Hybridogenesis in water frogs

Last updated
in the Danube delta Green frog (Pelophylax esculentus complex) Danube delta.jpg
in the Danube delta

The fertile hybrids of European water frogs (genus Pelophylax) 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 (containing a genome not recombined with the genome of the first parental species). [1] [2] [3] [4] The first parental genome is restored by fertilization of these gametes with gametes from the first species (sexual host). [5] [1] [4] In all-hybrid populations of the edible frog Pelophylax kl. esculentus, however, triploid hybrids provide this missing genome. [3] [6] [2]

Contents

Because half of the genome is transmitted to the next generation clonally (not excluded unrecombined intact genome), and only the other half sexually (recombined genome of the sexual host), the hybridogenesis is a hemiclonal mode of reproduction. [7] [8] [4]

For example, the edible frog Pelophylax kl. esculentus (mostly RL genome), which is a hybridogenetic hybrid of the marsh frog P. ridibundus (RR) and the pool frog P. lessonae (LL), usually excludes the lessonae genome (L) and generates gametes of the P. ridibundus (R). In other words, edible frogs produce gametes of marsh frogs. [2] [3] [4]

The hybrid populations are propagated, however, not by the above primary hybridisations, but predominantly by backcrosses with one of the parental species they coexist (live in sympatry [9] [10] ) with (see below in the middle). [11] [2] [3] [12] [9] [4]

Example crosses between pool frog (Pelophylax lessonae), marsh frog (P. ridibundus) and their hybrid - edible frog (P. kl. esculentus). The first example is the primary hybridization-generating cross. The second one is an example of hybridogenesis and occurs in the most widespread hybridogenetic L-E system, the third example occurs in the R-E system, is less frequent in nature , but is considered as possible e.g., if an L-E system is invaded by P. ridibundus . P. kl. esculentus x P. kl. esculentus crossings result in inviable P. ridibundus tadpoles and are not shown here. Large circles - adult frogs, small circles - gametes, x - lack of gametes containing genome of one of the parental species. Hybridogenesis in water frogs.gif
Example crosses between pool frog (Pelophylax lessonae), marsh frog (P. ridibundus) and their hybrid - edible frog (P. kl. esculentus). The first example is the primary hybridization-generating cross. The second one is an example of hybridogenesis and occurs in the most widespread hybridogenetic L–E system, the third example occurs in the R–E system, is less frequent in nature , but is considered as possible e.g., if an L-E system is invaded by P. ridibundus . P. kl. esculentus × P. kl. esculentus crossings result in inviable P. ridibundus tadpoles and are not shown here. Large circles - adult frogs, small circles - gametes, × - lack of gametes containing genome of one of the parental species.

Since the hybridogenetic hybrids require another taxon as sexual host to reproduce, usually one of the parental species, they are called kleptons [13] [14] [5] (with "kl." in scientific names [15] ).

Edible frog Pelophylax kl. esculentus Rana esculenta on Nymphaea edit.JPG
Edible frog Pelophylax kl. esculentus

There are three known hybridogenetic hybrids of the European water frogs:

Parental genome exclusion

Hybridogenesis implies that gametes of hybrids don't contain mixed parental genomes, as normally occurs by independent chromosome segregation and crossover in meiosis (see also second Mendel's law, recombination). Instead, each gamete carries a complete (haploid) genome of only one parent species. Usually one entire genome of the parental species is excluded prior to meiosis during gametogenesis, such that only one (remaining) parental genome is represented among gametes and genes from the other parent are not passed on by the hybridogen. [16] [3] [2] This discarding occurs gradually during subsequent mitotic divisions, not in one step. [2]

Pelophylax kl. esculentus are a hemiclone here, because they share half of their genome (R haplotype, red arrows). L-E system. Hybridogenesis in water frogs hemiclonal LE.gif
Pelophylax kl. esculentus are a hemiclone here, because they share half of their genome (R haplotype, red arrows). L-E system.
Typical gametogenesis in Pelophylax kl. esculentus (in the L-E system). 1 - exclusion of the P. lessonae genome, 2 - duplication (endoreduplication) of the P. ridibundus genome - restoration of diploidy, 3 - meiosis, L and R - P. lessonae and ridibundus genomes. Pelophylax esculentus - gametogenesis LE.gif
Typical gametogenesis in Pelophylax kl. esculentus (in the L-E system). 1 - exclusion of the P. lessonae genome, 2 - duplication (endoreduplication) of the P. ridibundus genome - restoration of diploidy, 3 - meiosis, L and R - P. lessonae and ridibundus genomes.
Gametes of a hybridogenetic hybrid contain the unrecombined genome of one parental species (C), instead of all possible combinations of both parental (red and green) chromosomes (B). A - somatic cell. Hybridogenesis in water frogs gametes.gif
Gametes of a hybridogenetic hybrid contain the unrecombined genome of one parental species (C), instead of all possible combinations of both parental (red and green) chromosomes (B).
A – somatic cell.

Hemiclones

Hybridogenesis is a hemiclonal mode of reproduction — half of a hybrid genome is transmitted intact clonally from generation to generation (R genome in the L-E system) — not recombined with a parental species genome (L here), while the other half (L) is transmitted sexually — obtained (replaced) each generation by sexual reproduction with a parental species (sexual host [5] [1] [4] , P. lessonae in the L-E system). [7] [8] [4]

Hybridogenetic systems overview

There are at least three hybridogenetic species (hybrids) of water frogs in Europe – edible frog Pelophylax kl. esculentus, Graf's hybrid frog Pelophylax kl. grafi and Italian edible frog Pelophylax kl. hispanicus. Their mating patterns are classified into several hybridogenetic systems: [2]

HybridOriginated fromMaintained by
crosses with		Excluded
genome		System
Pelophylax kl. esculentus
RL		P. ridibundus
RR		×P. lessonae
LL		P. lessonae
LL		LL–E
P. ridibundus
RR		R or L 3:1R–E
P. kl. esculentus
LLR		L from RL
R from LLR		E
P. kl. esculentus
RRL		R or L 3:1 from RL
L from RRL		E
Pelophylax kl. grafi
RP		P. ridibundus ?
RR or
P. kl. esculentus ?
RL		× P. perezi
PP		P. perezi
PP		PP–G
Pelophylax kl. hispanicus
RB		P. ridibundus
RR		×P. bergeri
BB		P. bergeri
BB		BB–H

(capital abbreviations below scientific names are genotypes)

All these hybrids contain genome of marsh frog P. ridibundus (R) and genome of second parental species (L, P or B). [2]

Most of above hybridogenic systems consist of a hybrid coexisting (living in sympatry [9] [10] ) with one of the parental species required for its reproduction. [2] P. kl. esculentus for example in the most frequent L-E system must mate with P. lessonae to produce new hybrids, in the R-E system with P. ridibundus. [3] [4] Because these hybrids depend on other taxa as sexual hosts to reproduce ("parasitize" on them sexually), they are kleptons [13] [14] [5] ("kl." in scientific names [15] ).

Edible frog Pelophylax kl. esculentus

The Pelophylax esculentus complex consists of the hybrid taxon – edible frog P. kl. esculentus (genotype RL) and parental species – marsh frog P. ridibundus (RR) and pool frog P. lessonae (LL). Hybrids are females and males, which is unusual, because hybrids of other hybridogenic species are only females. [2]

The primary hybridisation originating P. kl. esculentus (genotype RL) is:

It occurs between P. lessonae (LL) males and P. ridibundus (RR) females [11] [2] [3] [9] [4] , because smaller P. lessonae males prefer larger females. [11] [2] [3] [4] The lineages of hybrids are maintained later through other matings, described below. [2] [3] [6]

P. lessonae and P. ridibundus have distinct habitat requirements and usually don't live together. [17] [18]

P. lessonae – P. kl. esculentus (L–E) system

The P. lessonae – P. kl. esculentus [2] (L–E [2] [4] [9] [12] [8] , LE [3] [6] , lessonae–esculentus [3] ) system is most widespread hybridogenetic system. [2] [4] It is found in Western Europe. [2]

Hybrids P. kl. esculentus (genotype RL) exclude here the P. lessonae genome (L) and make exclusively clonal P. ridibundus gametes (R). [2] [4] In other words, edible frogs produce gametes of marsh frogs! [4] Their lineages are maintained usually through backcrosses of a female P. kl. esculentus (RL) with a male P. lessonae (LL). The offspring consist of only P. kl. esculentus. [2] [3]

P. kl. esculentus hybrids (RL) can mate also with each other, but only 3% of resulting tadpoles (RR) survive to sexual maturity (97% do not). The genomes of interhybrid crosses are female, because of carrying X chromosomes of females from primary hybridisation. [2]

Hybridogenesis - L-E and R-E systems. Hybridogenesis in water frogs LE RE.gif
Hybridogenesis – L–E and R–E systems.

P. ridibundus – P. kl. esculentus (R–E) system

The P. ridibundus – P. kl. esculentus [2] (R–E [2] [4] , RE [3] [6] , ridibundus–esculentus [3] ) system inhabits Eastern Europe. [2]

It is essentially a reverse form of the L–E system. [2] [3]

Hybrids P. kl. esculentus (genotype RL) exclude here the P. ridibundus (R) or P. lessonae (L) genome in a 3:1 ratio and make mainly clonal P. lessonae (L), less P. ridibundus gametes (R). [2] One frog produce either L or R gametes or a mixture of both. [4] Their lineages are maintained through backcrosses of a male [3] P. kl. esculentus (RL) with a female [3] P. ridibundus (RR). [2] [3] The offspring consist of P. kl. esculentus males (75%) or P. ridibundus females (25%). This is called hybrid-amphispermy. [2]

All-hybrid populations (E system)

All-hybrid populations [3] [2] (E system [2] , EE–system [6] ) consist exclusively of P. kl. esculentus – diploid RE and triploid LLR or RRL hybrids. [3] [2] There are even known tetraploid LLRR hybrids. [3] All-hybrid populations inhabit the entire range of the water frog complex. [3]

RL diploids discard L genome and produce gametes of P. ridibundus (R), or discard R or L genome and produce gametes of P. lessonae (L) or P. ridibundus (R) respectively. In both cases, diploid hybrids generate also not reduced diploid gametes (RL) needed to recreate triploids. [2]

Triploids LLR and RRL are providers of P. lessonae (L) [2] and P. ridibundus gametes (R) respectively in this system lacking both of parental species. [2] So triploid hybrids allow P. kl. esculentus populations to remain without the parental species. [3]

Because triploids discard this genome, which is available in one copy and leave two copies of second genome, they don't perform endoreduplication. [2] Moreover, this not eliminated genome is transmitted to haploid gametes sexually, not clonally (recombined between two L's or between two R's), in contrast to the genome of diploid hybrids. [3] [6]

Such modified hybridogenesis [19] (or gametogenetic system [20] ) occurring in allotriploid hybrids, where during meiosis chromosomes (genomes) from the doubled set (LL from LLR or RR from RRL here) are used to produce haploid gametes (L or R respectively), whereas the remaining ones may be excluded (R from LLR or L from RRL) is known as meiotic hybridogenesis. [19] [20] [6]

In one Slovakian population however, triploid males (LLR) and diploid LR females generate clonal LL and clonal R gametes respectively, instead of recombined L and clonal LR. [6]

P. lessonae (LL) and P. ridibundus (RR) offspring do not survive to sexual maturity in the E system. [2] [3]

Maintenance of pure (all-hybrid) P. kl. esculentus populations, without P. lessonae and ridibundus. [3]

L, R – P. lessonae and P. ridibundus haploid genomes;
LL, RR – do not survive to sexual maturity;
* females only (eggs); ** L gametes are produced by LR, but author doesn't write whether they take part in reproduction or not.

Hybridogenesis - All-hybrid (E) system. Hybridogenesis in water frogs All-hybrid E.gif
Hybridogenesis – All-hybrid (E) system.

Graf's hybrid frog Pelophylax kl. grafi and the P–G system

Hybridogenesis in Graf's hybrid frog Pelophylax kl. grafi (P-G system). Hybridogenesis in water frogs Graf's hybrid frog Pelophylax kl. grafi PG.gif
Hybridogenesis in Graf's hybrid frog Pelophylax kl. grafi (P–G system).

It is not clear, whether the primary hybridisation which originated Graf's hybrid frog Pelophylax kl. grafi (genotype PR) was: [2]

Unlike P. perezi and Pelophylax kl. grafi, P. ridibundus and P. kl. esculentus do not belong to native fauna of Iberian Peninsula. [2]

Hybrids P. kl. grafi (PR) discard the P. perezi genome (P) and make exclusively clonal P. ridibundus gametes (R). Their lineages are maintained in so called P–G system through backcrosses of P. kl. grafi (PR) with P. perezi (PP). [2]

Italian edible frog Pelophylax kl. hispanicus and the B–H system

Hybridogenesis in Italian edible frog Pelophylax kl. hispanicus (B-H system). Hybridogenesis in water frogs Italian edible frog Pelophylax kl. hispanicus B-H.gif
Hybridogenesis in Italian edible frog Pelophylax kl. hispanicus (B–H system).

The primary hybridisation which originated Italian edible frog Pelophylax kl. hispanicus (genotype RB) was: [2]

Hybrids Pelophylax kl. hispanicus (RB) discard the P. bergeri genome (B) and make exclusively clonal P. ridibundus gametes (R). Their lineages are maintained in so called B–H system through backcrosses of P. kl. hispanicus (PR) with P. bergeri (BB). [2]

Water frogs and hybridogenesis definition

Matting patterns of hybridogenetic water frogs don't fit precisely known definitions of hybridogenesis: [21] [1] [7]

Mitochondrial DNA

The Pelophylax kl. esculentus complex frogs have either of four phenotypes of mtDNA: [9]

TaxonmtDNA type
ABCD
marsh frog P. ridibundus++
pool frog P. lessonae++
edible frog P. kl. esculentus++++

Type A is P. ridibundus specific and type B is P. lessonae-like [2] (differs only by 0.3% from type C [9] ). Most of P. kl. esculentus have C or D phenotype of the P. lessonae, not P. ridibundus mtDNA. [9] [2]

Distribution of these phenotypes don't reflect exactly typical matting patterns. Mitochondria along with the mtDNA are inherited exclusively from the female. Since the primary hybridisations producing P. kl. esculentus occur between P. ridibundus females (large) and P. lessonae males (small) and later are maintained through backcrosses P. kl. esculentus females with P. lessonae males (L–E system [2] ), the expected mtDNA phenotype of P. kl. esculentus would be the phenotype of P. ridibundus. This unexpected phenotype distribution might be explained in such a way that most of P. kl. esculentus lineages might go through at least one backcross between P. kl. esculentus male with P. lessonae female. [9] [2] And such phenotype pattern suggests, that primary hybridisations are rare. [9]

The introgression of P. lessonae mtDNA in P. ridibundus (type B [9] ) might be caused by matting between P. ridibundus and P. kl. esculentus having P. lessonae mtDNA. [2]

Evolutionary origin of hybridogenesis in edible frog

During the ice ages,[ clarification needed ] the population of the common ancestor of both parental species of the edible frog was split into two. These populations diverged, but remained genetically close enough to be able to create fertile hybrids. However, when diploid edible frogs mate with each other, their offspring are often malformed, so there are no pure populations of edible frogs unless some triploid individuals are present (the E system described above).

Impact of alien species

Introduction of alien species belonging to water frog complex (Pelophylax esculentus complex), for example, the exotic marsh frog P. ridibundus, may be harmful to native frog populations because of the creation of new hybridisation opportunities and subsequent exclusion of some of genomes from the population. In some cases it was proved. [2] [8] [24]

See also

Related Research Articles

<span class="mw-page-title-main">Ploidy</span> Number of sets of chromosomes in a cell

Ploidy is the number of complete sets of chromosomes in a cell, and hence the number of possible alleles for autosomal and pseudoautosomal genes. Sets of chromosomes refer to the number of maternal and paternal chromosome copies, respectively, in each homologous chromosome pair, which chromosomes naturally exist as. Somatic cells, tissues, and individual organisms can be described according to the number of sets of chromosomes present : monoploid, diploid, triploid, tetraploid, pentaploid, hexaploid, heptaploid or septaploid, etc. The generic term polyploid is often used to describe cells with three or more sets of chromosomes.

<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">Polyploidy</span> Condition where cells of an organism have more than two paired sets of chromosomes

Polyploidy is a condition in which the cells of an organism have more than one pair of (homologous) chromosomes. Most species whose cells have nuclei (eukaryotes) are diploid, meaning they have two complete sets of chromosomes, one from each of two parents; each set contains the same number of chromosomes, and the chromosomes are joined in pairs of homologous chromosomes. However, some organisms are polyploid. Polyploidy is especially common in plants. Most eukaryotes have diploid somatic cells, but produce haploid gametes by meiosis. A monoploid has only one set of chromosomes, and the term is usually only applied to cells or organisms that are normally diploid. Males of bees and other Hymenoptera, for example, are monoploid. Unlike animals, plants and multicellular algae have life cycles with two alternating multicellular generations. The gametophyte generation is haploid, and produces gametes by mitosis; the sporophyte generation is diploid and produces spores by meiosis.

<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">Marsh frog</span> Species of frog

The marsh frog is a species of water frog native to Europe and parts of western Asia.

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

The pool frog is a European frog in the family Ranidae. Its specific name was chosen by the Italian herpetologist Lorenzo Camerano in 1882, in order to honour his master Michele Lessona.

<span class="mw-page-title-main">Hybrid speciation</span> Form of speciation involving hybridization between two different species

Hybrid speciation is a form of speciation where hybridization between two different species leads to a new species, reproductively isolated from the parent species. Previously, reproductive isolation between two species and their parents was thought to be particularly difficult to achieve, and thus hybrid species were thought to be very rare. With DNA analysis becoming more accessible in the 1990s, hybrid speciation has been shown to be a somewhat common phenomenon, particularly in plants. In botanical nomenclature, a hybrid species is also called a nothospecies. Hybrid species are by their nature polyphyletic.

<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 fertilisation. 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.

<i>Pelophylax</i> kl. <i>grafi</i> Hybrid amphibian

Graf's hybrid frog is a hybridogenic species in the true frog family Ranidae. It is found in France and Spain.

<span class="mw-page-title-main">Italian edible frog</span> Hybrid amphibian

The Italian edible frog is a hybridogenic species in the true frog family Ranidae. These frogs are the offspring of P. bergeri and either P. ridibundus or the edible frog which is itself of hybrid origin.

<i>Pelophylax</i> Genus of amphibians

Pelophylax is a genus of true frogs widespread in Eurasia, with a few species ranging into northern Africa. This genus was erected by Leopold Fitzinger in 1843 to accommodate the green frogs of the Old World, which he considered distinct from the brown pond frogs of Carl Linnaeus' genus Rana.

<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.

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.

Poeciliopsis lucida, the clearfin livebearer, is a species of small freshwater fish in the family Poeciliidae. Reproduction is viviparous, and the female can have several clutches of young developing internally at the same time. It is one of several species of small livebearing fish endemic to Mexico that were described in 1960 by the American ichthyologist Robert Rush Miller.

<span class="mw-page-title-main">Leszek Berger</span>

Leszek Berger was a Polish herpetologist and malacologist.

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.

References

  1. 1 2 3 4 5 6 7 Vrijenhoek, Robert C. (1998). "Parthenogenesis and Natural Clones" (PDF). In Knobil, Ernst; Neill, Jimmy D. (eds.). Encyclopedia of Reproduction. Vol. 3. Academic Press. pp.  695–702. ISBN   978-0-12-227020-8.
  2. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 Holsbeek, G.; Jooris, R. (2010). "Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex)" (PDF). Biological Invasions. 12: 1–13. doi:10.1007/s10530-009-9427-2. ISSN   1387-3547. Archived from the original (PDF) on 2019-07-13. Retrieved 2015-06-21.
  3. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 Christiansen, D. G. (2009). "Gamete types, sex determination and stable equilibria of all-hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus) Rana esculenta as deduced from mtDNA analyses". BMC Evolutionary Biology. 9 (135): 135. doi: 10.1186/1471-2148-9-135 . PMC   2709657 . PMID   19527499.
  4. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Ragghianti, M; Bucci, S; Marracci, S; Casola, C; Mancino, G; Hotz, H; Guex, GD; Plötner, J; Uzzell, T. (February 2007). "Gametogenesis of intergroup hybrids of hemiclonal frogs". Genetical Research. 89 (1): 39–45. doi: 10.1017/S0016672307008610 . PMID   17517158 . Retrieved 2015-06-21.
  5. 1 2 3 4 Polls Pelaz, Manuel (October 1990). "The Biological Klepton Concept (BKC)". Alytes. 8 (3): 75–89. Archived from the original on 2014-07-14. Retrieved 2015-06-22.
  6. 1 2 3 4 5 6 7 8 9 Pruvost, Nicolas B M; Hoffmann, Alexandra; Reyer, Heinz-Ulrich (Sep 2013). "Gamete production patterns, ploidy, and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus)". Ecology and Evolution. 3 (9): 2933–2946. doi:10.1002/ece3.687. PMC   3790541 . PMID   24101984.
  7. 1 2 3 4 Simon, J.-C.; Delmotte, F.; Rispe, C.; Crease, T. (2003). "Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals" (PDF). Biological Journal of the Linnean Society. 79: 151–163. doi: 10.1046/j.1095-8312.2003.00175.x . Retrieved 2015-06-21.
  8. 1 2 3 4 5 6 Vorburger, Christoph; Reyer, Heinz-Ulrich (2003). "A genetic mechanism of species replacement in European waterfrogs?" (PDF). Conservation Genetics. 4 (2): 141–155. doi:10.1023/A:1023346824722. ISSN   1566-0621. Archived from the original (PDF) on 2020-01-18. Retrieved 2015-06-21.
  9. 1 2 3 4 5 6 7 8 9 10 11 12 Spolsky, C; Uzzell, T (1986). "Evolutionary history of the hybridogenetic hybrid frog Rana esculenta as deduced from mtDNA analyses". Molecular Biology and Evolution. 3 (1): 44–56. doi: 10.1093/oxfordjournals.molbev.a040376 . PMID   2832687.
  10. 1 2 Christiansen, Ditte G.; Reyer, Heinz-Ulrich (July 2009). "From clonal to sexual hybrids: genetic recombination via triploids in all-hybrid populations of water frogs" (PDF). Evolution. 63 (7): 1754–1768. doi: 10.1111/j.1558-5646.2009.00673.x . PMID   19245393 . Retrieved 2015-06-21.
  11. 1 2 3 4 5 Berger, L. (1970). "Some characteristics of the crosses within Rana esculenta complex in postlarval development". Annales Zoologici, Warszawa. 27: 374–416.
  12. 1 2 3 Abt Tietje, Gaby; Reyer, Heinz-Ulrich (2004). "Larval development and recruitment of juveniles in a natural population of Rana lessonae and Rana esculenta" (PDF). Copeia. 2004 (3): 638–646. doi:10.1643/ce-03-273r1. Archived from the original (PDF) on 2015-04-10. Retrieved 2015-06-21.
  13. 1 2 Dubois, Alain (2009). "Asexual and metasexual vertebrates. Book review". Alytes. 27 (2): 62–66. Retrieved 2015-06-22. John C. Avise, 2008.–Clonality. The genetics, ecology, and evolution of sexual abstinence in vertebrate animals. New York, Oxford University Press: i–xi + 1–237. ISBN   978-0-19-536967-0.
  14. 1 2 Dubois, A.; Günther, R. (1982). "Klepton and synklepton: two new evolutionary systematics categories in zoology". Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere. 109: 290–305. ISSN   0044-5193.
  15. 1 2 Dubois, Alain (October 1990). "Nomenclature of parthenogenetic, gynogenetic and hybridogenetic vertebrate taxons: new proposals". Alytes. 8 (3): 61–74. Archived from the original on 2015-06-23. Retrieved 2015-06-22.
  16. 1 2 Tunner, H. G.; Heppich-Tunner, S. (1991). "Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog". Naturwissenschaften. 78 (1): 32–34. doi:10.1007/BF01134041.
  17. ↑ Berger, L. (1982). "Hibernation of the European water frogs (Rana esculenta complex)". Zoologica Poloniae. 29: 57–72.
  18. ↑ Holenweg Peter, Anna-Katherina (December 2001). "Dispersal rates and distances in adult water frogs, Rana lessonae, R. ridibunda and their hybridogenetic associate R. esculenta". Herpetologica. 57 (4): 449–460. JSTOR   3893052. url2 Archived 2015-06-21 at the Wayback Machine
  19. 1 2 Alves, M. Judite; Coelho, M. Manuela; Collares-Pereira, M. João (1998). "Diversity in the reproductive modes of females of the Rutilus alburnoides complex (Teleostei, Cyprinidae): a way to avoid the genetic constraints of uniparentalism". Molecular Biology and Evolution. 15 (10): 1233–1242. doi: 10.1093/oxfordjournals.molbev.a025852 . ISSN   0737-4038.
  20. 1 2 Morishima, K.; Yoshikawa, H.; Arai, K. (2008). "Meiotic hybridogenesis in triploid Misgurnus loach derived from a clonal lineage". Heredity. 100 (6): 581–586. doi: 10.1038/hdy.2008.17 . hdl: 2115/35324 . PMID   18382473.
  21. 1 2 3 Schultz, R. Jack (November–December 1969). "Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates". American Naturalist. 103 (934): 605–619. doi:10.1086/282629. JSTOR   2459036.
  22. 1 2 Hoffmann, Alexandra; Reyer, Heinz-Ulrich (4 December 2013). "Genomic effects on advertisement call structure in diploid and triploid hybrid waterfrogs (Anura, Pelophylax esculentus)". BMC Ecology. 13 (47): 47. doi: 10.1186/1472-6785-13-47 . PMC   4235041 . PMID   24304922.
  23. ↑ Arioli, M.; Jakob, C.; Reyer, H.U. (May 2010). "Genetic diversity in water frog hybrids (Pelophylax esculentus) varies with population structure and geographic location". Molecular Ecology. 19 (9): 1814–28. doi:10.1111/j.1365-294X.2010.04603.x. PMID   20374490. S2CID   23499806.
  24. ↑ Quilodrán, Claudio S.; Montoya-Burgos, Juan I.; Currat, Mathias (2015). "Modelling interspecific hybridization with genome exclusion to identify conservation actions: the case of native and invasive Pelophylax waterfrogs" (PDF). Evolutionary Applications. 8 (2): 199–210. doi:10.1111/eva.12245. PMC   4319866 . PMID   25685194. Archived from the original (PDF) on 2015-06-22. Retrieved 2015-06-21.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.