Genetic evidence for multiple events of hybridization between wolves and domestic dogs in the Iberian Peninsula

Hybridization between wild species and their domestic counterparts may represent a major threat to natural populations. However, high genetic similarity between the hybridizing taxa makes the detection of hybrids a difficult task and may hinder attempts to assess the impact of hybridization in conservation biology. In this work, we used a combination of 42 autosomal microsatellites together with Y-chromosome microsatellite-defined haplotypes and mtDNA sequences to investigate the occurrence and dynamics of wolf-dog hybridization in the Iberian Peninsula. To do this, we applied a variety of Bayesian analyses and a parallel set of simulation studies to evaluate (i) the differences between Iberian wolves and dogs, (ii) the frequency and geographical distribution of hybridization and (iii) the directionality of hybridization. First, we show that Iberian wolves and dogs form two well-differentiated genetic entities, suggesting that introgressive hybridization is not a widespread phenomenon shaping both gene pools. Second, we found evidence for the existence of hybridization that is apparently restricted to more peripheral and recently expanded wolf populations. Third, we describe compelling evidence suggesting that the dynamics of hybridization in wolf populations is mediated by crosses between male dogs and female wolves. More importantly, the observation of a population showing the occurrence of a continuum of hybrid classes forming mixed packs may indicate that we have underestimated hybridization. If future studies confirm this pattern, then an intriguing avenue of research is to investigate how introgression from free-ranging domestic dogs is enabling wolf populations to adapt to the highly humanized habitats of southern Europe while still maintaining their genetic differentiation.     

Combined use of maternal,paternal and bi-parental genetic markers for the identification of wolf-dog hybrids

The identification of hybrids is often a subject of primary concern for the development of conservation and management strategies, but can be difficult when the hybridizing species are closely related and do not possess diagnostic genetic markers. However, the combined use of mitochondrial DNA (mtDNA), autosomal and Y chromosome genetic markers may allow the identification of hybrids and of the direction of hybridization. We used these three types of markers to genetically characterize one possible wolf-dog hybrid in the endangered Scandinavian wolf population. We first characterized the variability of mtDNA and Y chromosome markers in Scandinavian wolves as well as in neighboring wolf populations and in dogs. While the mtDNA data suggested that the target sample could correspond to a wolf, its Y chromosome type had not been observed before in Scandinavian wolves. We compared the genotype of the target sample at 18 autosomal microsatellite markers with those expected in pure specimens and in hybrids using assignment tests. The combined results led to the conclusion that the animal was a hybrid between a Scandinavian female wolf and a male dog. This finding confirms that inter-specific hybridization between wolves and dogs can occur in natural wolf populations. A possible correlation between hybridization and wolf population density and disturbance deserves further research.     

Y-chromosome microsatellite variation in Italian wolves: A contribution to the study of wolf-dog hybridization patterns

One major concern in wolf (Canis lupus) conservation is the risk of genetic contamination due to crossbreeding with domestic dogs. Although genetic monitoring of wolf populations has become widely used, the behavioural mechanisms involved in wolf-dog hybridization and the detrimental effects of genetic introgression are poorly known. In this study we analysed Y-chromosome microsatellite variation in the recovering Italian wolf population and detected strikingly different allele frequencies between wolves and dogs. Four Y haplotypes were found in 74 analysed male wolves, and all of them were present in a focus wolf population in the Apennines. On the other hand, only 1 haplotype was found in the recolonizing wolf population from the Western Alps. The most common haplotype in a sample of domestic dogs, was also found in 5 wolves, 2 of which revealing a signature of recent hybridization. Moreover, another suspect hybrid carried a private haplotype of possible canine origin. These results give support to the idea that female wolves can breed with male stray dogs in the wild. The Y-chromosome variation in Italian wolves contrasts with the previously observed lack of mitochondrial variation. Further investigations are needed to clarify at what extent historical or recent wolf-dog hybridization events may have contributed to the observed haplotype diversity. In conclusion, the two molecular markers employed in this study represent effective means to trace directional genetic introgression into the wolves male lineage and have the noteworthy advantage of being suitable for analyses on low-quality DNA samples.     

Bucking the Trend in Wolf-Dog Hybridization: First Evidence from Europe of Hybridization between Female Dogs and Male Wolves

Studies on hybridization have proved critical for understanding key evolutionary processes such as speciation and adaptation. However, from the perspective of conservation, hybridization poses a concern, as it can threaten the integrity and fitness of many wild species, including canids. As a result of habitat fragmentation and extensive hunting pressure, gray wolf (Canis lupus) populations have declined dramatically in Europe and elsewhere during recent centuries. Small and fragmented populations have persisted, but often only in the presence of large numbers of dogs, which increase the potential for hybridization and introgression to deleteriously affect wolf populations. Here, we demonstrate hybridization between wolf and dog populations in Estonia and Latvia, and the role of both genders in the hybridization process, using combined analysis of maternal, paternal and biparental genetic markers. Eight animals exhibiting unusual external characteristics for wolves - six from Estonia and two from Latvia - proved to be wolf-dog hybrids. However, one of the hybridization events was extraordinary. Previous field observations and genetic studies have indicated that mating between wolves and dogs is sexually asymmetrical, occurring predominantly between female wolves and male dogs. While this was also the case among the Estonian hybrids, our data revealed the existence of dog mitochondrial genomes in the Latvian hybrids and, together with Y chromosome and autosomal microsatellite data, thus provided the first evidence from Europe of mating between male wolves and female dogs. We discuss patterns of sexual asymmetry in wolf-dog hybridization.     

Perspectives on the Iberian wolf in Portugal: population trends and conservation threats

The Iberian wolf (Canis lupus signatus), an endemic subspecies of the Iberian Peninsula, is endangered in Portugal. Contrary to the rest of Europe, the distribution of this subspecies has been declining in Portugal throughout the twentieth century to the present day. Knowledge of the Iberian wolf in Portugal is limited and this lack of detailed scientific knowledge makes it difficult to evaluate conservation priorities. To fill this gap, we summarize existing knowledge regarding trends and potential threats and provide a perspective on Iberian wolf population trends in Portugal, identifying potential factors modulating such trends. Priorities for research and existing monitoring gaps are presented. Declines are primarily associated with a scarcity of wild prey with consequent livestock predation, and illegal persecution primarily in retaliation for predation on livestock. If these limiting causal factors continue operating, Iberian wolf survival in Portugal is jeopardized. Wolf conservation will benefit from a long-term project including public awareness, scientific research and conservation and management solutions to protect this endangered subspecies. Future research should focus on the mechanisms regulating population size, territory occupancy and interactions with prey species, both domestic and wild.     

Simulating the impact of socio-economic trends on threatened Iberian wolf populations Canis lupus signatus in north-eastern Portugal

The IP4 highway and the new projected road network have been changing the critical Iberian wolf (Canis lupus signatus) habitat in Trás-os-Montes e Alto Douro region (north-eastern Portugal). A holistic stochastic dynamic methodology (SDM) was developed for predicting changes in Iberian wolf population due to the new highways construction, increasing road traffic density and urbanization. The ecological indicators for wolf presence and abundance were estimated indirectly from the density of attacks on livestock. The low density of wild ungulates in the area makes livestock the main source of food for wolves. These indirect ecological indicators and state variables are the underlying database of our SDM model. This model focus on the interactions between conceptually isolated key-components, such as the density of attacks on livestock and changes in habitat conditions, providing some basis to analyse the responses of wolf populations to the environmental scenarios that will characterize the region in the future. The model proposed was preceded by a conventional multivariate statistical procedure (stepwise multiple regression analysis) performed to discriminate the significant relationships between livestock attacks and socio-environmental variables. The holistic parameters of the model were estimated from the results of the statistical treatment and from regional data regarding tendencies within the use of land. The simulation results demonstrate the SDM capability in capturing the trends of this changing region, namely by showing a dramatically decrease of wolf attacks in the region for the next decade.     

To Eat or Not To Eat? The Diet of the Endangered Iberian Wolf (Canis lupus signatus) in a Human-Dominated Landscape in Central Portugal

Livestock predation by large carnivores and their persecution by local communities are major conservation concerns. In order to prevent speculations and reduce conflicts, it is crucial to get detailed and accurate data on predators’ dietary ecology, which is particularly important in human dominated landscapes where livestock densities are high. This is the case of the endangered Iberian wolf in Portugal, an endemic subspecies of the Iberian Peninsula, which has seen its population distribution and abundance decline throughout the 20th century. Accordingly, the diet of the Iberian wolf was analyzed, using scat analysis, in a humanized landscape in central Portugal. From 2011 to 2014, a total of 295 wolf scats were collected from transects distributed throughout the study area, prospected on a monthly basis. Scat analysis indicated a high dependence of Iberian wolf on livestock. Domestic goat predominated the diet (62% of the scats), followed by cow (20%) and sheep (13%); the only wild ungulate present in the scat analysis was the wild boar (4% of the scats). Our results show that even though livestock constitute most part of wolves diet, different livestock species may represent different predation opportunities. We conclude that the high levels of livestock consumption may be a result of low diversity and density of wild ungulates that settles livestock as the only abundant prey for wolves. Our findings help on the understanding of the Iberian wolf feeding ecology and have implications for conflict management strategies. Finally, management implications are discussed and solutions are recommended.     

Genetic and morphological relationships of the Berlenga wall lizard (Podarcis bocagei berlengensis: Lacertidae)

Six biometric characters and 15 electrophoretic loci of three known subspecies of Podarcis bocagei were studied. Contrary to biometric indications, Podarcis bocagei berlengensis showed a closer genetic relationship with Podarcis bocagei carbonelli than with the nominal subspecies. The biometric results were confounded by the relative large size of P. b. berlengensis . Post-glacial colonization from two different areas might explain the greater genetic differentiation between the P. b. bocagei and P. b. carbonelli populations (Nei's D - 0.158 - near the species threshold). It might also explain the known colonization of these two lizards through the islands off the west coast of the Iberian penninsula and their present distributions to the north of (Galicia; Northern Portugal) and to the south of the valley of river Douro (central Portugal, western and Sistema Central), respectively.     

On the path to extinction: Inbreeding and admixture in a declining grey wolf population

Allee effects reduce the viability of small populations in many different ways, which act synergistically to lead populations towards extinction vortexes. The Sierra Morena wolf population, isolated in the south of the Iberian Peninsula and composed of just one or few packs for decades, represents a good example of how diverse threats act additively in very small populations. We sequenced the genome of one of the last wolves identified (and road‐killed) in Sierra Morena and that of another wolf in the Iberian Wolf Captive Breeding Program and compared them with other wolf and dog genomes from around the world (including two previously published genome sequences from northern Iberian wolves). The results showed relatively low overall genetic diversity in Iberian wolves, but diverse population histories including past introgression of dog genes. The Sierra Morena wolf had an extraordinarily high level of inbreeding and long runs of homozygosity, resulting from the long isolation. In addition, about one‐third of the genome was of dog origin. Despite the introgression of dog genes, heterozygosity remained low because of continued inbreeding after several hybridization events. The results thus illustrate the case of a small and isolated wolf population where the low population density may have favoured hybridization and introgression of dog alleles, but continued inbreeding may have resulted in large chromosomal fragments of wolf origin completely disappearing from the population, and being replaced by chromosomal fragments of dog origin. The latest population surveys suggest that this population may have gone extinct.     

Viral gut metagenomics of sympatric wild and domestic canids,and monitoring of viruses: Insights from an endangered wolf population

Animal host–microbe interactions are a relevant concern for wildlife conservation, particularly regarding generalist pathogens, where domestic host species can play a role in the transmission of infectious agents, such as viruses, to wild animals. Knowledge on viral circulation in wild host species is still scarce and can be improved by the recent advent of modern molecular approaches. We aimed to characterize the fecal virome and identify viruses of potential conservation relevance of diarrheic free‐ranging wolves and sympatric domestic dogs from Central Portugal, where a small and threatened wolf population persists in a highly anthropogenically modified landscape. Using viral metagenomics, we screened diarrheic stools collected from wolves (n = 8), feral dogs (n = 4), and pet dogs (n = 6), all collected within wolf range. We detected novel highly divergent viruses as well as known viral pathogens with established effects on population dynamics, including canine distemper virus, a novel bocavirus, and canine minute virus. Furthermore, we performed a 4‐year survey for the six wolf packs comprising this endangered wolf population, screening 93 fecal samples from 36 genetically identified wolves for canine distemper virus and the novel bocavirus, previously identified using our metagenomics approach. Our novel approach using metagenomics for viral screening in noninvasive samples of wolves and dogs has profound implications on the knowledge of both virology and wildlife diseases, establishing a complementary tool to traditional screening methods for the conservation of threatened species.     

Genetic assessment of the Iberian wolf Canis lupus signatus captive breeding program

The main goal of ex situ conservation programs is to improve the chances of long term survival of natural populations by founding and managing captive colonies that can serve as a source of individuals for future reintroductions or to reinforce existing populations. The degree in which a captive breeding program has captured the genetic diversity existing in the source wild population has seldom been evaluated. In this study we evaluate the genetic diversity in wild and captive populations of the Iberian wolf, Canis lupus signatus, in order to assess how much genetic diversity is being preserved in the ongoing ex situ conservation program for this subspecies. A sample of domestic dogs was also included in the analysis for comparison. Seventy-four wolves and 135 dogs were genotyped at 13 unlinked microsatellite loci. The results show that genetic diversity in Iberian wolves is comparable in magnitude to that of other wild populations of gray wolf. Both the wild and the captive Iberian wolf populations have a similarly high genetic diversity indicating that no substantial loss of diversity has occurred in the captive-breeding program. The effective number of founders of the program was estimated as ∼ ∼16, suggesting that all founders in the studbook pedigree were genetically independent. Our results emphasize also the genetic divergence between wolves and domestic dogs and indicate that our set of 13 microsatellite loci provide a powerful diagnostic test to distinguish wolves, dogs and their hybrids.     

The evolutionary history of the allopolyploid Squalius alburnoides (Cyprinidae) complex in the northern Iberian Peninsula

Understanding the population structure, population dynamics and processes that give rise to polyploidy and helps to maintain it is central to our knowledge of the evolution of asexual vertebrates. Previous studies revealed high genetic diversity and several reproductive pathways in the southern populations of the Squalius alburnoides hybrid complex. In contrast, lower genetic variability and the associated limited chance of introducing new genetic combinations may threaten the survival of the northern Mondego populations. We analysed the genetic diversity and structure of nine populations of S. alburnoides in the Iberian Peninsula using microsatellite loci to provide further insights on the evolutionary history of this complex. Special attention was given to the less-studied northern populations (Mondego and Douro basins). Marked population structure, a high frequency of private alleles and a high diversity of some biotypes in the Douro basin indicate that some northern populations may not be at high risk of extinction, contrary to what was expected. The genetic diversity found in the northern Douro populations contradicts the general trend of remarkable genetic impoverishment northwards that occurs in other species and regions. The results indicate the possible existence of a glacial refugium in the Rabaçal River, corroborating findings in other species of this region. Historical events seem to have affected the geographical patterns of genetic variability found among and within the northern and southern populations of this complex and contributed to different patterns of genome composition. Therefore, historical events might have a major role in the long-term persistence of some polyploid hybrid taxa.     

Helminth infracommunity in a maned wolf,Chrysocyon brachyurus,from the humid Chaco,Argentina

Parasitism is an important factor in conservation worldwide, especially for endangered species, as it can affect host populations by reducing growth rates, fecundity and affecting nutritional status. The maned wolf Chrysocyon brachyurus, a near-threatened species, is distributed across different habitats from the south Amazonian forest in Brazil to northern Argentina, Paraguay and eastern Bolivia. Most studies on gastrointestinal parasites in wild maned wolves are based on coprological findings, and there is little information about adult parasites and parasite species richness. Therefore, this study aims to expand the knowledge about the helminth infracommunity of a maned wolf, describe adult parasites, and explore parasitic coinfections. We performed a necropsy of an adult individual found road killed in Chaco province, Argentina. We collected adult worms from subcutaneous tissues, from the right ventricle, kidneys, and intestine. The parasites were morphologically identified as Dirofilaria immitis, Dioctophyma renale and Spirometra sp. respectively. To our knowledge, this is the first record for adults of Dirofilaria immitis in maned wolves. Filarioids were located within the heart as well as in subcutaneous tissues with mature females containing uterine microfilariae; this study also adds C. brachyurus as a new host for Spirometra sp. in Argentina. Considering that the three helminths found herein are zoonotic and that the maned wolf is an endangered canid, it is essential provide baseline information to determine the risk factors involved in the transmission and extend the studies to sympatric wild and domestic canids in the area.     

The genetic legacy of extirpation and re-colonization in Vancouver Island wolves

Hybridization between wild and domestic species is of conservation concern because it can result in the loss of adaptations and/or disappearance of a distinct taxon. Wolves from Vancouver Island, British Columbia (Canada), have been subject to several eradication campaigns during the twentieth century and were considered virtually extirpated between 1950 and 1970. In this study, we use control region mitochondrial DNA sequences and 13 autosomal microsatellite loci to characterize Vancouver Island wolves as well as dogs from British Columbia. We observe a turnover in the haplotypes of wolves sampled before and after the 1950–1970 period, when there was no permanent wolf population on the island, supporting the probable local extinction of wolves on Vancouver Island during this time, followed by re-colonization of the island by wolves from mainland British Columbia. In addition, we report the presence of a domestic dog mtDNA haplotype in three individuals eliminated in 1986 that were morphologically identified as wolves. Here we show that Vancouver Island wolves were also identified as wolves based on autosomal microsatellite data. We attribute the hybridization event to the episodically small size of this population during the re-colonization event. Our results demonstrate that at least one female hybrid offspring, resulting from a cross of a male wolf and a female dog or a female hybrid pet with dog mtDNA, successfully introgressed into the wolf population. No dog mtDNA has been previously reported in a population of wild wolves. Genetic data show that Vancouver Island wolves are distinct from dogs and thus should be recognized as a population of wild wolves. We suggest that the introgression took place due to the Allee effect, specifically a lack of mates when population size was low. Our findings exemplify how small populations are at risk of hybridization.     

Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis

The world's most endangered canid is the Ethiopian wolf Canis simensis , which is found in six isolated areas of the Ethiopian highlands with a total population of no more than 500 individuals. Ethiopian wolf populations are declining due to habitat loss and extermination by humans. Moreover, in at least one population, Ethiopian wolves are sympatric with domestic dogs, which may hybridize with them, compete for food, and act as disease vectors. Using molecular techniques, we address four questions concerning Ethiopian wolves that have conservation implications. First, we determine the relationships of Ethiopian wolves to other wolf-like canids by phylogenetic analysis of 2001 base pairs of mitochondrial DNA (mtDNA) sequence. Our results suggest that the Ethiopian wolf is a distinct species more closely related to gray wolves and coyotes than to any African canid. The mtDNA sequence similarity with gray wolves implies that the Ethiopian wolf may hybridize with domestic dogs, a recent derivative of the gray wolf. We examine this possibility through mtDNA restriction fragment analysis and analysis of nine microsatellite loci in populations of Ethiopian wolves. The results imply that hybridization has occurred between female Ethiopian wolves and male domestic dogs in one population. Finally, we assess levels of variability within and between two Ethiopian wolf populations. Although these closely situated populations are not differentiated, the level of variability in both is low, suggesting long-term effective population sizes of less than a few hundred individuals. We recommend immediate captive breeding of Ethiopian wolves to protect their gene pool from dilution and further loss of genetic variability.     

Phylogeographical insights into the origins of the Squalius alburnoides complex via multiple hybridization events

The origin, the phylogeographical structure and divergence times of hybridrogenetic Squalius alburnoides complex were analysed based on the complete mitochondrial cytochrome b gene (1140 pb). The molecular phylogenetic analyses suggest that the S. alburnoides complex has at least five asexual lineages of independent origin. The events that produced this ancestral hybridization took place over a long period of time. There have been multiple hybridization events throughout time, beginning in the upper Pliocene and probably continuing into the present. Increased humidity caused by climate changes in the Pliocene, along with tectonic lifting and vasculation of the Iberian Peninsula, led to the formation of current river drainages which, in turn, contributed to these hybridization events. We postulate that the Northwestern (Mondego and Douro) and the Southwest (Quarteira) drainages of the Iberian Peninsula delimited the border of the maternal ancestral distribution and that vicariant events led to the disappearance of the maternal ancestor in these regions, leaving today only the hybrid species. Two hypotheses have been suggested to explain the similarities between the mtDNA diversity observed in S. alburnoides and its maternal ancestor (S. pyrenaicus). The first hypothesizes that mtDNA similarity results from the recent extinction of the paternal ancestor, while the other postulates that: 'reconstituted non hybrid males' assumed the place of the extinct bisexual paternal ancestor and produced new hybridizations with S. pyrenaicus females.     

First isolation of Pseudogymnoascus destructans in bats from Portugal

The psychrophilic fungus Pseudogymnoascus destructans (formerly known as Geomyces destructans) is considered the etiological agent of white-nose disease (WND), an emerging disease which affects bats during their hibernation period. This disease is clinically characterized by the growth of a white fungus on muzzle, ears, and wings’ membranes of affected bats. This infection caused the death of several million bats in North America. Conversely, European bats show no evidence of significant mortality occurrences associated with P. destructans colonization. This fungus has been isolated from bats in at least 15 European countries since 2008, but was never before reported in the Iberian Peninsula. This study describes the first case report of P. destructans colonization in bats from Portugal. We isolated P. destructans from three hibernating Myotis blythii (lesser mouse-eared bat) with visual signs of P. destructans colonization, during a routine visit to a mine located in the Trás-os-Montes region, Northern Portugal. M. blythii is one of the rarest bat species in Europe, classified as critically endangered in Portugal. P. destructans was obtained from at least three different parts of the body of each specimen analyzed. The identification of the respective fungal isolates was based on the macroscopic and microscopic characterization of the cultures and confirmed by PCR-based analysis. All nucleotide sequences obtained showed 100 % identity with previous data reported for P. destructans. This new finding improves the current knowledge about the European distribution of P. destructans, which is of great interest for forthcoming studies on the fungus dispersion and impact among bat populations at regional and/or global level.     

Biotic and abiotic factors modulating wild boar relative abundance in Atlantic Spain

The population dynamics of wild ungulates, particularly wild boar (Sus scrofa), are modulated by biotic (e.g. predation) and abiotic (environmental) determinants. Despite the evident potential interference of predation in the environmental patterns of wild boar population abundance, studies including both predation and abiotic factors are scarce. Here, using spatially explicit predictive models, we investigated the effects of habitat features on the relative abundance of wild boar populations and how the abundance of boars is related to frequency of Iberian wolf (Canis lupus signatus; hereafter, wolf) in the area. Wild boar relative abundance was determined by hunting bag statistics, including hunting effort-related variables (in order to avoid problems derived from modeling rates) as covariates, while wolf attacks to livestock were considered as a proxy of wolf frequency in the drive. After modeling, variation partitioning procedures were used to determine the relative importance of each factor and their overlaid effects. Our results showed that wild boar and wolf relative abundances are associated. According to previous knowledge on the wild boar ecology, we found that the species abundance is positively related to the percentage of surface occupied by mature forest and heather providing high food diversity and refuge, but these environmental variables achieved a low explanatory capacity in the models in relation to wolf frequency. The holistic approach followed in this study was attended to open new perspectives for thinking on the wolf-livestock conflict and to adequate wild boar management strategies taking into account hunting interests and natural processes.     

Y‐chromosome evidence supports widespread signatures of three‐species Canis hybridization in eastern North America

There has been considerable discussion on the origin of the red wolf and eastern wolf and their evolution independent of the gray wolf. We analyzed mitochondrial DNA (mtDNA) and a Y‐chromosome intron sequence in combination with Y‐chromosome microsatellites from wolves and coyotes within the range of extensive wolf–coyote hybridization, that is, eastern North America. The detection of divergent Y‐chromosome haplotypes in the historic range of the eastern wolf is concordant with earlier mtDNA findings, and the absence of these haplotypes in western coyotes supports the existence of the North American evolved eastern wolf (Canis lycaon). Having haplotypes observed exclusively in eastern North America as a result of insufficient sampling in the historic range of the coyote or that these lineages subsequently went extinct in western geographies is unlikely given that eastern‐specific mtDNA and Y‐chromosome haplotypes represent lineages divergent from those observed in extant western coyotes. By combining Y‐chromosome and mtDNA distributional patterns, we identified hybrid genomes of eastern wolf, coyote, gray wolf, and potentially dog origin in Canis populations of central and eastern North America. The natural contemporary eastern Canis populations represent an important example of widespread introgression resulting in hybrid genomes across the original C. lycaon range that appears to be facilitated by the eastern wolf acting as a conduit for hybridization. Applying conventional taxonomic nomenclature and species‐based conservation initiatives, particularly in human‐modified landscapes, may be counterproductive to the effective management of these hybrids and fails to consider their evolutionary potential.