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This is an electronic reprint of the original article.  
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Author(s): Astrid Vik Stronen, Jouni Aspi, Romolo Caniglia, Elena Fabbri, Marco Galaverni, 
Raquel Godinho, Laura Kvist, Federica Mattucci, Carsten Nowak, Alina von Thaden 
& Jenni Harmoinen 

Title: Wolf-dog admixture highlights the need for methodological standards and 
multidisciplinary cooperation for effective governance of wild x domestic hybrids 

Year: 2022 

Version: Published version 

Copyright:   The Author(s) 2022 

Rights: CC BY 4.0 

Rights url: http://creativecommons.org/licenses/by/4.0/ 

 
Please cite the original version: 

Vik Stronen A., Aspi J., Caniglia R., Fabbri E., Galaverni M, Godinho R., Kvist L., Mattucci F., Nowak 
C., von Thaden A., Harmoinen J. (2022). Wolf-dog admixture highlights the need for 
methodological standards and multidisciplinary cooperation for effective governance of wild x 
domestic hybrids. Biological Conservation 266, 109467. 
https://doi.org/10.1016/j.biocon.2022.109467. 


Biological Conservation 266 (2022) 109467

Available online 25 January 2022
0006-3207/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Perspective 

Wolf-dog admixture highlights the need for methodological standards and 
multidisciplinary cooperation for effective governance of wild x 
domestic hybrids 

Astrid Vik Stronen a,*,1, Jouni Aspi b, Romolo Caniglia c, Elena Fabbri c, Marco Galaverni d, 
Raquel Godinho e,f, Laura Kvist b, Federica Mattucci c, Carsten Nowak g,h, Alina von Thaden g,h, 
Jenni Harmoinen b,i,**,1 

a Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, 1000 Ljubljana, Slovenia 
b Ecology and Genetics Research Unit, P.O. Box 3000, University of Oulu, 90140 Oulu, Finland 
c Unit for Conservation Genetics (BIO-CGE), Department for the Monitoring and Protection of the Environment and for Biodiversity Conservation, Italian Institute for 
Environmental Protection and Research, Bologna, via Ca' Fornacetta 9, 40064 Ozzano Emilia, Italy 
d Science Area, WWF Italy, Via Po 25/c, 00198 Rome, Italy 
e CIBIO/InBIO, Centro de Investigaҫao em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal 
f Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal 
g Wildlife Genetics Center, Senckenberg Research Institute and Natural History Museum Frankfurt, Clamecystrasse 12, 63571 Gelnhausen, Germany 
h LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt am Main, Germany 
i Natural Resources Institute Finland, Latokartanonkaari 9, 00790 Helsinki, Finland   

A R T I C L E  I N F O   

Keywords: 
Anthropogenic hybridisation 
Canis lupus 
Conservation policy 
Introgression 
Wildlife monitoring 
Wild canid management 

A B S T R A C T   

Hybridisation between wild and domestic taxa raises complex questions for conservation. Genetic advances offer 
new methods for hybrid identification, yet social and cultural factors can influence study design, and the 
interpretation, application, and communication of results. A relevant illustration is hybridisation between do
mestic dogs (Canis lupus familiaris) and wild canids, such as grey wolves (C. lupus). For regional European 
monitoring programs in areas with expanding wolf populations, priorities include shared genetic markers and 
inclusion of all relevant reference populations to ensure dispersing wolves are identified as such and not clas
sified as wolf-dog hybrids, which may cause harmful management decisions. Beyond technical developments, 
hybrid research and conservation management can benefit from improved integration of legal and policy per
spectives, recognition of phenotypic traits as broadly unreliable for identification, and attention to the drivers of, 
and responses to, evolution in human-dominated landscapes. Additionally, the proliferation of unsubstantiated 
reports about hybrids in popular and social media shows that communication based on verified findings of 
hybridisation is essential. Hybridisation requires more constructive discussion on how to balance potentially 
competing conservation objectives, and the integration of multidisciplinary perspectives. These encompass the 
welfare of individual animals and preservation of historical predator-prey relationships. Conservation measures 
centred on preserving the ecological function of wild canids likely offer the most sustainable prospects but 
require improved understanding of the extent to which their behavioural ecology might differ from that of 
hybrids. Accurate genetic identification is required to fill this critical knowledge gap, advance public discourse, 
and initiate relevant conservation actions.   

* Correspondence to: A. V. Stronen, Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, 1000 Ljubljana, Slovenia. 
** Correspondence to: J. Harmoinen, Ecology and Genetics Research Unit, P.O. Box 3000, University of Oulu, 90140 Oulu, Finland. 

E-mail addresses: astrid.stronen@gmail.com (A.V. Stronen), jenni.harmoinen@luke.fi (J. Harmoinen).   
1 Except for the first and final author, all others are listed in alphabetical order. 

Contents lists available at ScienceDirect 

Biological Conservation 

journal homepage: www.elsevier.com/locate/biocon 

https://doi.org/10.1016/j.biocon.2022.109467 
Received 13 July 2021; Received in revised form 23 December 2021; Accepted 15 January 2022   

mailto:astrid.stronen@gmail.com
mailto:jenni.harmoinen@luke.fi
www.sciencedirect.com/science/journal/00063207
https://www.elsevier.com/locate/biocon
https://doi.org/10.1016/j.biocon.2022.109467
https://doi.org/10.1016/j.biocon.2022.109467
https://doi.org/10.1016/j.biocon.2022.109467
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Biological Conservation 266 (2022) 109467

2

1. Introduction 

Hybridisation is a complex evolutionary process which can increase 
the fitness of wild taxa or reduce their survival and long-term persistence 
(e.g., McFarlane and Pemberton, 2019; Quilodrán et al., 2020; Hirashiki 
et al., 2021; Klemme et al., 2021). Hybridisation between wild and 
domestic taxa is nonetheless an increasing concern worldwide, and 
recent genome-wide studies have shown complex spatio-temporal 
hybridisation patterns in several species including Atlantic salmon 
(Salmo salar, Wringe et al., 2018), wild boar (Sus scrofa, Iacolina et al., 
2018), sheep (Ovis sp., Cao et al., 2021), wildcat (Felis silvestris, Mattucci 
et al., 2019), and the dingo (referred to as Canis dingo, C. lupus dingo, or 
C. familiaris, van Eeden et al., 2019; Crowther et al., 2020). Human- 
induced (anthropogenic) hybridisation generates difficult questions for 
conservation and management, including forensic, legal, and policy is
sues (Trouwborst, 2014; Amorim et al., 2020; Salvatori et al., 2020; 
Cairns et al., 2021a). Associated human-wildlife conflicts raise ethical 
concerns about wildlife control (Dubois et al., 2017; van Eeden et al., 
2019) and protection of individual animals versus populations (Dubois 
et al., 2017; Wallach et al., 2018; Callen et al., 2020). The study of 
natural and anthropogenic hybridisation also involves complex and 
rapidly advancing topics in evolutionary research (vonHoldt et al., 
2018; Senn et al., 2019; Stanton et al., 2019; Taylor and Larson, 2019) 
that are often demanding for public outreach and science 
communication. 

A prerequisite for navigating the intricate and interdisciplinary 
questions around anthropogenic hybridisation is the ability to accu
rately identify wild-domestic hybrid individuals (McFarlane and Pem
berton, 2019). Monitoring of genetic introgression typically becomes 
increasingly difficult with the time since hybridisation, but, at mini
mum, it is essential to identify the first generation of hybrids (henceforth 
F1) and the first generation of their backcrosses to wild parental taxa 
(BC1). There is an urgent need for standardised methods of hybrid as
signments that are open for peer-review by independent scientists and 

can be implemented across national borders to help design conservation 
management plans at relevant scales, and that can help advance further 
research such as study of hybrid behavioural ecology. 

A good illustration of the problem with anthropogenic hybridisation 
is the situation for grey wolves (hereafter wolves, C. lupus, Pilot et al., 
2018). In recent decades, wolves have recovered parts of their historical 
range across Europe (Chapron et al., 2014), recolonising even strongly 
human-altered environments (e.g., Schley et al., 2021). The recent 
availability of entire genomes of both wolves and domestic dogs (C. l. 
familiaris or C. familiaris), which descend from – and hybridise with – 
wolves, has produced new insights about the timing and diffusion of 
wolf-dog hybridisation (e.g., Galaverni et al., 2017; Pilot et al., 2018; 
Fig. 1). Genome-wide analyses have found wolf-dog hybridisation to be 
recurrent on multiple timescales, albeit with considerable regional 
variation (see e.g., Smeds et al., 2021; Stenøien et al., 2021), and wolf 
populations generally appear to have retained their genetic integrity 
(Pilot et al., 2018). Whereas genomic analyses indicate historical gene 
flow across the genus Canis (Gopalakrishnan et al., 2018), ongoing 
anthropogenic hybridisation is nonetheless deemed a serious threat to 
wolves (Hindrikson et al., 2017). There is therefore increasing attention 
toward the need for consistent management actions to reduce the 
prevalence of free-ranging dogs and wolf-dog hybrids (Salvatori et al., 
2020), particularly for populations in southern and parts of eastern 
Europe, where feral and free-ranging dogs are widespread (Boitani et al., 
2015). 

The objective of this perspective article is to discuss technical, 
analytical, and societal factors of relevance for hybridisation. We reflect 
on areas where more interdisciplinary collaboration can help promote 
an evolutionary enlightened (sensu Ashley et al., 2003) and practical 
direction forward, with focus on conserving the ecosystem role of wild 
canids such as wolves and other wildlife species in human-dominated 
landscapes. We first consider possible ecological and evolutionary con
sequences, and next address different methodological, governance, and 
communication aspects likely to influence how society defines and 

Fig. 1. The problem of wolf-dog hybridisation requires improved genetic monitoring tools, but also prompt conservation management actions. This image shows one 
of the hybrid individuals identified in the central Apennines, Italy, and captured during the LIFE M.I.R.CO-Lupo project. Photo credit: Marco Antonelli. 

A.V. Stronen et al.                                                                                                                                                                                                                              


Biological Conservation 266 (2022) 109467

3

responds to anthropogenic hybridisation. 

2. Potential ecological and evolutionary consequences of 
hybridisation 

Below we discuss how co-dependent influences on behaviour and 
ecological function in human-dominated areas, and a possible cycle of 
reinforcement, or ‘hybridisation vortex’, might affect wolf evolution. 
Although speculative, this discussion addresses potential long-term ef
fects on predator-prey relationships. Preserving these relationships will 
require thoughtful conservation management, centred on how wolves 
and other large carnivores can continue to maintain their ecological 
function in increasingly anthropogenic landscapes. 

2.1. Ecological function 

Increased hybridisation between wolves and domestic dogs could 
influence ecological function, if the process results in a canid less suited 
to the role wolves have historically played as social predators of large 
ungulates, hunting by pursuit. Predators that shift from hunting live 
prey toward persisting on anthropogenic food sources and scavenging 
could be affected in multiple ways, including changes in territoriality, 
life history, and individual traits such as boldness and innovation 
(reviewed in Parsons et al., 2021). Human provision of food sources can 
limit the motivation of wolves to hunt, which may reduce historical 
selection pressures and favour more dog-like canids (Ordiz et al., 2013; 
Ciucci et al., 2020). Conversely, maintaining selective forces that pro
mote the ecological role of large predators hunting in social groups 
could be vital in preserving long-term ecological function (Pilot et al., 
2018), although more empirical research is needed to address these 
different hypotheses. At present, little is known about the general 
ecology and behaviour of wolf-dog hybrids (Lescureux and Linnell, 
2014; Pilot et al., 2018), but the ecological role of hybrids is receiving 
more attention. A first study indicated no significant differences in diet 
composition compared to that of wolves (Bassi et al., 2017), and similar 
results have been reported for dingoes affected by domestic dog intro
gression (Crowther et al., 2020). Yet domestic dogs may not have the 
same ability to persist in remote areas without access to anthropogenic 
resources (Cairns et al., 2021a). Dingoes have been found to play a major 
ecological role by suppressing mesopredators and promoting the con
servation of native small mammals (Letnic et al., 2009a, 2009b), and 
may thus provide key ecosystem services (Colman et al., 2014; van 
Eeden et al., 2020). As hybridisation is a particular concern for small 
populations (Muñoz-Fuentes et al., 2010) there is an urgent need for 
more data on these topics, although such research might inherently 
present difficult legal and ethical questions. 

2.2. Bold behaviour 

If dog-like hybrids are allowed to persist and increase in abundance, 
a central question is whether they may become more dependent on 
human resources and show bolder behaviour near humans. Potential 
bold behaviour could also occur in the vicinity of domestic animals, 
refuse sites, and in localities where humans approach animals to provide 
them with food. Such situations could result in negative long-term 
consequences for wolf-human relations (Linnell et al., 2008). Recent 
findings have suggested that human-directed selection for sociability in 
dogs may have influenced several linked behavioural genes (vonHoldt 
et al., 2017), and behavioural or cognitive traits derived from dogs could 
benefit wolves (Pilot et al., 2021). Yet, whether selection may favour 
dog vs. wolf genes in shaping hybrid behaviour will need further study in 
environments with various types of prey, ecological conditions, and 
degrees of human influence. A recent European Court of Justice decision 
(C-88/19) confirmed that the strict protection of species listed in the 
European Union's Habitats Directive Annex IV (a), including wolves, 
also applies to individuals that stray into human settlements (Curia, 

2020). Albeit important, this clarification of protection may amplify 
negative human attitudes toward free roaming canids (both wild and 
hybrids), potentially further elevating human-caused mortality, 
disruption of social structure, and the prevalence of hybridisation, and 
highlights the need to accurately identify hybrids and investigate their 
behaviour. 

2.3. Hybridisation vortex 

Earlier findings suggest that the loss of breeding members may 
contribute to the break-up of wolf packs (Brainerd et al., 2008), and 
human-caused mortality and high population turnover can disrupt the 
social structure of wild canids and augment hybridisation (Wallach 
et al., 2009; Rutledge et al., 2012; Leonard et al., 2014; Randi et al., 
2014; Cairns et al., 2021a). If human-caused mortality increases, this 
could augment hybridisation and generate further lethal control (van 
Eeden et al., 2019), thereby hampering the ecological function of wild 
canids. Such a scenario might produce a negative spiral – a hybridisation 
vortex – parallel to the extinction vortex described for populations at 
risk and supported by analyses across taxa (Fagan and Holmes, 2006). 
Such scenarios have also been described as ‘extinction via hybridisation’ 
(Rhymer and Simberloff, 1996). Although the process could result in a 
canid better-adapted to current human-dominated habitats (Newsome 
et al., 2017), the disruption of the ecological and evolutionary re
lationships between wolves and their large ungulate prey would repre
sent a major loss for the ecosystem (Ripple et al., 2014). 

3. Defining and responding to hybridisation 

Reliable detection of hybrids and admixture patterns are essential, as 
hybridisation and subsequent introgression of domestic genetic varia
tion into wildlife could have serious implications for long-term 
ecosystem conservation and human-wildlife relationships. Yet other 
concerns around hybridisation are not simply technical challenges, but 
instead require attention to human dimensions and communication. 
Despite recent technical progress, careful study design and data analyses 
are needed to produce meaningful results, which must (still) be inter
preted with caution, especially for species that are known as long- 
distance dispersers (e.g., Wabakken et al., 2007). We discuss methodo
logical issues and solutions, and then societal, governance, and 
communication aspects likely to be important for a balanced and sus
tainable response to anthropogenic hybridisation. 

3.1. Methodological considerations 

3.1.1. Standardising and sharing genetic markers and data 
National genetic monitoring programs for wildlife have traditionally 

employed microsatellite genetic markers, where the responsible orga
nisations have accumulated multi-year databases that provide context 
for spatio-temporal analyses on the status of local populations. However, 
integration of standard microsatellite genotypes across different labo
ratories and countries requires calibration, which is costly and time 
consuming. This extra step can impede timely conservation manage
ment, especially for species that disperse over long distances and na
tional boundaries, although this limitation can be alleviated by the 
exchange of reference samples among laboratories, to help identify 
dispersing individuals and their origin. Recent work on high-throughput 
sequencing of microsatellite markers (De Barba et al., 2017) and single 
nucleotide polymorphism (SNP) panels (e.g., Kraus et al., 2015) suitable 
for non-invasively collected samples have provided important ad
vancements (von Thaden et al., 2017). These new markers do not 
require calibration among laboratories, although it is important to 
mention that not all markers developed for specific populations will be 
suitable (i.e., polymorphic) in other populations (Giangregorio et al., 
2019). 

The detection of wolf-dog hybridisation has nevertheless continued 

A.V. Stronen et al.                                                                                                                                                                                                                              


Biological Conservation 266 (2022) 109467

4

to be a problem for monitoring efforts. However, in a recent study, 
Harmoinen et al. (2021) designed a panel of 96 SNP loci selected for 
their power to distinguish between dogs and wolves across Europe, 
suitable for DNA from non-invasively collected samples that are the 
typical source of data for monitoring programs. The panel of diagnostic 
SNPs provides standardisation in analyses and reporting, which will 
help resolve cases of putative hybridisation and determine the distri
bution and prevalence of hybridisation across the continent. 

3.1.2. Inclusion of relevant reference populations and documentation of 
analytical parameters 

Highly mobile species often cross jurisdictional and management 
borders, a situation which has important implications for regional and 
national monitoring programs. For genetic analyses of wolves and other 
species affected by anthropogenic hybridisation (e.g., wild boar; Iaco
lina et al., 2018; wildcat; Tiesmeyer et al., 2020), it is thus vital to 
include reference samples from all putative source populations. This will 
help ensure that dispersers are correctly identified, and that they and 
their descendants are not erroneously classified as hybrids (Harmoinen 
et al., 2021). Such errors can occur because wild canids and dogs have 
very similar genomic backgrounds that mostly differ in the frequency of 
the genetic variants (alleles). In principle, the new European diagnostic 
SNP panel for wolf-dog hybridisation eliminates the need for regional 
reference samples in hybrid identification, because the panel was 
designed and successfully tested across European populations (Har
moinen et al., 2021). However, monitoring programs in many regions 
still rely on traditional microsatellite markers. In addition to being well- 
established in local labs, these traditional markers provide a valued 
temporal connection in areas where older DNA sources have been 
exhausted and legacy data exist only as microsatellite profiles. Here, 
reference samples from local wolves and dogs, and, crucially, neigh
bouring wolf populations with different allelic frequencies, should be 
included to ensure that dispersing wolves are not accidentally mis
classified as wolf-dog hybrids. 

Population structure and geographic variation have been suggested 
as possible confounding factors in analyses of dingo-dog hybridisation 
(reviewed in van Eeden et al., 2019 and Crowther et al., 2020). Accurate 
detection of population structure and dispersers is also increasingly 
relevant for wolves, which are recolonising their historical ranges across 
Europe where their populations continue to reconnect (Ražen et al., 
2016; Hulva et al., 2018; Szewczyk et al., 2019). For example, wolves 
from the long-isolated and genetically divergent Italian population have 
recently dispersed into nearby countries including Slovenia, 
Switzerland, and Germany (Bartol et al., 2018; Dufresnes et al., 2019; 
Harmoinen et al., 2021). Reference samples from Italy and other distinct 
wolf populations are thus needed where dispersers are found, or may 
appear, in the future, and will aid monitoring programs in categorising 
local and dispersing wolves. Any unresolved profiles can then be geno
typed on the diagnostic SNP panel to investigate possible hybrid 
ancestry. Although genetic analysis costs for hybrid detection may be a 
concern (e.g., Dziech, 2021), genotyping of samples on the reduced 
panel is cost-effective (around 8 €/sample for high-quality tissue sam
ples and 24 € considering three replicates per sample for non-invasively 
collected samples, not considering working costs, taxes, initial costs for 
machine acquisition and maintenance (von Thaden et al., 2017, 2020). 

Moreover, various other steps can limit bias on inferred admixture 
proportions in population analyses, including equalised sample sizes 
(Toyama et al., 2020) and estimators accounting for uneven sample sizes 
(Puechmaille, 2016). Reference population allele frequencies should 
also be representative and updated where needed, especially for 
expanding populations (Caniglia et al., 2020). Natural long-distance 
dispersal is considered essential for the viability of small, isolated pop
ulations, but many long-distance dispersers die before reproducing in 
their new home range (Kojola et al., 2006; Bartoń et al., 2019). Correct 
identification of dispersers is thus of great practical importance for 
conservation. Conversely, studies that include neither relevant reference 

populations nor transparent reporting on reference populations and 
methods used may create confusion about scientific results. Such cases 
could reduce public trust in science and management, and limit 
constructive scientific and public discourse on how to address long-term 
consequences of human-induced hybridisation. 

3.2. Governance and societal issues 

3.2.1. Hybrid definition and management: Integration of scientific, legal, 
and policy perspectives 

The definition of hybrid is relevant for legal and conservation man
agement (van Eeden et al., 2019; Amorim et al., 2020; Dziech, 2021) and 
requires integration of genetic and legal information. Importantly, this 
definition may differ from the long temporal perspective often consid
ered in evolutionary research (e.g., Galaverni et al., 2017; Schweizer 
et al., 2018) and must focus on achieving effective conservation out
comes (Lorenzini et al., 2014; Senn et al., 2019; Salvatori et al., 2020; 
Cairns et al., 2021a). For example, backcrosses into wolf populations 
may in some instances be too difficult to detect and too abundant to 
allow their effective removal (Wayne and Shaffer, 2016; Salvatori et al., 
2019). The ability to detect hybridisation at increasing levels of reso
lution amplifies the normative challenges surrounding policies for 
conservation management, such as the level at which individuals – 
including those with traces of historical introgression – should be 
considered for protection under existing wildlife and habitat legislation 
(Wayne and Shaffer, 2016; Galaverni et al., 2017; Senn et al., 2019). 
Findings from Australia also suggested that used of the term ‘wild dog’ 
may have confounded members of the public about management actions 
that also affect dingoes and the ecosystem services they provide as apex 
predators (van Eeden et al., 2020), underscoring the importance of 
language and communication in wildlife management. Although hy
brids are not typically addressed in international conservation legisla
tion, wild-living wolf-dog hybrids appear to be protected by legal 
frameworks such as the European Union's Habitat Directive and the Bern 
Convention on European Wildlife and Natural Habitats (Trouwborst, 
2014). Trouwborst (2014) stated that although preventive measures to 
address hybridisation seem to be permitted under these frameworks and 
may even be required, it is not fully clear whether hybrids that present a 
potential threat to wolf populations could be managed in an effective 
and consistent manner. It would seem a priority to ensure good inte
gration of legal and genetic considerations, and to assure that hybrid 
regulations and guidelines reflect categories that genetic analyses can 
realistically achieve. Trouwborst (2014) noted that according to CITES 
guidelines, the protection of wolves also covers wolf-dog hybrids with 
wolf ancestry within the last four generations (backcrosses to dogs), 
although this level of ancestry can be difficult to discern even with high- 
density genome-wide profiles (Galaverni et al., 2017; Pilot et al., 2018). 
Moreover, although second and third backcrosses to wolves (BC2, BC3) 
were in most instances detectable with the Europe-wide 96-SNP panel – 
and conservation management is generally concerned with backcrosses 
to wolves or other wild species, not to their domestic counterparts – 
reliable detection of all individuals with wolf ancestry within the last 
four generations is not currently feasible (Harmoinen et al., 2021). If we 
cannot clearly discern the number of hybrid generations identified in 
legal and management guidelines, there is a mismatch in law and 
practical feasibility that may confound and limit conservation decisions. 
Focusing hybrid management guidelines on the recent-generations such 
as F1 and BC1wolf that have higher potential to spread dog genetic 
variants than back-crossed individuals with more limited dog ancestry 
(BC2wolf and beyond), could be a practical objective at the current state 
of the art (Caniglia et al., 2020). If advances in routine genetic methods 
can improve resolution in the future, guidelines could later be updated 
to allow implementation of new knowledge. 

3.2.2. Phenotypic traits in hybrids 
Findings from several taxa suggest that possible individual 

A.V. Stronen et al.                                                                                                                                                                                                                              


Biological Conservation 266 (2022) 109467

5

phenotypic and genetic indicators of hybridisation often differ (Iacolina 
et al., 2018; Kusak et al., 2018; Senn et al., 2019; Cairns et al., 2021b). 
Dingoes, for instance, showed a wide variation in coat colour and it was 
not possible to evaluate hybrid ancestry based on this trait, where 
certain unusual patterns also appear to be ancestral variants (Cairns 
et al., 2021b). In wolves, some individual phenotypic differences may 
simply represent natural variation in morphology, such as the presence 
of a black stripe on the foreleg (Pulliainen, 1965). In contrast, other 
traits have been associated with hybridisation or ancient introgression, 
exemplified by black coat colour (Anderson et al., 2009; Galaverni et al., 
2017). Importantly, genome-wide analyses of Italian canids show that 
black coat colour can occur in individuals assigned as hybrids and in 
individuals fully assigned to wolves (Galaverni et al., 2017). Although 
often unreliable on their own as indicators of hybridisation (Lorenzini 
et al., 2014), phenotypic traits might help identify priority areas for 
more detailed investigation of hybridisation, e.g., by camera-trapping. 
Areas where individuals with atypical phenotypic traits are observed 
can then be prioritised for non-invasive genetic monitoring. Another 
important outcome of such research is to understand whether certain 
phenotypic traits are not useful hybrid indicators for conservation 
management, but unreliable measures that risk producing harmful de
cisions (Galaverni et al., 2017; Cairns et al., 2021b). Moreover, the 
persistence of traits such as black coat colour in canids with genome- 
wide profiles fully assigned to wolves can offer insights about environ
mental selection and ecological function following introgression. An 
allele at the CBD103 gene in wolves, derived from historical wolf-dog 
hybridisation, is associated with black coat colour and immune func
tion (Schweizer et al., 2018), thus illustrating a situation where 
hybridisation and subsequent introgression may have provided fitness 
benefits. 

3.2.3. Identify drivers of, and responses to, evolution in anthropogenic 
landscapes 

Hybridisation can represent both fitness gains and costs for wild 
species (e.g., vonHoldt et al., 2018; McFarlane and Pemberton, 2019; 
Quilodrán et al., 2020; Dziech, 2021) and these effects may occur 
simultaneously, suggesting complex effects that are still poorly under
stood (Klemme et al., 2021). Although hybridisation is typically 
considered to have detrimental effects on the ecological function of 
wolves, introgression from dogs or other canids better adapted to 
human-dominated landscapes might, at times, increase survival and 
permit the use of additional habitats (Coulson et al., 2011; Godinho 
et al., 2011; Lescureux and Linnell, 2014). Notably, Schweizer et al. 
(2016) reported signs of selection in wolf ecotypes linked to diet and 
metabolism, and several dog breeds appear to have adaptations toward a 
diet rich in starch (Axelsson et al., 2013; Arendt et al., 2016). Such 
adaptations, if transferred to wolves, might promote wolf survival in 
habitats where animals depend increasingly on human-provided re
sources, but could thereby also augment human-wildlife conflicts. 
Another question concerns the extent to which ecological differences 
between wolves and wolf-dog hybrids might be observed in areas with 
medium-sized or large ungulates, which are typical prey species for 
wolves in many regions. Here, selection may favour larger individuals 
(MacNulty et al., 2009) and more wolf-like phenotypes. Similarly, few 
wild-living domestic dogs were reported in the arid interior of Australia, 
where environmental conditions may favour dingoes (Cairns et al., 
2021a). Natural selection based on historical ecological function could 
help restore wild phenotypes and genotypes (Pilot et al., 2018) and such 
a process might co-occur with selection on the immune system. For 
example, in response to canine distemper virus (Schweizer et al., 2018) 
or resistance against infectious disease associated with human impacts, 
such as canine parvovirus, which was first detected in dogs some de
cades ago and has since spread to other carnivore species (Allison et al., 
2013). Carefully designed studies and targeted genetic markers could 
help clarify how the genomes of wild canids and hybrids respond to such 
diverse evolutionary forces. The amount of habitat needed to ensure 

long-term sustainable populations of large carnivores may require them 
to occupy areas used by humans to various extent, and thereby adapt to 
some level of human presence throughout portions of their range (Carter 
and Linnell, 2016; López-Bao et al., 2017). Further investigations are 
needed across various environments, including southern and south- 
eastern Europe where high numbers of free-ranging dogs share their 
environments with wolves (Galaverni et al., 2017; Salvatori et al., 2020) 
and where dog-jackal hybridisation has also been confirmed (Galov 
et al., 2015). Parallel concerns exist in other areas where wild canids 
hybridise with dogs, including Africa (Mallil et al., 2020), and Australia 
(Claridge et al., 2014). 

3.2.4. Promote communication of peer-reviewed scientific findings 
The publication of genetic findings is frequently done in specialised 

journals behind paywalls, and articles include technical language that is 
often poorly accessible to non-scientists (or non-geneticists). This can 
make peer-reviewed scientific results difficult to access on several levels. 
In contrast, claims and reports of hybrids are at times offered high- 
profile publication in the media, even if based on unverified sources 
rather than results that have been subject to (or have been submitted for) 
peer-review by independent scientists. Such cases are deeply problem
atic, given the potential for management actions based on erroneous 
results, and because dissemination of erroneous results can create 
persistent public perceptions that can be difficult to reverse (Pivetti 
et al., 2020). For all laboratories involved in hybrid analysis, we 
therefore advocate for the use of standardised scientific techniques for 
investigating and reporting new cases, and peer-review publication of 
results where methodological details – including choices of reference 
populations, and discussion of possible limiting factors (e.g., sample 
quality and sample size) – are included in the research description. 
Where financial resources are available, open-access publication is 
recommended to promote scientific outreach, although the long pro
cessing time for peer-reviewed scientific literature remains a challenge 
for scientists, conservation managers, and dissemination of scientific 
results to the public and various interest groups. Yet, where possible, we 
encourage journalists writing popular articles about research on 
anthropogenic hybridisation to provide links to the original peer- 
reviewed scientific studies, to pre-print results awaiting such appraisal 
(see e.g., https://www.biorxiv.org/), or a note stating that the reported 
findings have not yet been subject to peer-review. Similarly, we 
encourage readers to consider such contextual information – or the lack 
thereof – before citing or (re)publishing reports of hybridisation, for 
example on social media. Social media coverage about carnivores is 
often focused on sensationalistic reports that can increase sharing but 
might also increase fear and reduce support for conservation, under
lining the need to disseminate more accurate and objective information 
(Nanni et al., 2020). 

3.2.5. Encourage constructive discussion while targeting changes in human 
behaviour 

The risks that hybrids and feral domestic animals may present to the 
genetic makeup, ecological function, and evolution of wild taxa, and the 
extent to which humans should mitigate human-induced hybridisation 
have been subject to extensive discussions (e.g., Wallach et al., 2018; 
Callen et al., 2020). These have highlighted ethical questions around 
possible sterilisation, capture, or killing of individuals (animal control) 
to advance conservation goals and offered insights on the – often con
flicting – societal aims in setting conservation objectives, and how we 
can start changing human behaviour to promote sustainable solutions 
(Dubois et al., 2017; Donfrancesco et al., 2019; Cairns et al., 2021a). For 
hybridisation, tackling the underlying problem of free-ranging dogs is 
fundamental to achieving meaningful long-term change (Lorenzini 
et al., 2014; Donfrancesco et al., 2019). However, addressing this critical 
step has frequently been avoided by conservation managers because of 
the – frequently complex – legal framework regarding domestic animals, 
and the risk of invoking strong ethical and emotional questions 

A.V. Stronen et al.                                                                                                                                                                                                                              

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6

(Donfrancesco et al., 2019). Efforts to control animals should be done on 
a case-by-case basis and only after consideration of all available options 
(Dubois et al., 2017), also for the removal of hybrids or their repro
ductive potential (Donfrancesco et al., 2019; Caniglia et al., 2020). 
Crucially, it is recognised that not taking action on hybrids and abundant 
feral animals also entails important risks (Callen et al., 2020; Salvatori 
et al., 2020). Typically, there is no uniform answer but a need to tailor 
solutions to local circumstances, and acceptance for hybrid removal may 
depend on the specific conservation context, local laws, and human 
attitudes (Lescureux and Linnell, 2014; Fitzpatrick et al., 2015; Wayne 
and Shaffer, 2016; Donfrancesco et al., 2019; Caniglia et al., 2020). 
Public sentiment toward hybrids may influence how policies are 
implemented, and managers need to consider the practical realities of 
public response to, and enforcement of, species-based or other ecolog
ical protections (Fitzpatrick et al., 2015; van Eeden et al., 2019). A 
reliable and commonly agreed-upon protocol for genetic analyses is the 
basis for a scientific assessment (Donfrancesco et al., 2019), and we 
contend that this step is critical for the subsequent decision processes 
that may involve scientists, conservation managers, NGOs, and other 
public interest groups. However, there are currently no commonly 
accepted best practices for how to manage hybrids and the surrounding 
debate is often highly emotional (Lescureux and Linnell, 2014; Don
francesco et al., 2019). This is also why the spread of any incorrect 
claims about hybridisation can be so detrimental for conservation ef
forts, and why accurate scientific data, including standardised genetic 
identification, is needed for meaningful discussion, prioritisation of re
sources, and broadly supported conservation actions. 

3.2.6. Integration of multidisciplinary perspectives 
Long-term efforts to mitigate hybridisation need to involve collabo

ration across disciplines, to address technical, ethical, legal, ecological, 
and evolutionary aspects and adapt these to local circumstances. 
Important priorities include (a) conserving the ecological function of 
wolves and other wild canids, and (b) limiting the proliferation of free- 
ranging dogs. Another key priority is to (c) better understand hybrid 
behaviour, especially whether hybrid ecological function and behaviour 
toward humans and livestock may differ from that of wolves. This 
research will need to be achieved while balancing many concerns, 
including how to best spend scarce conservation resources while 
obtaining essential data to inform hybrid management. In certain areas, 
returning hybrids that are collared and sterilised (i.e., retaining hor
monal functions and social behaviour) to the wild might offer important 
insights into their interactions with humans, domestic animals, and wild 
prey species, while assisting conservation managers in protecting 
vulnerable populations of wolves and other wild canids. Results from a 
recent project in Italy suggested that sterilisation and release of hybrids 
did not appear to affect their ability to re-join their original pack (LIFE 
M.I.R.CO-Lupo, 2020). 

In the red wolf (C. rufus) recovery program in the US, sterilised hy
brids between coyotes (C. latrans) and red wolves have been released 
and managed as ‘placeholder packs’, thereby acting as a buffer around 
red wolf packs to discourage hybridisation (Gese and Terletzky, 2015). 
Although this intervention concerns hybridisation between wild species, 
the conservation management context would be similar for wolf-dog 
hybrids. Such invasive procedures toward animals may encounter 
considerable objections. On the other hand, the current management 
response in several European countries is lethal removal of wolf-dog 
hybrids to prevent further introgression, although certain jurisdictions 
have contemplated and/or used sterilisation and release (Salvatori et al., 
2020 Table 2). Mitigation of hybridisation will need to consider national 
and regional legislation, wolf population size and conservation status, 
economic costs, and social attitudes (Donfrancesco et al., 2019; van 
Eeden et al., 2019; Caniglia et al., 2020). Local environmental factors 
are also essential for understanding why hybridisation is occurring in the 
first place. The focus must be on changing human activities that lead to 
animal control (Dubois et al., 2017) and avoiding makeshift solutions 

whereby we kill or manipulate animals without addressing the under
lying problems. As with the complex questions surrounding genetic 
management of threatened species (e.g., Liddell et al., 2021), there is 
probably no ideal and universal solution to anthropogenic hybridisation. 
The best (or least undesirable) outcome with broad support is therefore 
likely to be achieved by including local environmental knowledge and 
perspectives from diverse disciplines. 

3.3. Conclusion 

Whereas hybridisation in wild canids may represent an extreme 
showcase for conservation management in terms of their high public 
profile and broad geographic distribution, they offer a good example 
given that future environmental changes and species range shifts are 
expected to augment hybridisation (Scheffers et al., 2016). Mitigation of 
hybridisation caused or influenced by human activities may therefore 
increasingly require international collaboration across disciplines. 
Humans must impose a management boundary on what is an evolu
tionary gradient of wild-domestic hybridisation, and decisions may vary 
depending on perceived cost-benefits for conservation and the feasibility 
of removing hybrids or their reproductive potential without negative 
consequences for local ecosystems, while ensuring social acceptance 
(Allendorf et al., 2001; Lescureux and Linnell, 2014; Fitzpatrick et al., 
2015; Wayne and Shaffer, 2016). Conservation strategies are more likely 
to succeed where they focus on ecological function over genetic purity 
(Claridge et al., 2014; Fitzpatrick et al., 2015; Quilodrán et al., 2020). 
Actions that help maintain natural social structure in wild canids, and 
their historical ecological role as top predators, could therefore help 
wild populations resist or limit introgression (Rutledge et al., 2012; 
Galaverni et al., 2017; Cairns et al., 2021a). 

Although genetic methods and the resolution of individual genomic 
profiles have seen rapid advances, improved resolution of hybrid pro
files in the future will only shift, not eliminate, the conservation decision 
processes. As a starting point, we propose the use of standardised, 
shared, and transparent genetic methods, and further international 
collaboration across disciplines. These important steps will help ensure 
that genetic analyses of wide-ranging species, intraspecific genetic lin
eages and populations can distinguish (I) recent wild-domestic hybrids 
from (II) introgressed individuals that carry limited amounts of histor
ical domestic ancestry, and (III) immigrant individuals and their 
offspring with admixed ancestry from divergent wild populations. 

Declaration of competing interest 

The authors declare that they have no known competing financial 
interests or personal relationships that could have appeared to influence 
the work reported in this paper. 

Acknowledgements 

R.G. was supported by the Portuguese Foundation for Science and 
Technology, FCT. A.V.T. received partial funding by the Karl und Marie 
Schack-Stiftung. 

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	Vik Stronen et al 2021.pdf
	1-s2.0-S0006320722000209-main
	Wolf-dog admixture highlights the need for methodological standards and multidisciplinary cooperation for effective governa ...
	1 Introduction
	2 Potential ecological and evolutionary consequences of hybridisation
	2.1 Ecological function
	2.2 Bold behaviour
	2.3 Hybridisation vortex

	3 Defining and responding to hybridisation
	3.1 Methodological considerations
	3.1.1 Standardising and sharing genetic markers and data
	3.1.2 Inclusion of relevant reference populations and documentation of analytical parameters

	3.2 Governance and societal issues
	3.2.1 Hybrid definition and management: Integration of scientific, legal, and policy perspectives
	3.2.2 Phenotypic traits in hybrids
	3.2.3 Identify drivers of, and responses to, evolution in anthropogenic landscapes
	3.2.4 Promote communication of peer-reviewed scientific findings
	3.2.5 Encourage constructive discussion while targeting changes in human behaviour
	3.2.6 Integration of multidisciplinary perspectives

	3.3 Conclusion

	Declaration of competing interest
	Acknowledgements
	References