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Gynogenesis

Gynogenesis is a specialized form of reproduction in which an egg is stimulated to develop by sperm from a male, but the paternal genetic material is excluded or inactivated, resulting in diploid offspring that inherit their entire nuclear genome from the maternal parent alone.^[1] This process contrasts with typical sexual reproduction by producing clones of the mother, though it requires a male's sperm solely for activation rather than genetic contribution.^[2] In nature, gynogenesis occurs in select species across vertebrates and some invertebrates, including certain fish like the Amazon molly (Poecilia 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.^[2] It has also been documented in some amphibians and reptiles, though less commonly.^[1] Artificially induced gynogenesis, widely applied in aquaculture and genetics, involves inactivating sperm DNA through methods such as ultraviolet 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.^[3] This technique has been successfully implemented in over 50 fish species, including salmonids, tilapia, and cyprinids like the European loach and grass carp.^[4] Beyond animals, gynogenesis principles extend to plants, where gynogenetic diploids have been produced in more than 20 species since the 1970s, such as barley and sugar beet, aiding in the rapid generation of homozygous lines for breeding programs.^[1] In aquaculture, it is particularly valuable for creating all-female populations, which often exhibit faster growth rates and reduced sexual dimorphism, thereby improving economic yields in species like tilapia and salmon.^[1] Genetically, gynogenesis accelerates inbreeding by doubling the maternal genome, facilitating genomic studies, marker-assisted selection, and the production of isogenic lines for research.^[3] Despite its utility, challenges include high mortality rates during induction and potential epigenetic abnormalities in offspring, underscoring ongoing refinements in protocols.^[4]

Definition and Fundamentals

Definition

Gynogenesis is a form of asexual reproduction in which an egg is activated to develop into an embryo by contact with sperm from a male, but the sperm contributes no genetic material to the offspring, resulting in progeny that are genetically identical clones of the mother.^[1] This process contrasts with true sexual fertilization, as the sperm's nucleus either degenerates or is excluded following activation, preventing any paternal DNA integration.^[5]^[1] The term gynogenesis originates from the Greek words gynē (female) and genesis (origin or creation), reflecting its reliance on female genetic contribution alone.^[6] It is also referred to as pseudogamy or sperm-dependent parthenogenesis, emphasizing the obligatory role of sperm in triggering development without genetic inheritance from the male.^[7] As a specialized type of parthenogenesis, gynogenesis ensures clonal propagation while avoiding the need for full genetic recombination. In gynogenesis, offspring typically develop as diploids from unreduced maternal eggs, which bypasses the challenges of haploid development and maintains the mother's ploidy level across generations.^[1] This outcome reinforces the uniparental inheritance, producing females that perpetuate the lineage through repeated sperm activation.^[8] Gynogenesis differs from apomixis, a form of spontaneous parthenogenesis that occurs without meiosis or fertilization, in that gynogenetic eggs require external sperm activation to initiate embryonic development while remaining genetically uniparental and clonal.^[7] In apomixis, embryo formation proceeds autonomously without any sperm involvement, contrasting with the obligatory sperm dependency in gynogenesis that serves solely as a developmental trigger.^[9] Unlike androgenesis, which is the inverse process where the paternal genome is retained and the maternal genome discarded to produce offspring with solely paternal inheritance, gynogenesis preserves the entire maternal genome and excludes any paternal genetic contribution despite sperm contact.^[10] This uniparental maternal outcome in gynogenesis makes it a direct counterpart to androgenesis in vertebrates, though both are rare natural phenomena often induced experimentally for breeding purposes.^[11] Gynogenesis shares sperm dependency with hybridogenesis but lacks the hemiclonal genome replacement characteristic of the latter, where one parental genome is discarded and the retained genome undergoes recombination with incoming sperm DNA.^[12] While gynogenetic lineages produce fully clonal, all-maternal offspring, hybridogenetic systems transmit a hybrid genome partially, often involving unisexual biotypes that coexist with sexual hosts.^[13] Hybrids in gynogenesis typically arise from interspecific crosses but maintain maternal clonality without the selective genome elimination seen in hybridogenesis.^[14] In comparison to hermaphroditism or self-fertilization, gynogenesis superficially mimics sexual reproduction by necessitating sperm but yields genetically identical clonal progeny, bypassing the genetic recombination that occurs in self-fertilizing systems where gametes from the same individual fuse.^[15] 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 sperm only for activation cues.^[15] Evolutionarily, the sperm dependency in gynogenesis represents a "cheating" strategy within sexual systems, allowing asexual lineages to parasitize the gametes of coexisting sexual species without reciprocating genetic exchange, which poses a puzzle for its persistence despite potential costs to host populations.^[8] This dependency facilitates invasion of sexual niches but can reduce host fitness through sperm wastage, highlighting gynogenesis as an alternative reproductive mode that exploits sexual infrastructure for clonal propagation.^[16]

Biological Mechanism

Egg Activation Process

In gynogenesis, the process begins with the initial contact between sperm and egg, where the sperm binds to specific receptors on the egg's surface, such as those in the chorion or micropyle in teleost fish, facilitating penetration and mimicking the early stages of fertilization. This interaction allows the sperm to enter the egg cytoplasm without requiring species-specific compatibility in some gynogenetic species like the silver crucian carp (Carassius auratus gibelio).^[17]^[18] Upon sperm entry, activation signals are initiated through the release of sperm-derived cytosolic factors that trigger intracellular calcium (Ca²⁺) oscillations within the egg. These oscillations propagate as a wave from the site of sperm entry, leading to cortical granule exocytosis, which modifies the egg's extracellular matrix to block additional sperm penetration and prevent polyspermy, a mechanism conserved with normal fertilization in fish. In teleost species exhibiting gynogenesis, such as the loach (Misgurnus anguillicaudatus), this Ca²⁺ signaling is essential for resuming meiosis and initiating embryonic development.^[19]^[20] 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.^[21] Following activation, the egg completes meiosis, but in gynogenetic systems, the process often involves suppression of polar body extrusion, leading to duplication of the maternal chromosome set to restore diploidy without paternal input. This results in a haploid egg becoming diploid solely from maternal genomes. In natural gynogens like the loach (Misgurnus anguillicaudatus), meiosis is abortive and univalents form a metaphasic plate post-ovulation. In contrast, in the silver crucian carp (Carassius auratus gibelio), diploidy is restored through suppression of the first polar body extrusion via a tripolar spindle during meiosis I.^[17]^[22]^[23] 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.^[19]^[24]

Genetic and Developmental Outcomes

In gynogenesis, offspring exhibit uniparental inheritance, receiving 100% of their nuclear genetic material from the maternal genome while the sperm serves solely as a trigger for egg activation without contributing DNA.^[25] This results in clonal lineages that are genetically identical to the mother, preserving maternal traits across generations and enabling rapid fixation of advantageous alleles in stable environments.^[26] Mechanisms to restore diploidy vary by species and include suppression of polar body 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.^[27] To maintain diploidy despite the absence of paternal chromosomes, gynogenetic organisms employ mechanisms such as automixis, where meiotic products fuse to restore ploidy, or premeiotic endomitosis, which duplicates the maternal genome prior to meiosis, forming bivalents that undergo standard segregation.^[28] These processes, observed in hybrid fish like those in the Cobitis taenia complex, ensure homozygous diploid eggs but carry risks of increased homozygosity, potentially exposing recessive deleterious alleles and reducing genetic diversity over time.^[29] Phenotypically, gynogenetic offspring are morphologically similar to their mothers, reflecting the exclusive maternal genome, yet they may display developmental abnormalities arising from unresolved genomic imprinting, where certain maternally inherited genes fail to activate properly without paternal counterparts.^[30] For instance, in induced gynogenetic haploid fish embryos, such as goldfish, imprinting disruptions lead to organ malformations like abnormal eye development and edematous bodies, with survival limited beyond early stages due to improper gene expression regulation.^[30] Epigenetically, the activating sperm can influence offspring gene expression through non-genetic signals, such as calcium waves or protein factors, altering maternal chromatin without DNA incorporation and potentially modulating developmental pathways.^[26] Viability in gynogenesis is often compromised by higher rates of aneuploidy and sterility stemming from meiotic errors, particularly in induced or hybrid systems where chromosome segregation falters without paternal balancing.^[30] In natural diploid gynogens, premeiotic duplication mitigates some risks by filtering unpaired chromosomes, but persistent meiotic inaccuracies can still elevate aneuploidy, leading to reduced fertility in subsequent generations.^[28]

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.^[12] These lineages exhibit multiple independent evolutionary origins, with notable examples such as the Amazon molly (Poecilia formosa) and various crucian carp (Carassius spp.) populations.^[31] 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 sperm from related bisexual species.^[32] This complex includes biotypes that engage in gynogenetic reproduction, sometimes incorporating paternal genomes facultatively to generate diversity, though strict gynogenesis remains a core mode.^[12] Reports of gynogenesis in some anuran species are limited and primarily experimental, with natural occurrences less prevalent than in caudates.^[33] Gynogenesis is rare or undocumented in other vertebrate classes; it is absent in reptiles, birds, and mammals, where genomic imprinting and other genetic constraints likely preclude its evolution.^[12] In elasmobranchs, while facultative parthenogenesis has been observed in species such as the bonnethead shark (Sphyrna tiburo), gynogenesis remains unconfirmed.^[12] A common pattern across gynogenetic vertebrates is their hybrid origins, arising from interspecific hybridization between congeneric sexual species, which confers elevated heterozygosity and hybrid vigor while necessitating ongoing sperm parasitism from parental hosts.^[31] These all-female lineages typically coexist with one or both sexual parental species in shared habitats, relying on them for reproductive triggers without paternal genetic contribution, often stabilized by ecological niche partitioning or behavioral cues that facilitate heterospecific matings.^[8] 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 Poecilia lineages, reflecting the aquatic niches of their sexual ancestors.^[31] This distribution underscores the reliance on sympatric sexual populations in stable, resource-rich aquatic settings.^[12]

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.^[34]^[35] In arthropods, gynogenesis is notably reported in certain insects exhibiting haplodiploid sex determination. For instance, the Australian ant 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 spider beetle Ptinus clavipes, females require mating with males of the closely related P. pusillus to trigger egg development, yet the offspring inherit only maternal genetics, 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 ploidy outcomes distinct from the diploid-focused vertebrate models.^[35]^[34] 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.^[34]

Notable Examples

In Fish

Gynogenesis in fish was first documented in the 1930s with the discovery of the Amazon molly (Poecilia formosa), an all-female hybrid species endemic to northeastern Mexico and southern Texas.^[36] This small livebearing fish, originating from hybridization between the Atlantic molly (Poecilia mexicana) and the sailfin molly (Poecilia latipinna), reproduces exclusively through gynogenesis, where females produce diploid eggs that develop into clonal daughters upon activation by sperm from males of closely related Poecilia species.^[37] The sperm triggers embryogenesis but contributes no genetic material, enabling the persistence of this unisexual lineage without males.^[38] In ecological contexts, the Amazon molly functions as a sperm parasite, coexisting in sympatry with its sexual host species such as the sailfin molly, often attaining high population densities that can exceed those of the hosts in shared habitats like coastal springs and rivers.^[39] This parasitism imposes costs on host males through unproductive matings, potentially driving evolutionary responses in mate recognition, while the Amazon molly's morphological similarity to hosts facilitates deception and access to sperm.^[40] Similar dynamics occur in other poeciliid complexes, where gynogenetic forms reliant on sailfin molly males exhibit sperm parasitism without paternal genetic incorporation, contributing to stable unisexual populations in tropical freshwater systems.^[41] Among cyprinids, natural gynogenesis is exemplified by the gibel carp (Carassius gibelio), a widespread Eurasian fish where triploid females predominantly reproduce gynogenetically, using sperm from sympatric males of related cyprinids like the common carp (Cyprinus carpio) to activate eggs while excluding paternal DNA.^[42] This mode supports high-density populations in lakes and rivers, with occasional rare sexual reproduction or hybridization mimicking gene flow among cyprinid hosts.^[27] In research and aquaculture, gynogenesis is artificially induced in cyprinids such as common carp and zebrafish (Danio rerio) to generate all-female or homozygous stocks, leveraging techniques like UV-irradiated sperm and heat/pressure shocks for applications in genetics and breeding.^[17]

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 sperm from sympatric sexual species (including A. jeffersonianum, A. laterale, A. maculatum, and A. tigrinum) to activate egg development without incorporating paternal genetic material into the offspring.^[43] This process maintains clonal transmission of the maternal genome, though some populations exhibit kleptogenesis, selectively incorporating host sperm genomes to generate genetic diversity via intergenomic recombination. The complexity arises from the ability of these lineages to utilize sperm from multiple host species, enabling persistence across diverse habitats in eastern North America.^[12] 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 sperm, but the paternal genome is occasionally incorporated rather than fully discarded. This allows hybrids to "steal" genomes from coexisting parental species, 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 Europe, though it remains distinct from pure gynogenesis by permitting occasional paternal contributions.^[12] Gynogenetic amphibians like unisexual Ambystoma and Pelophylax hybrids are typically triploid or higher ploidy (up to pentaploid in some Ambystoma), resulting from ancient hybridization events followed by genome endoreduplication.^[43] 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 reproduction 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 Ontario between 1984–1991 and 2015–2017 threaten unisexual Ambystoma viability by reducing sperm availability.^[44] Habitat fragmentation 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.^[44] Reports of gynogenesis in other amphibian groups, such as caecilians (Gymnophiona), are exceedingly rare and remain unverified, with no confirmed natural occurrences beyond experimental inductions in anurans.^[12]

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 sperm from related species solely for egg activation, without incorporating paternal genetic material, thereby producing clonal offspring. This hybrid origin hypothesis is substantiated by molecular analyses, such as mitochondrial DNA sequencing and microsatellite genotyping, which reveal monophyletic lineages with fixed heterozygosity characteristic of a single foundational cross between distinct parental species. For example, in the Amazon molly (Poecilia formosa), genomic evidence confirms a hybrid ancestry from P. mexicana (maternal) and P. latipinna (paternal), with no signs of ongoing hybridization or backcrossing in contemporary populations.^[45]^[46]^[31] 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 molecular clock analyses. In fish like the Amazon molly, 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 chromosome banding and fluorescence in situ hybridization (FISH), provide molecular evidence of these origins by identifying persistent hybrid karyotypes with unbalanced or duplicated parental chromosome sets, distinguishing them from purely parthenogenetic forms.^[45]^[31]^[46] Key genetic triggers for gynogenesis involve the production of unreduced gametes during hybridization, leading to allopolyploidy (combination of divergent genomes) or autopolyploidy (duplication within a hybrid genome). These polyploid 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 Prussian carp (Carassius gibelio), polyploidy 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, polyploid females exhibit genome duplication events triggered by sperm incorporation, confirmed through cytogenetic mapping of ribosomal genes and sex chromosomes, which bypass meiotic barriers and stabilize unisexual lineages.^[47]^[31]^[48]

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.^[8] 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.^[12] 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 population growth and colonization in stable or predictable environments where genetic uniformity poses minimal risk.^[12] Additionally, occasional introgression of paternal genes during rare fertilization events allows gynogens to capture beneficial alleles, providing a mechanism to counteract Muller's ratchet—the irreversible accumulation of deleterious mutations in asexual lineages.^[8] 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 genetic load.^[49] Despite these benefits, gynogenesis incurs significant disadvantages, including the unchecked accumulation of deleterious mutations due to the absence of recombination, which heightens susceptibility to Muller's ratchet over evolutionary timescales.^[12] 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.^[50] Selective models for the persistence of gynogenesis emphasize ecological mechanisms that stabilize coexistence with sexual hosts, such as kin selection, where gynogens indirectly benefit relatives in host populations through shared ancestry, and host manipulation tactics like sexual mimicry to elicit sperm donation.^[8] Population genetics 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 overexploitation and supporting long-term persistence, as evidenced by only six local extinctions in monitored populations over three years.^[51] These dynamics highlight how niche partitioning and behavioral adaptations mitigate the parasitic burden on hosts.^[52] Looking to the future, climate change poses risks to gynogenetic persistence by altering host availability through habitat fragmentation and shifts in distribution, potentially exacerbating extinction vulnerabilities for ancient clones that depend on specific ecological associations.^[49] 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.^[53]

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new insights into the rare hybrid origin of gynogenesis in the ...
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Population genomics reveals a possible history of backcrossing and ...
Estimation of hybrid indices for the asexual individuals was also consistent with the hypothesis of hybrid origin: for the 41 P. formosa examined, hybrid index ...
[48]
[PDF] Polyploid fish and shellfish - Pacific Hybreed
For instance, several natural diploid–polyploid hybrid complexes are known in fish, in which allotriploid females are fertile and reproduce gynogenetically from ...
[49]
Gynogenesis - an overview | ScienceDirect Topics
Hybridogenesis occurs when half of the initial genome is passed on but the other half is not. Hybridogenetic females originate as crosses from two different ...
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Sperm‐dependent asexual species and their role in ecology and ...
Sep 28, 2023 · Asexual reproduction: reproductive mode in which an organism passes on its genome (or parts of it) clonally as a result of vegetative ...<|control11|><|separator|>
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https://pmc.ncbi.nlm.nih.gov/articles/PMC2596895/
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How populations persist when asexuality requires sex: the spatial ...
Asexual forms tend to outcompete sexuals but may eventually suffer higher extinction rates, creating tension between short- and long-term advantages of ...
[53]
https://doi.org/10.1002/ece3.10522
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https://doi.org/10.1002/ece3.10522