hybridization is an attempt to create an organism with traits from what type of organisms
Abstract
A dramatic increase in the hybridization between historically allopatric species has been induced past human activities. However, the notion of hybridization seems to lack consistency in ii respects. On the i paw, it is inconsistent with the biological species concept, which does non permit for interbreeding betwixt species, and on the other hand, it is considered either as an evolutionary process leading to the emergence of new biodiversity or as a cause of biodiversity loss, with conservation implications. In the first case, nosotros fence that conservation biology should avert the give-and-take around the species concept and delimit priorities of conservation units based on the bear on on biodiversity if taxa are lost. In the second case, we show that this is not a paradox but an intrinsic property of hybridization, which should exist considered in conservation programmes. We propose a novel view of conservation guidelines, in which man-induced hybridization may also be a tool to enhance the likelihood of accommodation to changing ecology weather condition or to increment the genetic diversity of taxa afflicted by inbreeding depression. The conservation guidelines presented here correspond a guide for the development of programmes aimed at protecting biodiversity as a dynamic evolutionary system.
Introduction
Biodiversity is in crisis and the main reasons are human activities inducing habitat modifications and the introduction of invasive speciesi. In add-on, global climate change will probably modify habitat characteristics, migration patterns, reproduction time, and place of various species2. Such human disturbances may produce new breeding overlaps, breaking the independent development of organisms and leading to hybridization (run into Glossary, Table 1)3. The function of hybridization in the evolution of several plant and animal taxa has been recognized in the light of newly developed molecular tools4. This has also alerted biologists about the threat this miracle may represent to biodiversity when enhanced by anthropogenic factorsv. We identified three types of hybridization regarding the reproductive properties of beginning-generation hybrids (F1). This is proposed as a framework to investigate the demographic and genetic furnishings of hybridization on biodiversity.
Our perspectives come up from the development of modeling simulation approaches applied to various real case studies, which helped us to explore the outcomes of hybridization from both conservation and evolutionary perspectives. Nosotros bring here a novel view of conservation guidelines aiming to land the atmospheric condition under which hybridization may represent priorities for conservation programmes or, alternatively, new evolutionary opportunities. Nosotros highlight that hybridization may certainly lead to biodiversity loss when enhanced by human factors, leading for instance to outbreeding depression or the introgression of maladaptive genes. However, it may also drive the emergence of new biodiversity, reducing the effects of inbreeding depression, and increasing the opportunities to adapt to changing environmental conditions.
Species concept trouble and interspecific hybridization
The widely accepted biological species concept formulated by Mayr6 states that species are "groups of really or potentially interbreeding natural populations which are reproductively isolated from other such groups". The key thought nether this vision is the reproductive isolation that delimits the species unit. This was already proposed past Georges-Louis Leclerc, Comte de Buffon, more than 260 years ago7. Buffon realized that a equus caballus and a donkey are morphologically more like than some unlike races of dogs. All the same, the reproduction in the first example leads to an infertile offspring (a mule) while in the second case, the offspring is fertile, highlighting that a line can be fatigued between organisms that cannot reproduce in order to differentiate species.
Charles Darwin supported a different view and dedicated an entire chapter of "On the Origin of Species" to the hybridization conceptviii. The ascertainment of interbreeding between distinct morphological species, with unlike degrees of offspring fertility, from completely sterile to even more fertile than parental species in determined conditions, was an argument confronting sterility or fecundity as a species delineation cistron. Darwin agreed with the notion that species may hardly remain unlike when costless sympatric mating occurs, but supported a more than continuous conception of species, influenced by the gradual effect of natural selection. However, the idea of species with various degrees of fertility was abased during the modern evolutionary synthesis6,ix,10.
Much of the understanding about reproductive isolation and interspecific hybridization has been revealed by experimental studies of Drosophila 11. Those works revealed that: (i) reproductive isolation is positively correlated with the phylogenetic distance between hybridizing species; (two) at the aforementioned level of genetic deviation, reproductive isolation is college between sympatric than allopatric species; and (iii) hybrid offspring follow Haldane's rule, meaning that if one sex activity is less viable or sterile, it is more probable to be the heterozygotic sex12,thirteen. During most of the 20th century, interspecific hybridization was considered to be rare in nature, mainly arising by human translocation of species and with a small effect in development, with hybrids supposedly having lower fertility in near cases14.
Despite the wide acceptance of reproductive isolation as a key chemical element to ascertain species, a large controversy persists around the biological species concept (Box one). This is mainly motivated by the semipermeable breeding barriers between some species and the difficulty of testing this notion in organisms with nonoverlapping spatial or temporal distribution ranges15,16.
Species concept and conservation
A problematic view arises when applying the biological species concept, which does not make room for interspecific hybridization17. The semipermeable barriers between genetically, morphologically or ecologically singled-out organisms take motivated a large debate about species and hybridization, e.1000., refs. xv,18. This discussion is not superfluous for conservation biology because it delimits the main unit of protection17. Yet, what are the central criteria to delineate the units that deserve protection? Some authors consider that considering species are evolutionary units, the most appropriate way to diagnose them objectively is through the phylogenetic species concept19. Merely the use of the phylogenetic species concept has been criticized because pocket-size, isolated populations may become well diagnosed evolutionary lineages through the effect of strong genetic migrate, inflating the number of species and rendering protection actions more than complex. Other authors have advocated that the criteria to delineate conservation units should rely on evidence of reproductive isolation or reduced reproductive fitnesstwenty, but these criteria are less objective and sometimes hard to evidence.
The debate well-nigh species concept and hybridization is non only a matter for biologists, but as well for scientists from very dissimilar domains, as well as politicians who define legal aspects of wildlife protection21. In this sense, Pasachnik et al.22 propose that whatever else a species is, in the field of conservation biological science it should be a grouping of organisms deserving legal protection because its extinction would institute a meaningful loss of biodiversity. The evolution of biodiversity represents a continuum, in which speciation processes may occur slowly or relatively fast, but volition always accept a menses of dubiousness regarding genetic differentiation between emerging species23. Conservation biological science may therefore consider the level of dubiety due to hybridization by protecting biodiversity as a dynamic system, which is not focused on reproductive isolation to delimit discrete units, but on the sum of features for which the loss of sure organisms may represent a detrimental effect on biodiversity.
Evolution of new biodiversity
Botanists first highlighted the important function of natural hybridization on the speciation procedure of several species, i.e., in generating new biodiversity, east.g., 24,25. Later, zoologists recognized the major evolutionary furnishings of introgression on numerous insects e.g., ref. 26, fishes, eastward.g. ref. 27, amphibians, e.thousand., ref. 28, reptiles, e.chiliad., ref. 29, birds, e.g., ref. 30, mammals, due east.one thousand., ref. 31; and other organisms, e.g., ref. 32, including mod humans (Box 2). At that place are effectually 25% of plants and x% of animals that are currently known to hybridize with another species and the effect of this phenomenon in development is considered to be much more important than previously thought33.
Species tin can naturally change their historical home range in response to irresolute ecology conditions and meet closely related taxa34. Several species bear signatures of hybrid ancestry from the concluding Ice Historic period period, e.g., ref. 27. For this reason we can discover Deoxyribonucleic acid of dark-brown bears in polar bears, because ancient hybridization events occurred during the Pleistocene35. The Bering Country Span recurrently emerged during this fourth dimension, assuasive organisms to drift betwixt Eurasia and North America, leading to opportunities of hybridization, such equally those observed between Canada lynx (Lynx canadensis) and Eurasian lynx (Lynx lynx)31. Organisms can have introgressed genes from locally extinct species even if they accept never been in contact, considering a tertiary species, acting every bit a temporal bridge to cistron flow, has hybridized with both of them east.g., ref. 36.
Natural option may fix beneficial alleles obtained by hybridization or, to the reverse, remove detrimental introgressed alleles. Adaptive introgression has been important for several speciation processes33. For example, the antipredatory mimicry of iii Heliconius butterflies in South America has been caused by interspecific hybridization, for which the parts of the genome related to color patterns have more introgressed alleles than other regions of the genome37. Introgressed alleles can rapidly spread among individuals when they are related to adaptive traits. For instance, "warfarin" is a rodenticide that was developed in 1948 to control business firm mice (Mus musculus). Mice started to be resistant during the 1960s past acquiring a unmarried gene from the Algerian mouse (K. spretus) through hybridization38. These species were isolated until the development of human agricultural lands. They rarely interbreed and hybrids take limited survival with half of them being sterile, but the resistance cistron apace spread across Europe. In Germany, where both species do non mingle, one third of house mice accept the introgressed resistance gene coming from Algerian mice38. A like instance was documented between two species of mosquitos that are vectors of malaria and have different levels of resistance to an insecticide39. The insecticide acted as a selective pressure driving the spread of resistant alleles obtained by hybridization, even when hybrids had reduced fertility40. The reduced fertility of the offspring is therefore not necessarily selected against and can also represent adaptive mate choice41.
Opportunities for speciation as a result of hybridization can be generated when hybrids exploit unique ecological niches. For instance, a rapid incipient speciation was recently observed in the offspring of 2 species of yeast, Saccharomyces paradoxus and South. cerevisiae, whose hybrids accept the potential to exploit a unique environmental that is intermediate between those of the parental species32. The new genetic architecture generated by hybridization tin thus also facilitate ecological difference, promoting a speciation process by exploiting a specific niche, e.g., ref. 42.
Positive option can set adaptive alleles and purifying selection can remove the detrimental alleles, due east.g., ref. 27, but introgressed genes can remain even without the event of natural choice. Neutral introgressed alleles can persist in high proportion, even when the original species is extinct. Currat et al.43 demonstrated through estimator simulations and by a review of the literature, that invasive species in range expansion may conduct a big quantity of neutral alleles that are introgressed from a local species. The opposite is not necessarily true unless interbreeding is rare (Fig. 1). When hybridization occurs during the expansion of an invasive species into the territory of a local species, introgression is indeed expected to be much higher in the invasive species than in the local species (Fig. 1). This blueprint of asymmetric introgression is more often than not robust to the density and population structure within both species and to the level of interspecific competition. Information technology results from the hybridization level and from the population demographic imbalance at the wave front of the invasion, in which introgressed alleles that are continuously introduced in the invasive species along its expansion, may surf and attain a higher frequency than expected nether a stationary context44. While this pattern may be perturbed by density-dependent dispersal45 and long-distance dispersal46, there are several existent cases of asymmetrical introgression betwixt demographically imbalanced species that take been proposed to follow this neutral expectation, east.g. refs. 47,48.
a The context of this expected pattern of introgression is the expansion of an invasive species (in beige) in an area where the local species (in blue) is already in demographic equilibrium. The invasive species starts its colonization from the bottom left side of the area with few individuals. b The level of introgression is asymmetrical and higher in the invasive organisms when the interbreeding charge per unit is big enough (after the dotted line in the 10-centrality). The value of the admixture rate that delineates this expected higher introgression in the invasive taxon depends on the combination of demographic and migration parameters43. The introgression disproportion between the two species is due to local alleles continuously introduced at the wave front end of the invasive range expansion, with a relatively high probability of increasing in frequency due to the surfing process44. The invasive organisms are non necessarily non-indigenous and may also stand for threatened organisms that increase in frequency at the expense of exotic organisms45.
Biodiversity loss
Hybridization is considered as a major conservation business concern when information technology is motivated past anthropogenic factors, such every bit translocation of invasive species or by modification of natural habitats5,49. The breakdown of the reproductive barriers betwixt organisms may disrupt their independent evolution and has already increased the run a risk of extinction of several plant and beast taxa, e.g., refs. 50,51.
Hybridization may atomic number 82 to different merely potentially interacting mechanisms that threaten species persistence. First, outbreeding low may stand for a meaning loss of reproductive value and detonates a rapid extinction when it interacts with a demographic pass up. This may be stronger between genetically distant species e.g., ref. 52, but organisms do non need to exist distantly related to be afflicted by outbreeding depression. For example, the human domestication of Atlantic salmon (Salmo salar) has led to lower fertility when mating with conspecifics in the wild, representing a serious threat for wild salmon in Norway53. Second, native genotypes tin disappear by genetic swamping and exist replaced by the numerical or competitive advantage of invasive genotypes. Third, the introgression of non-native genes can disrupt local adaptations by introducing maladaptive gene complexes54. Quaternary, the behavior of wild animals may exist perturbed in a mode that is difficult to predict, more peculiarly when information technology concerns human domesticated animals55, which have been artificially selected co-ordinate to human lifestyle and, when spreading their genes in nature, may influence a whole network of ecological interactions, due east.thousand., ref. 56. Fifth, hybridization may affect the effective population size of the interacting species with major consequences for rare or threatened species, which already take a reduced number of breeders57. Finally, an important trouble for conservation biology arises when the few remaining individuals of a threatened species testify a level of introgression that may crusade them to lose their legal protection condition when hybrids are not considered to exist protected organisms, even though the hybrids may have an ecological function otherwise lost with the extinction of parental species21,58.
The loss of species distinctiveness due to introgression has also been called "speciation reversal", e.g., ref. 59. This may seriously impact key ecological adaptations that appeared during species radiation. Vonlanthen et al.sixty documented the rapid extinction of whitefish (Coregonus spp.) in Swiss lakes, which evolved according to ecological opportunities, only human eutrophication and homogenization of the surround is driving extinction by hybridization and demographic decline. A similar example was documented for cichlid fishes of Lake Victoria (Eastward Africa), for which the coloration blueprint is a key character that determines mate option and reproductive isolation, simply the turbidity of the water induced by eutrophication relaxed sexual choice, destroying the diversification machinery61. Speciation reversal is a conservation concern, because it erodes the ecological and genetic distinctiveness between closely related, but ecologically divergent, speciessixty. In a context of climate change, Owens and Samuk62 refers to hybridization as a double edge sword, because even when increasing the pool of potentially adaptive genes, some of these genes may be related to reproductive isolation, weakening whatever reproductive barrier. The various cases of hybridization leading speciation reversal, e.yard., refs. 59,61, advise that the extinction chance may be more all-encompassing than previously thought60.
Hybridization between wild and domesticated organisms is a worldwide problem of conservation. For instance, the main electric current threat for the persistence of European wildcats (Felis silvestris) is the hybridization with domestic cats (Felis catus)63,64. Domestic cats were originally domesticated from a mutiny inhabiting the Almost East (Felis lybica), only they are genetically singled-out to all electric current F. lybica subspecies65. There are notwithstanding some wildcat populations remaining in Europe, e.g., ref. 66, but the complete admixture and the loss of genetic distinctiveness have already been accomplished in some countries67. Domestic dogs (Dog) can hybridize with any kind of wolf-similar canids and have already led to conservation problems in various cases50, such every bit for the grey wolf (Canis lupus) in Europe, e.g., ref. 68 the coyote (Canis latrans) in North America, e.k., ref. 56 or the Ethiopian wolf (Canis simensis) in Africa, e.thou. ref. 69. Ellington and Murray56 found that hybridization with domestic dogs was driving changes in the space occupied by coyotes, suggesting consequences at the ecosystem level. A particular threat is the hybridization of domestic dogs with the Ethiopian wolf, which is the world'due south nearly endangered canid, persisting with around 500 individuals in 6 isolated populations69,lxx. The detrimental effects of hybridization with domesticated organisms is reinforced, because they far outnumber their wild counterparts, eastward.k., ref. 71, in which the extinction risk can be particularly accelerated when rare species hybridize with more abundant species.
Genetically modified organisms and genetic applied science have generated a large fence on how to regulate the spread of modified genes in nature through hybridization due east.g., ref. 72. Genomic alteration for economical purposes may induce higher fertility and resistance to pathogens that brand crops or hybrids highly invasive73. The reduced fertility of the commencement-generation hybrids (Fone) is not a bulwark for the spread of advantageous alleles74, which are ofttimes observed in the wild, e.one thousand., ref. 75 with hybrids condign invasive in diverse cases76. The ecological release of their natural predators or pathogens conferred by the resistant alleles has been proposed as a factor that is initiating this invasion73. A serious take a chance has been detected in the unmarried wild population of rice in Costa Rica (Oryza glumaepatula) that hybridizes with invasive commercial rice (O. sativa)77. The concerns are non but related to modified plant crops, only also to animals of economical interest, ordinarily with unpredictable ecological furnishings, east.g., ref. 78 or to non-target insects, equally has been documented for the monarch butterfly Danaus plexippus of North America, e.thousand., ref. 79.
Types of hybridization
We defined three main types of hybridization that may exist used equally a framework for the understanding of the ecological and evolutionary consequences of hybridization (Fig. two). These categories include: (1) afar species hybridization, by and large preventing factor flow because hybrids are infertile (Type 1) or (2) because homologous chromosomes practice not recombine (Blazon 2); and (3) interbreeding betwixt more than closely related taxa, in which homologous chromosomes recognize themselves during meiosis, resulting in gene period and consequent introgression between parental organisms (Type iii) (Box 3).
Type one represents infertile or inviable hybrids. Type 2 hybrids are fertile but introgression is prevented in further generations due to the generation of gametes without recombination during gametogenesis in hybrid offspring. Type 3 hybrids are fertile and there is recombination during gametogenesis allowing introgression in further generations. Non-human-induced hybridization represents hybrids naturally found in nature, in which evolutionary opportunities arise when hybrids are fertile. Conservation guidelines are proposed for homo-induced hybridization, which are motivated by any anthropogenic factor. They represent either a purely demographic or both a demographic and genetic effect on interbreeding taxa. The conservation priorities to avoid biodiversity loss are highlighted in red and basically represent human-induced hybridization that produces demographic decline or ecological disequilibrium. A potential tool to increase genetic diversity is highlighted in green.
Unlike steps that may be considered to recognize the type of hybridization when in that location is evidence of interbreeding between taxa (modified from Quilodrán et al.81).
Type 1: Infertile hybrids, no introgression
The first type of hybridization does not consequence in introgression, considering offspring are inviable or infertile. This type of hybridization represents an extinction risk when the loss of reproductive value enhances a demographic decline for one (or both) parental species. The reasons could exist either considering pocket-sized populations interbreed with more abundant populations and therefore waste material reproductive efforts, or considering boosted threats are accumulated, such equally a disease. For instance, in the case of hybridization betwixt Atlantic salmon (Salmo salar) and brownish trout (Salmo trutta), hybridization alone is probable not a threat, but could pb to the extinction of some local salmon populations that are already threatened by a parasitic disease80. This type of hybridization may be considered an evolutionary dead-finish.
Type 2: Fertile hybrids, no introgression
The second blazon of hybridization results in fertile F1 hybrids, but introgression is prevented because their offspring are clonal or hemiclonal, transmitting a unmarried parental genome, also called hybridization with genome exclusion. Nosotros recently showed that the extinction of natives and the invasion of exotic organisms might exist reached in very few generations81. For example, in the instance of hybridogenesis betwixt Western European water-frogs (Pelophylax species complex)51, the extinction run a risk is non genetically driven, only adamant past the "demographic flow" betwixt parental species and mediated past hybrid offspring. Nosotros previously demonstrated that this hybridization is a highway to extinction, which may be underappreciated considering it emulates the result of hybridization blazon one (i.due east., only displaying F1 hybrid phenotypes)81. Evolutionary opportunities may emerge from these systems by generating self-reproducing polyploid forms82, which are observed in plants simply rarely constitute in animals83.
Type 3: Fertile hybrids, introgression
The third blazon of hybridization defines interbreeding with gene period between parental organisms leading to genomic mixing and therefore to introgression. This type of hybridization may result in ii unlike effects on biodiversity, either a genetic and demographic risk of species extinction5, or the opportunity of adaptation and evolution of novel diversityfourteen. For instance, hybrids may replace native species and facilitate biological invasions every bit in the instance of mallard (Anas platyrhynchos), which has been widely translocated, cohabiting with other duck species and threatening them by hybridization84. In some other example, however, genes from extinct hominids may even so be found in high frequency in current human populations due to old hybridization events43,85. This type of hybridization can also represent a new evolutionary opportunity by increasing genetic diversity and possibilities of adaptation84.
Conservation guidelines
Allendorf et al.49 proposed hybridization categories that are widely used to prioritize conservation deportment. They considered three categories, but divers differently than ours: (i) sterile hybrids, (ii) widespread introgression, and (3) complete admixture. Indeed, they ignore the effect of fertile hybrids without introgression (hybridization blazon ii), which is the category that may induce faster extinctions. In add-on, they considered the anthropogenic motivation a sine qua non condition to distinguish the conservation bug of hybridization. We highlight here that hybridization, even when induced past humans, is potentially representing a source of genetic variation that could exist useful for conservation purposes.
The nomenclature of Allendorf et al.49 has been employed during the past 20 years, but the wider agreement of hybridization impact brought by more than recent studies allows the states to propose a novel view of conservation priorities (Fig. 2). Given our classification, the conservation priorities are also institute in human-induced hybridization, but this is non the single cut-off to delimit them. Hybridization type ane is a conservation concern when promoting demographic turn down, either because two species with high density-imbalance interbreed or because hybridization amplifies other existing risks80. Hybridization blazon ii is always a threat that may precipitate extinction inside very few generations81. Hybridization blazon 3 is also a priority when affecting fundamental ecological interactions, either by enhancing demographic turn down or because it changes the beliefs of wild individuals84.
Hybridization types ane and 3 should non correspond a priority when they are non triggering demographic pass up or the disruption of ecological functionseighty,84. We suggest that the resources to protect biodiversity may be redirected either to other conservation issues or other threatened organisms. In such conditions, hybridization type 3 may even be used equally a conservation tool to increase genetic multifariousness. However, all of these should be implemented carefully84. The potential fitness loss and the detrimental ecological furnishings of hybridization have offset to exist evaluated, and this is often difficult to achieve. In the offset case, controlled breeding experiments may help to appraise the fertility of hybrids. If this is non possible, monitoring the demography of parental species may help to evaluate a potential fitness loss due to hybridization. A detrimental ecological upshot of hybridization is more difficult to evaluate but the beliefs of hybrids may provide valuable data. Equally an example, in United kingdom, extent hybridization has been registered between Scottish wildcats and domestic cats86, every bit well as between European polecat and feral ferrets87. While the phenotype of Scottish wildcats has been seriously affected86, the polecat phenotype has been much less affected due to hybridization87. In both cases, the increased genetic diversity may take a positive issue in front of irresolute environmental conditions, but the bear upon of hybridization on the behavior of wildcats55, and on the fitness of the polecat population88, deserve more attention before rejecting hybridization every bit a threat or proposing it as a conservation management tool.
Nosotros propose that phylogenetically closer taxa with similar ecological requirements may offer some guidelines for assisted hybridization every bit a tool in conservation. For example, assisted hybrization betwixt subspecies of panthers has promoted the recovery of Florida panthers (Puma concolor coryi) by increasing heterozygosity and decreasing inbreeding, resulting in an overall increase of survival and fitness89. Hybridization between different species has likewise promoted the recovery of American chestnuts (Castanea dentata) through the transfer of pathogen resistance from Chinese chestnuts (C. mollisima)90. In circumstances where organisms are evolutionarily close and share similar ecologies, and when the local species is on the brink of extinction, hybrids may also represent a subject of protection, even when hybridization is caused by anthropogenic factors. An example is the interspecific hybridization betwixt coral reefs, in which the parental species Acropora palmata and A. cervicornis have been in a disquisitional reject over the terminal decades, simply their hybrids (too called A. prolifera) take increased in several locations91. The hybrids have been shown to exist as fit or even more fit than the parental species92. While the parental species are legally protected, protecting hybrids represents a legal challenge, which may help to preserve functional ecosystems otherwise lost with the extinction of the parental species91.
Conclusions
Hybridization that influences both the loss and the cosmos of new biodiversity may seem paradoxical at a first glance. The loss of native biodiversity is certainly an effect related to conservation biology when it is induced past anthropogenic factors under the conditions exposed in Fig. 2. Notwithstanding, hybridization had influenced the evolution of several species of hybrid origins, e.g., refs. 26,31, participating in the creation of novel biodiversity. This is therefore not a real paradox, but an intrinsic property of hybridization, which may drive the extinction of native species and at the same time stimulate the appearance of new species. The conservation guidelines divers here constitute an important framework to understand the ecological and evolutionary consequences of hybridization. The conservation priorities established in Fig. two are not delimitated only past man hyphen induced origins of hybridization, merely by the disruption of fundamental ecological interactions driven by genetic and demographic factors. This highlight that hybridization, even when induced by humans, may also correspond a subject of protection. This nomenclature notably incorporates the outcome of hybridization type 2, which was previously ignored49. We propose that it should be considered every bit a potential highway to extinction, and thus deserves high priority in conservation programmes.
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Acknowledgements
This study was supported by grants from the Swiss National Science Foundation, Nos. 31003A_182577 to M.C., 310030_185327/1 to J.M.B., and P400PB_183930 to C.South.Q. We give thanks two bearding reviewers for their comments and suggestions on an before version of this newspaper.
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C.S.Q., M.C., and J.I.Thousand.B. conceived the original idea. C.South.Q. wrote the first draft of the paper. All authors participated in data analysis and interpretation, and contributed in the class of word and critical comments.
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Quilodrán, C.S., Montoya-Burgos, J.I. & Currat, M. Harmonizing hybridization dissonance in conservation. Commun Biol iii, 391 (2020). https://doi.org/ten.1038/s42003-020-1116-9
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DOI : https://doi.org/10.1038/s42003-020-1116-9
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