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Gynogenesis
Gynogenesis
Gynogenesis
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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.[1] 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.[2] Gynogenetic species, "gynogens" for short, are unisexual, meaning they must mate with males from a closely related bisexual species that normally reproduces sexually.[3]

Gynogenesis is a disadvantageous mating system for males, as they are unable to pass on their DNA. The question as to why this reproductive mode exists, given that it appears to combine the disadvantages of both asexual and sexual reproduction, remains unsolved in the field of evolutionary biology. The male equivalent to this process is androgenesis where the father is the sole contributor of DNA.[4]

Taxonomic range

[edit]
Poecilia formosa, the Amazon molly, requires sperm from a related species for gynogenesis.[5]

Most gynogenetic species are fishes or amphibians.[3] Among the fishes, Amazon mollies (Poecilia formosa) require the sperm of closely related male Poecilia latipinna to engage in gynogenesis. P. latipinna males prefer to mate with females of their own species.[5] This presents a problem for P. formosa, as they must compete for males who do not favour them. However, those P. formosa successful in finding a mate make up the deficit by producing twice as many female offspring as their competitors.[5] Among salamanders, the Ambystoma platineum, a unisexual mole salamander, is hybrid of sexually reproducing A. jeffersonianum and A. laterale.[6] A. platineum individuals normally live in proximity to either of these parent species, so as to access their sperm.[6]

Gynogenesis with haplodiploidy

[edit]
Gynogenesis with haplodiploidy in the ant Myrmecia impaternata. Ploidy is shown diagrammatically as 2N=6 for clarity.

The ant Myrmecia impaternata is a hybrid of M. banksi and M. pilosula.[7] In ants, sex is determined by the haplodiploidy system: unfertilized eggs result in haploid males, while fertilized eggs result in diploid females. In this species – its specific epithet impaternata meaning 'fatherless' – the queen reproduces through sexual interaction, yet not fertilization, with gynogenetically produced females, and males reared from fatherless eggs. Since these males are haploid, they are genetically identical to one of the two parent species, but are produced by a queen of M. impaternata. The queens therefore have no need to mate parasitically with males of either parent species. This situation is unique.[7]

Evolutionary origin

[edit]

Two evolutionary pathways may be considered to explain how and why gynogenesis evolved. The single-step pathway involves multiple changes taking place simultaneously: meiosis must be interrupted, one gender's gametes eradicated, and a unisexual gender formation must arise.[2] The second option involves multiple steps: a sexual generation is formed with a strongly biased sex ratio, and because of Haldane's rule the species evolves towards loss of sexuality, with selection preferential towards the gynogen.[2] Experimenters who attempted unsuccessfully to induce P. formosa by hybridizing its genetic ancestors concluded that the evolutionary origin of P. formosa was not from the simple hybridization of two specific genomes, but the movement of certain alleles.[8]

See also

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References

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Gynogenesis

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from Grokipedia
Gynogenesis is a specialized form of in which an is stimulated to develop by from a male, but the paternal genetic material is excluded or inactivated, resulting in diploid offspring that inherit their entire nuclear from the maternal parent alone. This process contrasts with typical by producing clones of the mother, though it requires a male's solely for activation rather than genetic contribution. In nature, gynogenesis occurs in select species across vertebrates and some invertebrates, including certain fish like the ( formosa), which relies on sperm from related species to trigger egg development without paternal inheritance, and the gibel carp (Carassius auratus gibelio), enabling unisexual lineages. It has also been documented in some amphibians and reptiles, though less commonly. Artificially induced gynogenesis, widely applied in and , involves inactivating DNA through methods such as or gamma irradiation, followed by physical shocks—like thermal, hydrostatic pressure, or chemical treatments—to restore diploidy either by suppressing the second meiotic division (retaining the polar body) or inhibiting the first mitotic cleavage. This technique has been successfully implemented in over 50 fish species, including salmonids, , and cyprinids like the European loach and . Beyond animals, gynogenesis principles extend to , where gynogenetic diploids have been produced in more than 20 species since the 1970s, such as and , aiding in the rapid generation of homozygous lines for breeding programs. In , it is particularly valuable for creating all-female populations, which often exhibit faster growth rates and reduced , thereby improving economic yields in species like and . Genetically, gynogenesis accelerates by doubling the maternal , facilitating genomic studies, , and the production of isogenic lines for . Despite its utility, challenges include high mortality rates during induction and potential epigenetic abnormalities in offspring, underscoring ongoing refinements in protocols.

Definition and Fundamentals

Definition

Gynogenesis is a form of in which an is activated to develop into an by contact with from a , but the contributes no genetic material to the offspring, resulting in progeny that are genetically identical clones of the mother. This process contrasts with true sexual fertilization, as the 's nucleus either degenerates or is excluded following activation, preventing any paternal integration. The term gynogenesis originates from the Greek words gynē (female) and genesis (origin or creation), reflecting its reliance on female genetic contribution alone. It is also referred to as pseudogamy or sperm-dependent , emphasizing the obligatory role of in triggering development without genetic from the male. As a specialized type of , gynogenesis ensures clonal propagation while avoiding the need for full . In gynogenesis, offspring typically develop as diploids from unreduced maternal eggs, which bypasses the challenges of haploid development and maintains the mother's level across generations. This outcome reinforces the uniparental , producing females that perpetuate the lineage through repeated sperm activation. Gynogenesis differs from , a form of spontaneous that occurs without or fertilization, in that gynogenetic eggs require external activation to initiate embryonic development while remaining genetically uniparental and clonal. In , embryo formation proceeds autonomously without any involvement, contrasting with the obligatory dependency in gynogenesis that serves solely as a developmental trigger. Unlike , which is the inverse process where the paternal is retained and the maternal discarded to produce with solely paternal inheritance, gynogenesis preserves the entire maternal and excludes any paternal genetic contribution despite sperm contact. This uniparental maternal outcome in gynogenesis makes it a direct counterpart to in vertebrates, though both are rare natural phenomena often induced experimentally for breeding purposes. Gynogenesis shares sperm dependency with hybridogenesis but lacks the hemiclonal genome replacement characteristic of the latter, where one parental is discarded and the retained undergoes recombination with incoming DNA. While gynogenetic lineages produce fully clonal, all-maternal offspring, hybridogenetic systems transmit a hybrid partially, often involving unisexual biotypes that coexist with sexual hosts. Hybrids in gynogenesis typically arise from interspecific crosses but maintain maternal clonality without the selective genome elimination seen in hybridogenesis. In comparison to hermaphroditism or self-fertilization, gynogenesis superficially mimics by necessitating but yields genetically identical clonal progeny, bypassing the that occurs in self-fertilizing systems where gametes from the same individual fuse. Self-fertilization in hermaphrodites produces offspring with recombined genomes, increasing heterozygosity decay over generations, whereas gynogenesis avoids such mixing entirely, relying on heterospecific or conspecific only for cues. Evolutionarily, the dependency in gynogenesis represents a "" strategy within sexual systems, allowing asexual lineages to parasitize the gametes of coexisting sexual without reciprocating genetic exchange, which poses a puzzle for its persistence despite potential costs to host populations. This dependency facilitates of sexual niches but can reduce host fitness through wastage, highlighting gynogenesis as an alternative reproductive mode that exploits sexual for clonal propagation.

Biological Mechanism

Egg Activation Process

In gynogenesis, the process begins with the initial contact between and , where the binds to specific receptors on the 's surface, such as those in the or in fish, facilitating penetration and mimicking the early stages of fertilization. This interaction allows the to enter the without requiring species-specific compatibility in some gynogenetic species like the silver crucian carp ( auratus gibelio). Upon entry, activation signals are initiated through the release of sperm-derived cytosolic factors that trigger intracellular calcium (Ca²⁺) oscillations within the . These oscillations propagate as a wave from the site of entry, leading to cortical granule , which modifies the 's extracellular matrix to block additional penetration and prevent , a mechanism conserved with normal fertilization in . In species exhibiting gynogenesis, such as the (Misgurnus anguillicaudatus), this Ca²⁺ signaling is essential for resuming and initiating embryonic development. The fate of the sperm nucleus in gynogenesis differs critically from standard fertilization: it fails to decondense and form a functional male pronucleus, remaining as a condensed chromatin mass that is either excluded from the female pronucleus or gradually absorbed by the egg's cytoplasm without contributing genetic material. In the silver crucian carp, eggs selectively prevent decondensation of heterologous sperm nuclei, ensuring no paternal DNA integration while still utilizing the sperm for activation. This exclusion occurs during or shortly after meiotic resumption, avoiding pronuclear fusion. Following activation, the egg completes , but in gynogenetic systems, the process often involves suppression of polar body extrusion, leading to duplication of the maternal set to restore diploidy without paternal input. This results in a haploid egg becoming diploid solely from maternal genomes. In natural gynogens like the (Misgurnus anguillicaudatus), is abortive and univalents form a metaphasic plate post-ovulation. In contrast, in the silver (Carassius auratus gibelio), diploidy is restored through suppression of the first polar body extrusion via a tripolar spindle during I. Key molecular players include unidentified cytosolic sperm factors in teleost fish that induce Ca²⁺ release and oscillations, analogous to but distinct from mammalian PLC-ζ, ensuring activation without subsequent genome integration. These factors are delivered upon sperm-egg fusion, highlighting the sperm's role as a physiological trigger rather than a genetic contributor in gynogenesis.

Genetic and Developmental Outcomes

In gynogenesis, exhibit uniparental , receiving 100% of their nuclear genetic material from the maternal while the serves solely as a trigger for activation without contributing . This results in clonal lineages that are genetically identical to the , preserving maternal traits across generations and enabling rapid fixation of advantageous alleles in stable environments. Mechanisms to restore diploidy vary by species and include suppression of extrusion, premeiotic endoreplication, or automixis. Additionally, some gynogenetic species like the silver crucian carp exhibit dual reproductive modes, including occasional gonochoristic reproduction, as documented in studies up to 2024. To maintain diploidy despite the absence of paternal chromosomes, gynogenetic organisms employ mechanisms such as automixis, where fuse to restore ploidy, or premeiotic endomitosis, which duplicates the maternal prior to , forming bivalents that undergo standard segregation. These processes, observed in hybrid like those in the Cobitis taenia complex, ensure homozygous diploid eggs but carry risks of increased homozygosity, potentially exposing recessive deleterious alleles and reducing over time. Phenotypically, gynogenetic offspring are morphologically similar to their mothers, reflecting the exclusive maternal , yet they may display developmental abnormalities arising from unresolved , where certain maternally inherited genes fail to activate properly without paternal counterparts. For instance, in induced gynogenetic haploid fish embryos, such as , imprinting disruptions lead to organ malformations like abnormal and edematous bodies, with survival limited beyond early stages due to improper regulation. Epigenetically, the activating can influence offspring through non-genetic signals, such as calcium waves or protein factors, altering maternal without DNA incorporation and potentially modulating developmental pathways. Viability in gynogenesis is often compromised by higher rates of and sterility stemming from meiotic errors, particularly in induced or hybrid systems where segregation falters without paternal balancing. In natural diploid gynogens, premeiotic duplication mitigates some risks by filtering unpaired chromosomes, but persistent meiotic inaccuracies can still elevate , leading to reduced in subsequent generations.

Taxonomic Distribution

In Vertebrates

Gynogenesis is primarily documented among teleost fishes, where it occurs in approximately 50 named species across several families, including Poeciliidae, Cyprinidae, and Cobitidae, often manifesting as all-female clonal lineages that depend on sperm from sympatric sexual species for egg activation. These lineages exhibit multiple independent evolutionary origins, with notable examples such as the Amazon molly (Poecilia formosa) and various crucian carp (Carassius spp.) populations. In amphibians, gynogenesis is notable in salamanders of the genus Ambystoma, particularly within the A. laterale-jeffersonianum complex, where unisexual triploid females produce unreduced triploid eggs that develop clonally upon activation by from related bisexual . This complex includes biotypes that engage in gynogenetic reproduction, sometimes incorporating paternal genomes facultatively to generate diversity, though strict gynogenesis remains a core mode. Reports of gynogenesis in some anuran are limited and primarily experimental, with natural occurrences less prevalent than in caudates. Gynogenesis is rare or undocumented in other vertebrate classes; it is absent in reptiles, birds, and mammals, where and other genetic constraints likely preclude its evolution. In elasmobranchs, while facultative has been observed in such as the (Sphyrna tiburo), gynogenesis remains unconfirmed. A common pattern across gynogenetic s is their hybrid origins, arising from interspecific hybridization between congeneric sexual , which confers elevated heterozygosity and hybrid vigor while necessitating ongoing sperm from parental hosts. These all-female lineages typically coexist with one or both sexual parental in shared habitats, relying on them for reproductive triggers without paternal genetic contribution, often stabilized by partitioning or behavioral cues that facilitate heterospecific matings. Geographically, gynogenetic vertebrates are predominantly found in freshwater and coastal environments, such as North American lakes and ponds for Ambystoma salamanders and northeastern Mexican river systems for lineages, reflecting the aquatic niches of their sexual ancestors. This distribution underscores the reliance on sympatric sexual populations in stable, resource-rich aquatic settings.

In Invertebrates

Gynogenesis in invertebrates occurs sporadically across phyla and is generally rarer than in vertebrates, often manifesting as a facultative reproductive strategy integrated with other modes like haplodiploidy or parthenogenesis. Unlike the more uniform diploid restoration seen in vertebrate gynogens, invertebrate forms exhibit greater variability in ploidy levels, including cases of polyploidy or haplodiploid outcomes, reflecting diverse genetic mechanisms adapted to specific ecological pressures. These systems typically depend on sperm from conspecific or heterospecific males solely for egg activation, without paternal genetic incorporation, enabling all-female lineages while exploiting shorter generation times compared to vertebrates for rapid colonization of niches such as hypersaline environments or parasitic habitats. In s, gynogenesis is notably reported in certain insects exhibiting haplodiploid sex determination. For instance, the Australian Myrmecia impaternata represents a unique hybrid-origin species that reproduces via gynogenesis, where eggs are activated by sperm from related Myrmecia species but develop into diploid females without paternal genomic contribution, maintaining an all-female population. Similarly, in the Ptinus clavipes, females require with males of the closely related P. pusillus to trigger egg development, yet the offspring inherit only maternal , highlighting gynogenesis as a mechanism to ensure reproductive assurance in low-density populations. These arthropod examples illustrate how gynogenesis can integrate with haplodiploid systems, producing variable outcomes distinct from the diploid-focused models. Among other invertebrate groups, gynogenesis is reported in some nematodes, often linked to parasitic lifestyles, with mating stimuli from males triggering egg-laying without genetic fusion, facilitating persistence in host-dependent cycles. Overall, invertebrate gynogenesis underscores a spectrum of ploidy variability—ranging from haploid to polyploid—and a strong reliance on heterospecific sperm for activation, contrasting with vertebrate forms through accelerated generational turnover that enhances adaptability in fragmented or extreme habitats.

Notable Examples

In Fish

Gynogenesis in fish was first documented in the 1930s with the discovery of the (Poecilia formosa), an all-female hybrid species endemic to northeastern and southern . This small livebearing fish, originating from hybridization between the Atlantic molly (Poecilia mexicana) and the (Poecilia latipinna), reproduces exclusively through gynogenesis, where females produce diploid eggs that develop into clonal daughters upon activation by from males of closely related Poecilia species. The triggers embryogenesis but contributes no genetic material, enabling the persistence of this unisexual lineage without males. In ecological contexts, the functions as a sperm , coexisting in with its sexual host species such as the , often attaining high population densities that can exceed those of the hosts in shared habitats like coastal springs and rivers. This imposes costs on host males through unproductive matings, potentially driving evolutionary responses in mate recognition, while the 's morphological similarity to hosts facilitates deception and access to sperm. Similar dynamics occur in other poeciliid complexes, where gynogenetic forms reliant on males exhibit sperm without paternal genetic incorporation, contributing to stable unisexual populations in tropical freshwater systems. Among cyprinids, natural gynogenesis is exemplified by the gibel carp (Carassius gibelio), a widespread where triploid females predominantly reproduce gynogenetically, using sperm from sympatric males of related cyprinids like the common carp ( carpio) to activate eggs while excluding paternal DNA. This mode supports high-density populations in lakes and rivers, with occasional rare or hybridization mimicking among cyprinid hosts. In research and , gynogenesis is artificially induced in cyprinids such as common carp and (Danio rerio) to generate all-female or homozygous stocks, leveraging techniques like UV-irradiated sperm and heat/pressure shocks for applications in and breeding.

In Amphibians and Other Vertebrates

Gynogenetic reproduction in amphibians is prominently exemplified by unisexual lineages in the genus Ambystoma, particularly mole salamanders such as A. platineum, which originated through hybridization between A. jeffersonianum and A. tigrinum. These triploid females reproduce gynogenetically, relying on from sympatric sexual (including A. jeffersonianum, A. laterale, A. maculatum, and A. tigrinum) to activate egg development without incorporating paternal genetic material into the offspring. This process maintains clonal transmission of the maternal genome, though some populations exhibit kleptogenesis, selectively incorporating host genomes to generate via intergenomic recombination. The complexity arises from the ability of these lineages to utilize from multiple host , enabling persistence across diverse habitats in eastern . In European water frogs of the genus Pelophylax, particularly the hybrid P. esculentus complex (involving P. lessonae and P. ridibundus), reproductive modes border on gynogenesis through kleptogenesis, a variant where unreduced diploid eggs are activated by , but the paternal is occasionally incorporated rather than fully discarded. This allows hybrids to "steal" from coexisting parental , producing offspring that may retain the kleptogenized genome or revert to clonal transmission, contrasting with strict hybridogenesis in diploid forms. Such flexibility has enabled these polyploid lineages to thrive in mixed populations across , though it remains distinct from pure gynogenesis by permitting occasional paternal contributions. Gynogenetic amphibians like unisexual Ambystoma and Pelophylax hybrids are typically triploid or higher (up to pentaploid in some Ambystoma), resulting from ancient hybridization events followed by genome endoreduplication. Their life history is tightly linked to the seasonal breeding cycles of host species, as egg activation depends on synchronous mating periods in vernal pools or wetlands, limiting to brief windows and increasing susceptibility to environmental disruptions. Conservation efforts for these taxa face challenges due to their dependence on declining host populations; for instance, reductions in A. texanum (small-mouthed salamander) abundance from 28.1% to 3.3% at monitored sites in between 1984–1991 and 2015–2017 threaten unisexual Ambystoma viability by reducing sperm availability. further exacerbates this vulnerability, as limited dispersal (often <50 m) prevents access to alternative hosts, contributing to local extirpations and necessitating targeted protection of breeding sites under species-at-risk legislation. Reports of gynogenesis in other amphibian groups, such as (Gymnophiona), are exceedingly rare and remain unverified, with no confirmed natural occurrences beyond experimental inductions in anurans.

Evolutionary Dynamics

Origins and Hybridization

Gynogenesis in vertebrates predominantly originates from interspecific hybridization, where the resulting hybrid females develop a reproductive mode that relies on from related solely for activation, without incorporating paternal genetic material, thereby producing clonal . This hybrid origin hypothesis is substantiated by molecular analyses, such as sequencing and , which reveal monophyletic lineages with fixed heterozygosity characteristic of a single foundational cross between distinct parental . For example, in the ( formosa), genomic evidence confirms a hybrid ancestry from P. mexicana (maternal) and P. latipinna (paternal), with no signs of ongoing hybridization or in contemporary populations. The timeline of gynogenesis evolution indicates multiple independent origins across taxa, with genetic divergence estimates placing most lineages between 10,000 and 300,000 years ago based on analyses. In fish like the , the hybridization event is dated to approximately 100,000–300,000 years ago, representing one of the more ancient verified cases, while other complexes, such as those in Poeciliopsis, suggest more recent emergences around 50,000 years. Cytogenetic studies, including banding and (FISH), provide molecular evidence of these origins by identifying persistent hybrid karyotypes with unbalanced or duplicated parental sets, distinguishing them from purely parthenogenetic forms. Key genetic triggers for gynogenesis involve the production of unreduced gametes during hybridization, leading to allopolyploidy (combination of divergent s) or autopolyploidy (duplication within a hybrid ). These states circumvent typical hybrid sterility by enabling genome-wide duplication, which restores fertility and suppresses recombination, allowing clonal propagation. In allotriploid fish hybrids, such as the ( gibelio), arises from interspecific crosses followed by genome retention and duplication, as evidenced by karyotypic analyses showing three divergent genome sets that support gynogenetic egg production. Similarly, in the Ambystoma salamander complex, females exhibit genome duplication events triggered by incorporation, confirmed through cytogenetic mapping of ribosomal genes and , which bypass meiotic barriers and stabilize unisexual lineages.

Persistence and Selective Pressures

Gynogenetic species exhibit a sperm dependency paradox, wherein they require sperm from closely related sexual host species to activate egg development without incorporating paternal genetic material, rendering them vulnerable to fluctuations in host population density and distribution. This dependency paradoxically enables gynogens to evade the twofold cost of sex by producing only female offspring, thereby doubling reproductive output compared to sexual counterparts that allocate resources to males. For instance, in the Amazon molly (Poecilia formosa), this reliance on sperm from species like P. mexicana or P. latipinna has sustained the lineage for an estimated 100,000–300,000 years despite the potential for host rejection through mate discrimination. Among the advantages of gynogenesis is rapid clonal propagation, which facilitates efficient and in stable or predictable environments where genetic uniformity poses minimal risk. Additionally, occasional of paternal genes during rare fertilization events allows gynogens to capture beneficial alleles, providing a mechanism to counteract —the irreversible accumulation of deleterious mutations in asexual lineages. Empirical studies on unisexual lineages, such as those in the genus Cobitis, demonstrate that this gene capture has enabled persistence across hundreds of thousands of generations by periodically purging . Despite these benefits, gynogenesis incurs significant disadvantages, including the unchecked accumulation of deleterious mutations due to the absence of recombination, which heightens susceptibility to over evolutionary timescales. This clonal nature also reduces adaptability to environmental changes, as populations lack the genetic diversity needed for rapid evolution in response to novel selective pressures, with molecular evidence indicating that most unisexual vertebrate lineages are evolutionarily short-lived, often less than 1 million years old. Selective models for the persistence of gynogenesis emphasize ecological mechanisms that stabilize coexistence with sexual hosts, such as , where gynogens indirectly benefit relatives in host populations through shared ancestry, and host manipulation tactics like to elicit . analyses, including spatial metapopulation models, reveal that gynogens maintain stability by balancing colonization rates with local extinction risks; for example, in Poecilia formosa systems, mixed patches predominate when asexual exploitation of hosts is moderate, preventing and supporting long-term persistence, as evidenced by only six local extinctions in monitored populations over three years. These dynamics highlight how niche partitioning and behavioral adaptations mitigate the parasitic burden on hosts. Looking to the future, poses risks to gynogenetic persistence by altering host availability through and shifts in distribution, potentially exacerbating vulnerabilities for ancient clones that depend on specific ecological associations. In systems like Central European Cobitis hybrids, such changes could limit sperm-dependent asexuals' ability to track suitable hosts, amplifying the impacts of reduced genetic adaptability.

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