Parthenogenesis". Journal of Medical Genetics. 15 (3): 165–181. doi:10.1136/jmg.15.3.165. PMC   1013674 . PMID   353283.
  2. 1 2 Tokunaga, Chiyoko (1949). "Albino frogs produced by artificial parthenogenesis". The Journal of Heredity. 40 (10): 279–281. doi:10.1093/oxfordjournals.jhered.a105958. PMID   15393921.
  3. 1 2 3 4 5 Bi, Ke; Bogart, J.P. (2010). "Probing the meitotic mechanism of intergenomic exchanges by genomic in situ hybridization of lampbrush chromosomes in Ambystoma (Amphibia: Caudata)". Chromosome Research. 18 (3): 371–382. doi:10.1007/s10577-010-9121-3. PMID   20358399.
  4. 1 2 3 4 5 Hedges, S; Bogart, J.P.; Maxson, L.R. (1992). "Ancestry of unisexual salamanders". Nature. 356 (6371): 708–710. Bibcode:1992Natur.356..708H. doi:10.1038/356708a0. PMID   1570014.
  5. 1 2 3 Bi, K.; Bogart, J.P. (2010). "Time and again: Unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates". BMC Evolutionary Biology. 10: 238. Bibcode:2010BMCEE..10..238B. doi: 10.1186/1471-2148-10-238 . PMC   3020632 . PMID   20682056.
  6. ↑ Neaves, W.B.; Brandon, R.A. (2011). "Unisexual reproduction among vertebrates". Trends in Genetics. 27 (3): 81–88. doi:10.1016/j.tig.2010.12.002. PMID   21334090.
  7. 1 2 3 Graf, J.D.; Pelaz, M.P. (1989). "Evolution and Genetics of Unisexual Vertebrates". In Dawley, R.M.; Bogart, J.P. (eds.). Evolutionary Genetics of the Rana esculenta complex. New York: New York State Museum.
  8. 1 2 3 4 5 6 7 8 9 10 Avise, John (2008). "Reproduction in the semichaste: Gynogenesis, hybridogenesis and kleptogenesis". Clonality: The Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals. Oxford: Oxford University Press. pp. 81–118. ISBN   978-0-19-536967-0.
  9. ↑ Bogart, J.P.; Lichts, L.E. (1986). "Reproduction and the origin of polyploids in hybrid salamanders of the genus Ambystoma". Canadian Journal of Genetics and Cytology. 28 (4): 605–617. doi:10.1139/g86-089. PMID   3756609.
  10. ↑ Bogart, J.P.; Lowcock, L.A.; Zeyl, C.W.; Mable, B.K. (1987). "Genome constitution and reproductive biology of hybrid salamanders, genus Ambystoma, on Kelleys Island in Lake Erie". Canadian Journal of Zoology. 65 (9): 2188–2201. doi:10.1139/z87-333.
  11. ↑ Bogart, J.P.; Bartoszek, J.; Noble, D.W.A.; Bi, K. (2009). "Sex in unisexual salamanders: Discovery of a new sperm donor with ancient affinities". Heredity. 103 (6): 483–493. doi: 10.1038/hdy.2009.83 . PMID   19639004.
  12. ↑ Ichikawa, Y; Miura, I.; Ohtani, H. (1997). "Early gonadal development of the genetic ZZ males and XX females produced by gynogenesis in Rana rugosa". Zoological Science. 14: 73.
  13. ↑ Morris, M.A.; Brandon, R.A. (1984). "Gynogenesis and hybridization between Ambystoma platineum and Ambystoma texanum in Illinois". Copeia. 1984 (2): 324–337. doi:10.2307/1445188. JSTOR   1445188.
  14. ↑ Bogart JP, Bi K, Fu J, Noble DW, Niedzwiecki J (February 2007). "Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes". Genome. 50 (2): 119–36. doi:10.1139/g06-152. PMID   17546077.
  15. 1 2 Gibbs HL, Denton RD (June 2016). "Cryptic sex? Estimates of genome exchange in unisexual mole salamanders (Ambystoma sp.)". Mol Ecol. 25 (12): 2805–15. doi:10.1111/mec.13662. PMID   27100619.
  16. ↑ Cimino, M.C. (1972). "Meiosis in triploid all-female fish (Poeciliopsis, Poeciliidae)". Science. 175 (4029): 1484–1486. Bibcode:1972Sci...175.1484C. doi:10.1126/science.175.4029.1484. PMID   5013682.
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