![Relative frequencies of (a) orders represented in 115 papers included in the systematic review, (b) orders represented across all currently recognized mammalian species [62] and (c) families represented in 115 papers included in the systematic review.](https://www.researchgate.net/publication/357348403/figure/fig2/AS:1105611982938112@1640609846284/Relative-frequencies-of-a-orders-represented-in-115-papers-included-in-the-systematic_Q320.jpg)
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Citation: Adavoudi, R.; Pilot, M.
Consequences of Hybridization in
Mammals: A Systematic Review.
Genes 2022,13, 50. https://doi.org/
10.3390/genes13010050
Academic Editor: Arne Ludwig
Received: 12 November 2021
Accepted: 20 December 2021
Published: 24 December 2021
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genes
G C A T
T A C G
G C A T
Review
Consequences of Hybridization in Mammals:
A Systematic Review
Roya Adavoudi and Małgorzata Pilot *
Museum and Institute of Zoology, Polish Academy of Sciences, ul. Nadwi´sla´nska 108, 80-680 Gda´nsk, Poland;
radavoudi@miiz.waw.pl
*Correspondence: mpilot@miiz.waw.pl
Abstract:
Hybridization, defined as breeding between two distinct taxonomic units, can have an
important effect on the evolutionary patterns in cross-breeding taxa. Although interspecific hy-
bridization has frequently been considered as a maladaptive process, which threatens species genetic
integrity and survival via genetic swamping and outbreeding depression, in some cases hybridization
can introduce novel adaptive variation and increase fitness. Most studies to date focused on docu-
menting hybridization events and analyzing their causes, while relatively little is known about the
consequences of hybridization and its impact on the parental species. To address this knowledge gap,
we conducted a systematic review of studies on hybridization in mammals published in 2010–2021,
and identified 115 relevant studies. Of 13 categories of hybridization consequences described in these
studies, the most common negative consequence (21% of studies) was genetic swamping and the most
common positive consequence (8%) was the gain of novel adaptive variation. The total frequency of
negative consequences (49%) was higher than positive (13%) and neutral (38%) consequences. These
frequencies are biased by the detection possibilities of microsatellite loci, the most common genetic
markers used in the papers assessed. As negative outcomes are typically easier to demonstrate than
positive ones (e.g., extinction vs hybrid speciation), they may be over-represented in publications.
Transition towards genomic studies involving both neutral and adaptive variation will provide a
better insight into the real impacts of hybridization.
Keywords:
adaptive introgression; genetic swamping; hybridization; hybrid speciation; hybrid zones;
outbreeding depression; mammals
1. Introduction
Until recently, hybridization was considered as a rare phenomenon in the animal king-
dom and thus its role in animal evolution has been underappreciated [
1
]. Growing amount
of whole genome sequence data produced in recent years made it possible to demonstrate
that a broad range of animal species have experienced hybridization events [
2
]. Although
hybridization frequency (i.e., the proportion of individuals interbreeding with another
species and producing hybrid offspring) is low in most species [
3
], it has been estimated
that around 25% of plant species and 10% of animal species have been affected by hybridiza-
tion [
4
]. Hybridization is most frequent among recently diverged sister species, which are
frequently characterized with incompletely developed prezygotic isolation (behavioural
and mechanical) and postzygotic isolation (zygote mortality and hybrid inviability and
sterility) [
5
]. Hybridization is now recognized as a widespread phenomenon with signif-
icant impact on species evolution [
6
,
7
] and potentially serious consequences for species
conservation and management [8].
Cross-breeding between species with limited postzygotic isolation can often lead to
an intake of genetic variation typical of one species into another species’ gene pool—a
process called introgression. Introgressive hybridization can affect creation, maintenance
and loss of biodiversity [
9
]. In some cases, introgression may facilitate species evolutionary
Genes 2022,13, 50. https://doi.org/10.3390/genes13010050 https://www.mdpi.com/journal/genes
Genes 2022,13, 50 2 of 26
responses to environmental changes by promoting rapid acquisition of new adaptive ge-
netic variants [
10
,
11
], thus increasing adaptive potential of these species [
12
–
15
]. Moreover,
introgressive hybridization can contribute to speciation by creating new genetic variation
and functional novelty [
6
,
16
]. Introgression of alleles from one species into another one
can create novel adaptive combinations of alleles and form a new admixed population,
which is genetically distinct from both parental populations [
17
]. Such population may
develop reproductive isolation from the parental populations and thus maintain distinc-
tiveness even in a contact zone [
18
]. However, speciation through hybridization occurs
less frequently in mammals compared to other vertebrates, because reproductive barriers
between mammalian species are in general well established [
19
]. In species with low
genetic variation, introgressive hybridization could increase genetic variation and decrease
inbreeding, without any signs of outbreeding depression [20,21].
On the other hand, hybridization can be also considered as a potential threat to species
survival [
22
–
24
]. Accumulation of deleterious variation [
25
], outbreeding depression
[26–28]
and genetic swamping [
29
–
31
] are among detrimental consequences of hybridization. In
extreme cases, severe outbreeding depression and decline in the population growth rate
below the replacement rate due to wasted reproductive effort in one or both parental
lineages may lead to extinction [
32
]. High risk of extinction due to hybridization has been
reported for rare or endangered species interbreeding with more common relatives [
33
,
34
].
However, hybridization was mentioned as a factor contributing to extinction in only
11 species out of 120,369 extinct species assessed [
23
]. The negative impact of hybridization
should not be neglected, but the conservation policies should not be focused on the negative
aspects of hybridization only [
23
]. From a conservation perspective, hybridization outcomes
may range from considerable introgression with significant negative impacts, e.g., reduced
survival or reproductive success of hybrids, through minimal introgression with negligible
impact, to moderate introgression with significant positive impacts, e.g., increased fitness
of admixed individuals [
35
]. Given than hybridization can represent either a threat to
species survival or a potential pathway to evolutionary rescue, it is important to examine
its impacts case-by-case [35].
Hybridization may be particularly common in widespread, abundant species and in
non-indigenous species that were intentionally or unintentionally introduced into a new
habitat by humans [
32
,
36
]. Hybridization has also been frequently reported for domesti-
cated species and their wild relatives, e.g., wild boar and domestic pig [
20
,
37
], gray wolf
and domestic dog [
38
–
43
], wild cat and domestic cat [
44
–
47
]. In such cases hybridization
may lead to the introgression of gene variants typical for domestic animals into gene pools
of wild species [
48
,
49
]. This may have a range of negative consequences, such as the loss
of specific adaptations [
41
] and reduced viability [
50
]. These negative consequences are
particularly pronounced in small, fragmented and isolated populations [
51
]. Moreover,
introgressive hybridization can also affect feral populations of domesticated animals [
52
,
53
].
Cross-breeding between individuals originating from captive-bred populations and their
wild conspecifics may have similar consequences as that between domesticated and wild
populations [54].
In recent decades, several review papers on hybridization have been published. They
were focused on specific aspects of hybridization and/or particular taxonomic groups, for
example the evolutionary importance of natural hybridization [
2
], the role of hybridization
in extinction [
32
], hybrid fitness [
55
], introgression during anthropogenic hybridization [
56
],
mammalian hybrid zones [
57
], taxonomic problems associated with inter-specific gene
flow [
58
], hybridization in European ungulates [
59
] and hybridization in New Zealand
taxa [
60
]. Most studies to date focused on documenting hybridization events and analyzing
their causes, while relatively little is known about the consequences of hybridization and its
impact on the parental species [
23
]. To address this knowledge gap, we conducted a system-
atic review of studies on hybridization in mammals and assessed the frequency of different
consequences of hybridization reported. In addition, we evaluated the contribution of dif-
ferent mammalian orders and families in published studies on hybridization. We selected
Genes 2022,13, 50 3 of 26
mammals as the focal class because of the large number of available studies, resulting in
part from the profound role of species from this class in ecosystem functioning [61].
2. Materials and Methods
We focused on papers on hybridization in mammals published between 2010 and 2021.
The database search for papers published in 2021 was completed on the 3rd of December
of that year, so papers published after that date are excluded from the results. For finding
relevant papers in the Web of Science, we employed the following string: (“hybridiza-
tion*” OR “hybridisation*” OR “outbreeding*” OR “outcrossing” OR “admixture*” OR
“admixed individual*” OR “hybrid zone” OR “hybrid individual$*” OR “backcrosse$”)
AND (“mammal$*” OR “vertebrate$” OR “consequence” OR “implication” OR “Extinc-
tion” OR “genetic swamping” OR “adaptive introgression” OR “hybrid speciation” OR
“outbreeding depression”) NOT (“protein$” OR “fish$” OR “plant$” OR “invertebrate$”
OR “avian reptile$” OR “non avian reptile$” OR “fung$” OR “bird$” OR “Lizard$” OR
“penguin$” OR “turtle$” OR “insect$” OR “frog$” OR “butterfl$” OR “homoploid” OR
“moth$” OR “salamander$”). With these keywords we found limited numbers of relevant
papers (49 papers), we therefore applied different sets of keywords: (“hybridization*” OR
“hybridisation*” OR “hybrid$*” OR “outbreeding” OR “outcrossing” OR “admixture*”
OR “introgression*” OR “admixed individual *”OR “hybrid zone” OR “hybrid individ-
ual$*” OR “backcrosse$”) AND (“mammal$ *”) NOT (“protein$” OR “cell$” OR “fish$” OR
“plant$” OR “invertebrate$” OR “avian reptile$” OR “non avian reptile$” OR “fung$” OR
“Cell$” OR “bird$” OR “Lizard$” OR “penguin$” OR “turtle$” OR “insect$” OR “frog$”
OR “butterfl$” OR “homoploid” OR “moth$” OR “salamander$”). We combined the search
results based on these two sets of keywords.
We excluded from the search books, review papers, theses, annuals or meeting reports.
We also excluded papers published in journals that were outside of the following categories:
Evolutionary Biology, Genetics and Heredity, Ecology, Biology, Zoology, Biodiversity Con-
servation, Multidisciplinary Science and Biochemistry and Molecular Biology. Abstracts of
the papers that were identified after applying this automatic exclusion (793 and 641, respec-
tively) were read and these papers that were not focused on the hybridization process in
mammals were removed. We also removed one of the two copies of papers that overlapped
between the paper sets resulting from the search with each set of keywords (
Figure 1
).
We then combined the results from the two sets of papers, including only the papers
meeting the following criteria: experimental studies, focused on mammalian species, that
investigate hybridization among different species and subspecies. Studies that evaluated
admixture among populations of the same species were removed from the analysis, with
the exception of wild and domesticated forms that have been classified as the same species
(e.g., wild cat Felis silvestris silvestris and domestic cat Felis silvestris catus), as well as wild vs
captive/farmed populations of the same species. Although we designed the search terms
to be as comprehensive as possible in the detection of studies on mammalian hybridization,
some relevant studies could have been missed. Nevertheless, the resulting set of papers is
free of human bias (except for the choice of keywords) and therefore provides a reliable
overview of the current knowledge on the consequences of hybridization.
Genes 2022,13, 50 4 of 26
Genes 2022, 13, x FOR PEER REVIEW 4 of 26
Figure 1. Flow diagram showing the selection stages of studies to be included in the review based
on the two sets of keywords used.
3. Results
According to the inclusion criteria defined above, a total of 49 and 87 published pa-
pers were selected based on the first and second set of keywords. This was a small subset
of papers initially identified with each set of keywords; we tried multiple versions of key-
words and did not manage to improve the accuracy of results. After excluding overlap-
ping papers between the two sets of keywords (15.4%), 115 papers were retained for the
subsequent analysis (Figure 1). These papers are listed in Supplementary Table S1.
We calculated the frequency of mammalian orders and families involved in hybridi-
zation process in the surveyed studies (Figure 2). 39.13% of these studies focused on the
order Carnivora (45 papers), of which Canidae (24.34%, 28 papers), Felidae (6.95%, eight
papers), and Mustelidae (6.08%, seven papers) were the most-studied families. Order Ce-
tartiodactyla was the second most-studied order (26.95%, 31 papers), in which Cervidae
(7.82%, nine papers), Bovidae (6.95%, eight papers) and Suidae (5.21%, six papers), were
the most-studied families. The third most represented order was Rodentia (15.65%, 18 pa-
pers), in which Cricetidae (8.69%, 10 papers), Sciuridae (5.21%, six papers) and Muridae
(1.75%, two papers) had the largest contribution. Other orders were represented by only
two families (Chiroptera, 5.21%, six papers and Diprotodontia 2.60%, three papers) or one
family (Primates (3.40%, four papers), Lagomorpha (4.34%, five papers), Macroscelidea
Figure 1.
Flow diagram showing the selection stages of studies to be included in the review based on
the two sets of keywords used.
3. Results
According to the inclusion criteria defined above, a total of 49 and 87 published
papers were selected based on the first and second set of keywords. This was a small
subset of papers initially identified with each set of keywords; we tried multiple versions
of keywords and did not manage to improve the accuracy of results. After excluding
overlapping papers between the two sets of keywords (15.4%), 115 papers were retained
for the subsequent analysis (Figure 1). These papers are listed in Supplementary Table S1.
We calculated the frequency of mammalian orders and families involved in hybridiza-
tion process in the surveyed studies (Figure 2). 39.13% of these studies focused on the
order Carnivora (45 papers), of which Canidae (24.34%, 28 papers), Felidae (6.95%, eight
papers), and Mustelidae (6.08%, seven papers) were the most-studied families. Order
Cetartiodactyla was the second most-studied order (26.95%, 31 papers), in which Cervidae
(7.82%, nine papers), Bovidae (6.95%, eight papers) and Suidae (5.21%, six papers), were the
most-studied families. The third most represented order was Rodentia (15.65%, 18 papers),
in which Cricetidae (8.69%, 10 papers), Sciuridae (5.21%, six papers) and Muridae (1.75%,
two papers) had the largest contribution. Other orders were represented by only two
families (Chiroptera, 5.21%, six papers and Diprotodontia 2.60%, three papers) or one
family (Primates (3.40%, four papers), Lagomorpha (4.34%, five papers), Macroscelidea
(0.86%, one study), Perissodactyla (0.86%, one study) and Soricomorpha (0.86%, one study).
Genes 2022,13, 50 5 of 26
Genes 2022, 13, x FOR PEER REVIEW 5 of 26
(0.86%, one study), Perissodactyla (0.86%, one study) and Soricomorpha (0.86%, one
study).
Figure 2. Relative frequencies of (a) orders represented in 115 papers included in the systematic
review, (b) orders represented across all currently recognized mammalian species [62] and (c) fam-
ilies represented in 115 papers included in the systematic review.
We compared the frequencies of species representing different mammalian orders in
the surveyed studies on hybridization with the frequencies of all currently recognized
contemporary mammalian species [62] representing different mammalian orders. This
comparison demonstrated a considerable bias in the number of studies on hybridization
focused on representatives of different mammalian orders (Figure 2a,b).
We classified the hybridization outcomes described in the 115 papers included in the
systematic review into 13 categories (Table 1). These categories were non-exclusive and in
some cases the consequences of hybridization reported could be classified to more than
one category. Among the 115 surveyed papers, 10 papers did not provide sufficient infor-
mation to classify them in any category, e.g., [63,64]. Therefore, this classification is based
on 105 papers. The reported frequencies of different hybridization outcomes in these pa-
pers should not be considered as reliable estimates of the real frequencies, because of the
biases discussed below. We classified the impacts of each possible outcome as (1) positive
(e.g., gaining novel adaptive variation), (2) neutral or unknown, (3) negative (e.g., extinc-
tion, loss of reproductive output) and (4) considered as negative. In this last category we
included genetic swamping and introgression from a domesticated lineage, which are fre-
quently described as negative in the literature [29,30,65–67]. Given that direct empirical
evidence for their negative effects is limited, we did not classify them as unequivocally
negative outcomes. It is important to note that extinction due to extreme genetic swamp-
ing is classified in a separate category, given its clearly negative impact.
Figure 2.
Relative frequencies of (
a
) orders represented in 115 papers included in the systematic
review, (
b
) orders represented across all currently recognized mammalian species [
62
] and (
c
) families
represented in 115 papers included in the systematic review.
We compared the frequencies of species representing different mammalian orders
in the surveyed studies on hybridization with the frequencies of all currently recognized
contemporary mammalian species [
62
] representing different mammalian orders. This
comparison demonstrated a considerable bias in the number of studies on hybridization
focused on representatives of different mammalian orders (Figure 2a,b).
We classified the hybridization outcomes described in the 115 papers included in
the systematic review into 13 categories (Table 1). These categories were non-exclusive
and in some cases the consequences of hybridization reported could be classified to more
than one category. Among the 115 surveyed papers, 10 papers did not provide sufficient
information to classify them in any category, e.g., [
63
,
64
]. Therefore, this classification
is based on 105 papers. The reported frequencies of different hybridization outcomes in
these papers should not be considered as reliable estimates of the real frequencies, because
of the biases discussed below. We classified the impacts of each possible outcome as (1)
positive (e.g., gaining novel adaptive variation), (2) neutral or unknown, (3) negative (e.g.,
extinction, loss of reproductive output) and (4) considered as negative. In this last category
we included genetic swamping and introgression from a domesticated lineage, which are
frequently described as negative in the literature [
29
,
30
,
65
–
67
]. Given that direct empirical
evidence for their negative effects is limited, we did not classify them as unequivocally
negative outcomes. It is important to note that extinction due to extreme genetic swamping
is classified in a separate category, given its clearly negative impact.
Genes 2022,13, 50 6 of 26
Table 1.
Outcomes of hybridization described in papers included in the systematic review. The
outcomes are grouped by the character of their impact. The reported frequencies of different hy-
bridization outcomes in the papers studied should not be considered as reliable estimates of the
real frequencies.
Results Impacts Number of
Papers Percentage Description
1 Genetic swamping Considered as
negative 29 20.71
Genetic integrity of a species involved in hybridization
being threatened by introgression from another species
2Introgression from a
domesticated lineage Considered as
negative 25 17.85 Genetic integrity of wild species being threatened by
introgression from a domesticated lineage
3Extinction due to extreme
genetic swamping Negative 3 2.14 Complete loss of genetic material of one of the species
involved in hybridization
4 Outbreeding depression Negative 7 5.0 Reduction or loss of specific adaptations and
overall fitness
5 Morphological anomalies Negative 2 1.4 Morphological anomalies with negative effects
on fitness
6
Loss of reproductive output
Negative 3 2.14 Decrease in growth rate of parental species because of
wasted reproductive effort
7
Increase in genetic diversity
and reduction of inbreeding
Positive 3 2.14 Increase in genetic diversity via low rates of
introgression, without any evidence of outbreeding
depression; reduction of inbreeding levels
8Gaining novel adaptive
variation Positive 11 7.85 Transferring of adaptive variants through
hybridization
9 Hybrid speciation Positive 4 2.85 Creation of a new species via hybridization
10 Intermediate phenotypic
traits Neutral or
unknown 10 7.14 Intermediate morphological characteristics of hybrid
individuals relative to the parental species
11 Hybrid zone Neutral or
unknown 14 10.0 Geographically restricted zones where genetically
distinct species meet and mate
12 Hybridization without
significant impacts Neutral or
unknown 5 3.57
Evidence of hybridization without substantial changes
in the gene pools of each species
13 No or rare evidence of
hybridization Neutral or
unknown 24 17.14 Hybridization is rare and does not result
in introgression
Of 115 studies considered, 21 (18.26%) identified hybrids using microsatellite loci as
the only genetic markers, 18 studies (15.65%) used mtDNA fragments, 35 (30.43%) studies
used both microsatellite loci and mtDNA, 12 studies (10.43%) used genome-wide single
nucleotide polymorphisms (SNPs) or whole genome sequencing, two studies (1.73%) used
all these three types of markers, and the remaining studies used another method of hybrid
detection. Altogether, 50.42% of studies used microsatellite loci as either the only type of
genetic markers or together with other types.
To assess whether the analysis of genome-wide data may affect the type of hybridiza-
tion outcomes observed, we calculated the frequencies of different outcomes based on
14 papers that used genome-wide SNPs or whole genome sequencing. As more than half
of these papers (eight studies) focused on hybridization between domestic animals and
their wild relatives, introgression from a domesticated lineage was the most common
negative effect (36% of studies), followed by genetic swamping (18%). Novel adaptive
variation was the only positive impact of hybridization and was reported in five studies
(23%). In total, negative outcomes were reported more frequently than positive ones (54%
and 23%, respectively). The frequencies of both negative and positive outcomes were
higher than in the entire dataset (49% and 13%), while the frequency of neutral outcomes
was smaller. However, these frequencies should be treated with caution due to the small
number of studies and overrepresentation of hybridization with domestic animals among
the studies considered.
Genes 2022,13, 50 7 of 26
4. Discussion
4.1. Hybridization in Mammalian Orders and Families
4.1.1. Mammalian Orders
The frequency of different mammalian orders in the studies included in this systematic
review does not reflect the number of species within each order. Representatives of orders
Carnivora and Cetartiodactyla prevail among the species studied, with the frequencies
of 39% and 27%, respectively. The frequency of species from these orders among all
mammalian species are 5% and 6%, respectively [
62
]. In contrast, two most species-
rich mammalian orders, Rodentia (42% of species) and Chiroptera (21% of species) were
represented in only 16% and 5% of studies, respectively. In studies of hybrid zones, rodents
have been represented more frequentlythan other mammalian orders, but nevertheless only
eight rodent genera have been studied, as reported in a review paper [
57
]. Therefore, the
underrepresentation of rodents in hybridization studies may result from the focus on well-
studied genera only, such as e.g., the genus Mus. Several studies published in the previous
decade (i.e., not considered in this systematic review) detected signatures of hybridization
in several bat species e.g., [
68
–
71
], but altogether hybridization was reported for less than 20
of over 1000 known bat species. This may be associated with a limited number of studies on
hybridization in bats [
72
] or a stronger reproductive isolation in bat species compared with
other mammals [
70
,
73
]. As bats can form mixed-species groups during mating seasons [
74
]
and during maternal care [
75
], reproductive barriers are particularly important for the
maintenance of species distinctiveness.
Accordingly, overrepresentation of orders Carnivora and Cetartiodactyla in hybridiza-
tion studies may result from more relaxed reproductive barriers between congeneric species
from these orders compared with other mammals, overrepresentation of studies focused on
these orders, or a combination of both. High interest in studying species from these orders
may result from their important roles in ecosystems and in some cases their high commer-
cial value. Large species from the order Carnivora are keystone species in their ecosystems
and are frequently subject to active management and conservation strategies [
76
–
79
]. Ac-
cordingly, many representatives of Artiodactyla are valuable game species. Moreover,
species from Carnivora and Cetartiodactyla orders can compete with humans over re-
sources by consuming game species, livestock depredation and fisheries depredation, as
well as damaging crops and wild vegetation [
78
,
80
]. For these reasons, they are of particular
interest to wildlife researchers, also in the context of hybridization.
In theory, the proportion of species within each mammalian order that are subject
to introgressive hybridization could be used as a measure of the strength of reproductive
barriers between species within each order. However, to achieve a reliable comparison
between mammalian orders, several sources of bias would have to be accounted for,
including the above-mentioned differences in intensity of research on different mammalian
orders as well as differences in criteria used to define species. Therefore, in practice the
frequency of detected hybridization cases is not a reliable measure of the strength of
reproductive isolation.
4.1.2. Mammalian Families
The frequency of families within each mammalian order that are subject to hybridiza-
tion studies is biased as well. For example, the Canidae family is represented in 62% of
studies on the order Carnivora and 24% of all 115 studies on mammalian hybridization
assessed in this systematic review. The second most frequently represented family within
Carnivora is the Felidae family, represented in 18% of studies on this order. Canidae
and Felidae are the only families within the order Carnivora that include domesticated
species, the domestic dog (Canis lupus familiaris) and the domestic cat (F. s. catus), respec-
tively. Among the studies included in this systematic review, most (68%) of studies on
the Canidae family were focused on hybridization between gray wolves and domestic
dogs [
38
,
81
–
84
]. Accordingly, seven out of eight studies (87%) on the Felidae family were
focused on hybridization between domestic cats and wild cats [
85
,
86
]. Due to a recent
Genes 2022,13, 50 8 of 26
origin of domestic animals, their hybrids with the wild relatives are fertile and thus can
back-cross into parental populations [
87
–
89
]. Moreover, global populations of domestic
dogs and cats have been increasing with human population growth, and the majority of
individuals globally are free-ranging and thus can breed freely [
90
]. Widespread occurrence
of free-ranging domestic dogs and cats may have promoted their interactions with their
wild relatives and as a result increased the rate of hybridization between them [
81
,
91
,
92
].
The presence of a domesticated species within a particular family and order may be thus
an important factor increasing the hybridization rate.
Within Artiodactyla, Cervidae, Bovidae and Suidae were the most studied families. All
hybridization cases described in the family Suidae were between the wild boar (Sus scrofa)
and domestic pig (Sus scrofa domesticus). Although free-roaming domestic pigs are rare,
hybridization with wild boars may occur in open domestic boar farms [
93
]. Cross-breeding
with wild boars is also used intentionally by humans to obtain less aggressive and larger-
sized animals, and to increase growth rate of offspring [
93
]. Climate change, low frequency
of predators, supplementary feeding, reforestation of agricultural areas and intentional
releases for hunting have led to the range expansion of the wild boar, which as a result
has become one of the most widespread large mammals in the world and the second most
frequent ungulate in Europe [
94
–
97
]. In many regions, the wild boar has been considered
as a pest species for croplands [
93
,
98
]. One hypothesis for the vast distribution of wild
boars is that introgression from domestic pigs could have led to their increased fitness
and invasiveness [
99
,
100
]. Hybridization between domestic yaks (Bos grunniens) and wild
yaks (Bos mutus) [
101
] (Bovidae) is spatially more restricted, given geographically restricted
ranges of the wild species, but similarly as in the case of pig–wild boar hybridization, it
occurs as both a spontaneous admixture and intentional cross-breeding by humans. Overall,
36% of studies (41 papers) considered in this review were focused on hybridization between
domestic animals and their wild relatives, suggesting that the presence of domesticated
forms within a family facilitates hybridization.
The effect of human activities on hybridization has long been known [
102
], and
domestication is one of many anthropogenic factors that may increase the frequency of
hybridization. The introduction of invasive species to distribution ranges of closely related
species may have a similar effect [
36
,
103
]. Together with habitat fragmentation and destruc-
tion, introduced species are an important threat to global biodiversity
[104–107]
. Many
wild ungulates are valuable game species, and therefore are strongly affected by humans
by extensive translocations and introductions of non-native species, hunting, and artificial
management; all these factors contribute to hybridization within ungulate families [108].
In particular, the Cervidae family includes multiple valuable game species. One of
them, the sika deer (Cervus nippon), was deliberately introduced to many European coun-
tries for hunting [
109
], which has led to hybridization with native deer species in some
regions [
110
–
112
]. Another cervid, European roe deer (Capreolus capreolus), is known to
hybridize with Siberian roe deer (Capreolus pygargus) [
15
,
113
] and Italian roe deer (Capreolus
c. italicus) [
114
]. Although natural processes (e.g., range expansion) could have caused
hybridization in this genus, human-mediated introductions of Siberian roe deer, aimed at in-
creasing body mass and trophy size of European roe deer, affected the rate of hybridization
between these species [
15
]. In Bovidae family, hybridization was reported between Tatra
chamois (Rupicapra rupicapra tatrica) and introduced Alpine chamois (Rupicapra rupicapra
rupicapra) [21]. In that case, the introduction was carried out for conservation purposes.
In cetacean species, hybridization has been documented both in captive breeding sites
and in the wild [
115
,
116
], with around 20% of species known to hybridize [
117
]. Cross-
breeding was shown to be more common between species that have similar morphological
and behavioral traits [
117
–
119
], and to be facilitated by population fragmentation [
120
–
122
].
Although until recently it was believed that hybridization in cetaceans is a dead-end process,
as most known hybrids seemed to be infertile [
120
], a study on hybridization between
fin whale (Balaenoptera physalus) and blue whale (Balaenoptera musculus) showed that the
hybrid individuals can reproduce and survive to adulthood in specific circumstances [
123
].
Genes 2022,13, 50 9 of 26
4.2. Typical Outcomes of Hybridization between Mammalian Species
Depending on species and environmental conditions, hybridization may have either
negative or positive impacts, and sometimes there may be very limited consequences.
In some cases, hybridization can drive species toward extinction, while in others it pro-
vides an opportunity to create new species [
124
]. Genetic swamping, outbreeding depres-
sion, introgression of variants originating from domesticated lineages, and morphological
anomalies are typically associated with negative consequences, such as loss of adaptive
variation [
26
,
125
–
130
], high mortality rates [
131
], and even extinction [
30
]. However,
hybridization can be considered as a beneficial process in some circumstances. Introgres-
sion from a closely related species may facilitate adaptation by providing novel adaptive
variation; this may be particularly important when a population occupies a sub-optimal,
poor-quality habitat, expands to a new habitat, or experiences rapid changes in local
environmental conditions [15,20,132].
Of 13 categories of hybridization outcomes identified in the studies considered in this
review (Table 1), genetic swamping and introgression of variants originating from domesti-
cated lineages were two most common outcomes (21% and 18% of studies, respectively).
Both these outcomes are commonly considered as negative. Another common outcome
(17% of studies), “no or rare evidence of hybridization”, can be classified as neutral. The
most common positive outcome (8%) was the gain of novel adaptive variation. Graphical
representation of the common outcomes of hybridization is presented on Figure 3.
Genes 2022, 13, x FOR PEER REVIEW 10 of 26
Figure 3. Graphical representation of the common outcomes of hybridization.
The frequencies of different outcomes of hybridization may be affected by the specific
sets of keywords that were employed in the literature search. We included keywords such
as “Genetic swamping”, “Hybrid zone”, “Hybrid speciation”, “Extinction”, and “Out-
breeding depression”, and therefore studies focusing on these topics may be overrepre-
sented. Furthermore, information about the consequences of hybridization is missing
from some studies, which could also affect the result. Nonetheless, we also identified out-
comes that were not included in the keywords, and some which were included had very
low frequencies among the selected papers (e.g., “Hybrid speciation”).
4.2.1. Negative Outcomes
Genetic Swamping
Genetic swamping refers to the process where genotypes of one or both parental spe-
cies are partially replaced by hybrid genotypes [32]. Genetic swamping is typically con-
sidered as a negative consequence of hybridization due to its disruptive effects on genetic
integrity of species and potential to eliminate unique adaptations. Negative results of this
process are well documented in some cases, e.g., when it leads to extinction (see below)
or results in outbreeding depression e.g., [133]. However, many studies reporting genetic
swamping do not assess its fitness consequences or long-term effects on the gene pool
composition, and therefore it remains unclear whether the negative consequences of this
process prevail among all the cases when it occurs. Genetic rescue, i.e., a reduction of ex-
tinction probability of a small, isolated population by restoring gene flow [134] is neces-
sarily associated with genetic swamping, especially if the source of gene flow belongs to
another species. Therefore, in some cases negative effects of genetic swamping on the spe-
cies genetic integrity may be compensated by positive effects, such as reduction of in-
breeding depression in isolated populations.
Nearly half (48%) of studies included in this systematic review that reported genetic
swamping were focused on hybridization between domesticated mammals and their wild
relatives, including wolf and domestic dog [38,81,135], wild boar and domestic pig
Figure 3. Graphical representation of the common outcomes of hybridization.
Genes 2022,13, 50 10 of 26
The frequencies of different outcomes of hybridization may be affected by the specific
sets of keywords that were employed in the literature search. We included keywords
such as “Genetic swamping”, “Hybrid zone”, “Hybrid speciation”, “Extinction”, and
“Outbreeding depression”, and therefore studies focusing on these topics may be overrepre-
sented. Furthermore, information about the consequences of hybridization is missing from
some studies, which could also affect the result. Nonetheless, we also identified outcomes
that were not included in the keywords, and some which were included had very low
frequencies among the selected papers (e.g., “Hybrid speciation”).
4.2.1. Negative Outcomes
Genetic Swamping
Genetic swamping refers to the process where genotypes of one or both parental
species are partially replaced by hybrid genotypes [
32
]. Genetic swamping is typically
considered as a negative consequence of hybridization due to its disruptive effects on
genetic integrity of species and potential to eliminate unique adaptations. Negative results
of this process are well documented in some cases, e.g., when it leads to extinction (see
below) or results in outbreeding depression e.g., [
133
]. However, many studies reporting
genetic swamping do not assess its fitness consequences or long-term effects on the gene
pool composition, and therefore it remains unclear whether the negative consequences of
this process prevail among all the cases when it occurs. Genetic rescue, i.e., a reduction
of extinction probability of a small, isolated population by restoring gene flow [
134
] is
necessarily associated with genetic swamping, especially if the source of gene flow belongs
to another species. Therefore, in some cases negative effects of genetic swamping on the
species genetic integrity may be compensated by positive effects, such as reduction of
inbreeding depression in isolated populations.
Nearly half (48%) of studies included in this systematic review that reported ge-
netic swamping were focused on hybridization between domesticated mammals and
their wild relatives, including wolf and domestic dog [
38
,
81
,
135
], wild boar and domestic
pig
[20,30,93]
and wild cat and domestic cat [
44
]. More than a quarter (28%) of the stud-
ies reported genetic swamping of a native gene pool as the main result of hybridization
between introduced species and native species, e.g., in Cervidae [
36
,
136
] and Mustelidae
families [
29
,
137
,
138
]. Over 80% of the studies reporting genetic swamping focused on
cases where hybridization was directly or indirectly caused by human actions, i.e., either
domestication or species translocation (deliberate or unintentional). This implies that either
such cases are considered as greater concern than introgression resulting from natural
hybridization between pairs of wild native species and thus are studied more frequently, or
genetic swamping is indeed more frequent when it involves a domesticated or introduced
species cross-breeding with a native wild species.
Reproductive barriers between closely related species that evolved in geographic
isolation may be weak, and therefore after the secondary contact due to translocation, cross-
breeding and production of fertile offspring may be common. In such cases, continuous
cross-breeding across generations may result in considerable genetic swamping [
36
]. Ac-
cordingly, reproductive isolation between domesticated mammals and their wild ancestors
is frequently incomplete due to their recent divergence. For example, hybridization between
wolves and domestic dogs results in introgression of hybridization-derived variants into
gene pools of both canids [
139
]. In wolves, introgression of dog variants is mostly driven
by drift, with only a small number of genes experiencing negative or positive selection due
to this process [
139
]. In free-ranging domestic dogs, the observed proportion of candidate
genes under positive selection was larger than those under negative selection, suggesting
that introgression from wolves may provide dogs with an adaptive advantage [
139
]. This
last case demonstrates that genetic swamping is not an unequivocally negative process,
and its outcomes should be considered on an individual basis.
Genes 2022,13, 50 11 of 26
Extinction via Genetic Swamping
In extreme cases, extensive genetic swamping may lead a population or an entire
species towards extinction [
32
,
140
]. Endemic species with patchy, isolated habitats are
under a particularly high risk of extinction via hybridization with introduced or invasive
closely related species. Of 115 papers considered in this systematic review, three papers
mentioned the risk of extinction by genetic swamping [
30
,
114
,
141
]. One of these papers
describes the case of the Java warty pig (Sus verrucosus), which is endangered with extinc-
tion via genetic swamping from the common Indonesian banded pig (Sus scrofa vitattus),
because of high hybridization rates resulting from the breakdown of reproductive barriers
and reduced fertility of hybrids [
30
]. The second paper reports the case of extinction of
the endemic Italian roe deer (C. c. italicus) due to extreme genetic swamping from the
introduced European roe deer (Capreolus c. capreolus) [
114
]. The third study presents a
mathematical model on hybridization between the mountain hare (Lepus timidus) and
European hare (Lepus europaeus), showing that under climate change scenarios, increased
hybridization rate can lead to the mountain hare’s extinction via genetic swamping [
141
].
These studies focused on endemic species, which are threatened by habitat fragmentation
and overhunting, and are interbreeding with common, closely related species. Extinction
of endemic species through genetic swamping has also been reported in other taxonomic
groups, including plants e.g., [140].
Notably, identifying key factors involved in the extinction process is very challenging.
In many cases, interaction of different forces such as environmental stress, low genetic
diversity and small population size, may lead to the extinction vortex [
142
,
143
]. Therefore,
while hybridization may play an important role in pushing a species towards extinction, it
may not be the only contributing factor. Overall, hybridization contributed to extinction in
only 11 documented cases [23].
Outbreeding Depression
Outbreeding depression occurs when cross-breeding between two species or pop-
ulations that are adapted to different environmental conditions results in a loss of local
adaptations and reduction of fitness in hybrid individuals [
144
]. In the studies reviewed
here, outbreeding depression has been reported in native species that cross-bred with
non-native or invasive species, such as the roe deer interbreeding with the introduced
sika deer [
36
,
145
], and also in cases of admixture between wild and captive-bred popu-
lations e.g., wild versus captive-born American mink, [
26
]. In both cases, introgression
may break-up co-adapted gene complexes, reducing fitness in wild populations and result-
ing in outbreeding depression [
146
,
147
]. Selection pressures in captive-bred populations,
associated with adaptations to the captive environment and artificial selection on traits
desirable for humans result in the presence of gene variants that are maladaptive in natural
habitats [
32
,
148
]. Moreover, captive-bred populations have small sizes, which leads to low
genetic diversity and inbreeding depression. Introgressive hybridization may introduce
maladaptive gene variants present in such captive populations to natural populations, with
negative effects on their fitness.
On the other hand, captive breeding programs for conservation purpose have become
a conservation tool to prevent extinctions and support reintroductions in cases when
remaining wild populations are small and have low genetic diversity [
149
,
150
]. For example,
captive breeding program of European mink was lunched as a conservation tool for this
critically endangered species [151,152].
Among the papers discussed in this systematic review, five studies were focused on
admixture between wild and captive-bred populations of the same species. Two of these
studies did not detect any signatures of hybridization, and the remaining three studies
reported both outbreeding depression and genetic swamping. One of them reported genetic
swamping for the native population and increase in genetic diversity for the captive-bred
population studied.
Genes 2022,13, 50 12 of 26
Introgression from a Domesticated Lineage
Hybridization between wild species and their domesticated relatives frequently results
in the introgression of gene variants typical of domesticated animals to wild populations.
Although there is a considerable overlap between the studies included in this category with
other categories, we consider it separately due to specific conservation problems resulting
from this type of introgression [
153
]. Domesticated mammals are not separated from their
wild ancestors by strong reproductive barriers, and therefore they are likely to cross-breed
in regions where their ranges overlap. Introgression of domesticated species’ alleles to wild
species’ gene pool may threaten the genetic integrity of wild species [
154
], and therefore it
is typically considered as a negative process. However, such introgression may increase
the genetic variability in wild species suffering the effects of a severe bottleneck, and/or
accelerate the process of adaptation to changing environmental conditions by providing
novel genetic variation [
155
]. For example, the Alpine ibex (Capra ibex ibex) acquired one
of its two MHC DRB alleles from domestic goats (Capra aegagrus hircus), which critically
increased diversity of this genetically impoverished species at the key component of the
immune system [156].
Among 25 studies from our systematic review that fit in this class, 15 studies focused
on hybridization between the grey wolf or the dingo and the domestic dog, four studies
focused on the wild boar and the domestic pig, four studies on the wild cat and the
domestic cat, one study on the wild sheep and the domestic sheep, and one study on the
wild yak and the domestic yak. These studies show that the introgression from domestic
animals into their wild relatives is more frequent than in the opposite direction. Population
sizes of domestic animals are dependent on the human population size, and therefore
human population growth combined with the fragmentation of natural habitats increases
both the numbers of domestic animals and the probability of encounters with their wild
relatives. Given that wild populations are typically considerably smaller than populations
of domestic animals, a single hybridization and back-crossing event will have a larger effect
on gene pools of wild populations compared with domestic ones.
Studies focused on hybridization between domestic animals and their wild relatives
constituted 36% of studies considered in this systematic review, and thus they had sig-
nificant impact on the overall proportions of different consequences of hybridization. By
default, they were responsible for all the cases of introgression from domesticated lineages,
which were reported in 44% of studies focused on hybridization with domestic animals.
Further 24.5% of studies reported genetic swamping; in this case, the difference between
these two consequences is only in wording, with the exception of introgression cases from
wild to domestic populations. The most common positive consequence was gaining novel
adaptive variation (7%). Overall, the frequency of hybridization outcomes considered as
negative (70%) was considerably higher than the frequency of positive outcomes (9%). This
suggests that studies on hybridization between domestic animals and their wild relatives
have a disproportional contribution to the negative hybridization outcomes in the overall
assessment. However, this is based on the assumption that introgression from domesticated
lineages and genetic swamping are negative outcomes by default, which has rarely been
tested. Given low divergence between domesticated animals and their wild relatives, it
may be expected instead that introgression will rarely lead to increased mortality and
infertility of admixed individuals, but the presence of atypical phenotypic traits may result
in reduced fitness.
Morphological Anomalies
Interspecific hybridization influences phenotypic traits and may create novel or un-
usual traits [
157
,
158
]. Morphological anomalies and abnormal growth are common among
hybrid individuals [
159
] and are sometimes used as a proxy to detect hybridization [
160
].
Morphological anomalies usually reduce fitness and in extreme cases may cause inviability,
and therefore we classified them as a negative outcome of hybridization. In cases where
morphological anomalies increase fitness of hybrid individuals, they are considered as
Genes 2022,13, 50 13 of 26
novel adaptive variation, which is a separate category of hybridization outcomes identified
in this review (see below).
The divergence of phenotypic traits of admixed individuals from average traits within
each of the cross-breeding species increases with their divergence time [
157
,
161
,
162
]. De-
pending on the species, the anomalies can occur in different body parts, including teeth,
skull, horn shape, body size etc. Among the papers considered in this systematic review,
we found only two papers that reported morphological anomalies in hybrid individuals,
including abnormal placental growth in hybrids between two species of dwarf hamsters
(Phodopus campbelli and Phodopus sungorus) [
131
] and skull, dental and horn anomalies in
the wildebeest hybrids (Connochaetes taurinus and Connochaetes gnu) [157].
Loss of Reproductive Output
Hybridization can change reproductive output by leading to changes in mating behav-
ior [
163
] or by wasting reproductive efforts. These changes typically involve reduction in
reproductive success, and therefore are considered as a negative consequence of hybridiza-
tion. For instance, unidirectional introgression from the fin whale to blue whale resulted in
the reduction of reproductive rate of the blue whale, reducing its recovery [
123
]. In cases
when most hybrid individuals are infertile and inviable, introgression does not happen or
is rare, and therefore the consequences of hybridization are reduced to the production of F1
hybrids only. Moreover, in some cases the reproductive output differs between different
generations of hybrids. For example, hybridization between Microtus hartingi lydius and
Microtus hartingi strandzensis produces viable and prolific F1 hybrids, while in the F2 gener-
ation, males are sterile and the mortality rate is high [
164
]. Falling fertility rates and loss
of reproductive outputs may lead to severe demographic declines in parental species and
even a rapid extinction of local populations involved in cross-breeding.
4.2.2. Positive Outcomes
Increase in Genetic Diversity and Reduction of Inbreeding
In a specific case when genetic diversity of a population is very low and the rate of
inbreeding is high, introgression from a non-native population or species can increase
genetic diversity without any signs of outbreeding depression. This can be considered as a
positive consequence of hybridization. Moreover, in small and fragmented populations
that have low genetic diversity and experience inbreeding depression, hybridization can
restore population viability [
165
,
166
]. Genetic rescue, i.e., restoration of genetic diversity
and mitigation of inbreeding depression through gene flow can be a valuable tool in
conservation of small, isolated populations [
167
]. For instance, introgressive hybridization
with a non-native Alpine chamois (R. r. rupicapra) was shown to improve genetic diversity
of Tatra chamois (R. r. tatrica), an endangered endemic population in the Tatra Mountains
that suffered from a high level of inbreeding depression [21].
Although introgression from domesticated lineages can be considered as a threat for
wild populations, in some circumstances it can increase genetic diversity and viability
of wild populations. For example, increase in genetic diversity has been reported in
European wild boars that cross-bred with domestic pigs [
20
]. Accordingly, admixture
between feral and farmed populations of American mink (Neovison vison) increased genetic
diversity of the invasive populations of these species in Europe, which could increase their
adaptive potential and therefore compromise management efforts to control them [
137
].
Although this is a negative process from the conservation perspective, it can be considered
as a positive outcome of hybridization in terms of increasing individual fitness in the
invasive population.
Novel Adaptive Variation
In some cases, creation of novel genetic diversity via hybridization can facilitate species
adaptation to variable or novel environmental conditions, without a loss of its genetic
integrity [
132
,
168
]. Admixed individuals may acquire new adaptive traits, providing them
Genes 2022,13, 50 14 of 26
with selective advantages in comparison to their parental species [
169
,
170
]. For instance, in
eastern Poland, introgression from the Siberian roe deer (C. pygargus) allowed the European
roe deer (C. capreolus) to adapt better to severe winters, which are an important contributing
factor of roe deer mortality [
171
]. Furthermore, hybridization between the coyote (Canis
latrans) and the grey wolf (Canis lupus) in Canada has resulted in the introduction of novel
adaptive variation to the coyote populations, allowing them to increase in body size, which
in turn improved their success in hunting deer [172].
In several mammalian species, including humans, the presence of adaptive variation
from their extinct relatives has been detected [
173
–
175
], implying that ancient hybridization
events provided long-lasting positive fitness effects [
176
]. For example, Tibetan and Hi-
malayan wolves experienced ancient introgression from an unknown canid lineage, which
resulted in the introgression of an EPAS1 haplotype that confers an adaptive advantage in
high altitude environments [
175
]. In humans, ancient cross-breeding with Neanderthals
and Denisovans in Eurasia resulted in introgression of novel adaptive variation, but also
increased the genetic load compared with non-admixed African populations [
25
,
177
]. Alto-
gether, among 14 papers considered in this systematic review that used genome-wide SNPs
or whole genome sequencing, there were six papers reporting cases of ancient introgression.
Three of these studies showed that ancient introgression was associated with gaining novel
adaptive variation, and the remaining three papers reported ancient introgression without
investigating its consequences.
Hybrid Speciation
Hybrid speciation refers to the process in which hybridization results in the creation of
a new species, which is characterized by mixed ancestry and distinct genetic composition
from its parental species [
18
]. Hybridization may act as a driving force in speciation by cre-
ating new hybrid phenotypes or providing necessary material for adaptive divergence [
17
].
Given that the creation of a new species increases biodiversity, it can be considered as a
positive outcome of hybridization.
Three criteria should be met to demonstrate speciation via hybridization; first, con-
firmed evidence of a past hybridization event in the putative hybrid species, second,
reproductive isolation between the hybrid species and its parental species, and finally the
presence of isolating impacts of hybridization [
178
]. Hybrid speciation may allow the new
species to colonize a new habitat [179].
In this review we found four studies that reported hybrid speciation [
131
,
180
–
182
].
These studies showed that the emergence of distinct phenotypic traits in hybrid individ-
uals may play an important role in speciation by impeding gene flow between parental
species and hybrid individuals [
131
]. For instance, differentiation in facial patterns in the
primate genus Cercopithecus is one of the key mechanisms driving hybrid speciation in
this genus [
181
,
183
]. Abnormal growth patterns in hybrids between two dwarf hamster
species, P. campbelli and P. sungorus, were suggested to play an important role in speciation
by contributing to reproductive isolation between these recently diverged species [
131
].
Despite its potentially important role in mammalian speciation, the genetic basis of growth-
related developmental inviability is still unknown [
131
]. However, studies on a hybrid
zone between subspecies the house mouse (Mus musculus), which is a model species in
genetics, provided an insight into the molecular mechanisms underlying hybrid specia-
tion. Dysfunction in the Mecp2 protein in the house mouse resulting from introgressive
hybridization within the hybrid zone may induce changes in the expression of thousands
of genes, which may initiate the speciation process [182].
4.2.3. Neutral or Unspecified Outcomes
Intermediate Phenotypic Traits
Although in some cases interspecific hybridization may create deleterious morpho-
logical anomalies or novel adaptive traits (see above), hybrid individuals frequently show
intermediate phenotypic traits compared to their parents [
184
]. The additive effect, domi-
Genes 2022,13, 50 15 of 26
nance effect, and/or epistatic effect may create variation in polygenic traits [
157
,
185
]. In
the additive model, F1 hybrid offspring shows intermediate phenotypes relative to their
parents [
185
]. A classic example of the effect of hybridization on morphological traits are
the Darwin finches in Galapagos, where most hybrid individuals have intermediate body
size and beak shape compared with the parental species [
186
]. Several studies in this review
reported intermediate phenotypes, e.g., in cetaceans [
187
], mustelids [
188
], camelids [
189
]
and primates [
181
]. The presence of admixed individuals with intermediate phenotypes
may impede species identification in the field. For instance, field identification of four
chipmunk species (Tamias spp.) in the Sierra Nevada, USA, was associated with 14% error
rate, which was in part attributed to sporadic hybridization among these species [
190
].
The fitness consequences of intermediate phenotypic traits have rarely been studied and
therefore this outcome of hybridization could not be classified as either positive or negative.
Hybrid Zones
Hybrid zones are areas where two genetically distinct linages meet, mate and create
viable offspring [
191
]. These geographic regions are usually narrow, with the width ranging
from several meters to several kilometers [
192
]. Hybrid zones can be created through
natural hybridization between parapatric or sympatric species [
193
,
194
]. Most hybrid zones
are maintained by the balance between natural selection against hybrids and dispersal
capabilities of the cross-breeding taxa [
179
,
191
]. If before the range expansion or removal
of a geographic barrier, reproductive isolation between closely related species has not
been complete, hybrid zone may be formed. For example, due to a recent divergence and
weak reproductive isolation between the pine marten Martes martes and the sable Martes
zibellina in Western Siberia, a vast hybrid zone has formed between these species after
the Last Glacial Maximum [
138
]. Features of hybrid zones, such as fertility or sterility
of hybrid individuals, directionality of mating, hybridization frequency, and geographic
extent of introgression, vary considerably, and their examination can help understand
the mechanisms of hybrid zone maintenance [
195
]. In woodrat species (Neotoma bryanti
and Neotoma lepida), a hybrid zone has been maintained as a result of sporadic cross-
breeding between these species and hybrid fertility [196]. Among studies included in this
literature review, hybrid zones have been described in mice (Mus musculus musculus and
Mus musculus domesticus) [
197
], different woodrat species [
195
,
196
,
198
–
200
], marmots [
201
],
primates [181], artiodactyles [157,202], Diprotodontia [203,204] and carnivores [138,205].
Hybridization without Significant Impacts
Some studies included in this review showed that despite hybridization, populations
maintained their genetic distinctiveness [
206
]. For instance, despite extensive rate of hy-
bridization among different bat species in Poland, their gene pools have not been disrupted
by introgression [
74
]. Furthermore, admixture between Italian wolves and domestic dogs
did not affect the integrity of wolves’ gene pool [
207
]. The lack of significant effects on the
gene pool does not necessarily imply the lack of any effects, e.g., loss of reproductive effort.
Given that these effects were not studied, we classified this type of outcome as neutral.
No or Rare Evidence of Hybridization
This category includes studies that have not found any signs of hybridization in the
populations studied or found only very limited evidence e.g., [
154
,
208
–
215
]. We found
24 studies that fitted this category. This could include cases where hybridization was rare
or did not occur, as well as cases where limitations in sampling and the use of low number
of genetic makers could result in poor detection of hybridization [
216
–
225
]. The number
of genetic markers is important to detect signatures of hybridization, especially if cross-
breeding and/or back-crossing events are rare [
56
,
124
]. Moreover, small data sets may
show only a preliminary assessment of hybridization [226], and comprehensive sampling
is necessary to obtain reliable results.
Genes 2022,13, 50 16 of 26
In some cases, efficient conservation management may result in low rate of hybridiza-
tion [
212
,
227
]. For example, because of careful monitoring and management, the Scan-
dinavian wolf population shows a lower level of hybridization with dogs compared to
other European wolf populations, which was demonstrated based on the comprehensive
sampling and the analysis of whole genomes [
82
]. The rate of hybridization between the
same pairs of species may differ regionally depending on environmental conditions [
228
].
For example, hybridization between bat species Myotis myotis and Myotis blythii has been
reported in Europe, but in Turkey no signs of hybridization between these species have
been detected [229].
Altogether, 38% of the studies assessed in this systematic review reported neutral
or unspecified outcomes of hybridization. Within this group, “no or rare evidence of
hybridization” was the most common hybridization outcome, which occurred in 17% of
all the studies on hybridization. This result suggests that one of the five categories of
hybridization outcomes delineated for the purpose of species conservation [
35
], “negligible
impact and minimal introgression of genes into the species of concern”, occurs relatively
frequently. Therefore, a presumption that hybridization always constitutes a threat to
biodiversity is incorrect, and instead the decision-making regarding the management and
conservation of wild-living hybrids should be based on the examination of hybridization
outcomes case-by-case [35].
4.2.4. Consequences of Hybridization for Threatened Species
Only 18% of studies considered in this review were focused on threatened species
(having the IUCN Red List categories of Near Threatened (NT), Vulnerable (VU), Endan-
gered (EN), Critically Endangered (CR), Extinct in the Wild (EW)). Negative consequences
(e.g., genetic swamping, extinction via genetic swamping, introgression from domesticated
lineages and loss of reproductive output) were reported in 38% of these studies and positive
consequences (with only one category, gaining novel adaptive variation) were reported
in 14% of them. In the remaining studies, the authors did not mention any positive or
negative consequences or did not find any evidence of hybridization. The frequency of
the positive consequences reported for all the studies assessed in this systematic review
was very similar (13%), while the frequency of the negative consequences was higher (49%)
compared to those observed in the studies on threatened species. This suggests that the
negative consequences of hybridization are not intensified in endangered species, at least
the mammalian species considered in this review.
5. Conclusions
Among the papers included in this systematic review, hybridization outcomes typically
considered as negative had considerably higher frequency (49%) than those considered
as positive (13%). However, these frequencies could have been biased by several factors
and therefore should be treated with caution. For instance, two most frequent outcomes of
hybridization, genetic swamping and introgression of variants from domestic animals are
typically considered as negative, but this is not always the case. In some circumstances,
moderate levels of genetic swamping or introgression of domestication-related variants
may result in increased fitness and genetic rescue [
155
,
230
]. The cases where hybridization
outcomes are unequivocally negative, leading to extinction or loss of reproductive output,
are relatively rare. They were reported in 13% of the studies considered in this review—
the same frequency as that of the positive outcomes. In cases when the hybridization
outcome cannot be easily determined, e.g., when genetic swamping occurs at a low rate,
long-term monitoring of admixed populations is required to conclude about advantages
and disadvantages of introgressive hybridization. For this purpose, at least two consecutive
generations should be monitored [
12
,
13
], but currently, many studies are based on a singular
sampling effort, and fitness of sampled individuals is rarely assessed.
It is also important to stress that the detection of different outcomes of hybridization
depends on the type of molecular markers applied. Microsatellite markers enable identifi-
Genes 2022,13, 50 17 of 26
cation of first-generation hybrids and recent back-crosses, but cannot reliably detect more
distant hybridization events [
56
]. Since microsatellites are neutral genetic markers and
are typically genotyped in small numbers (<100), they cannot be used to detect adaptive
introgression or hybrid speciation, which are among the most frequently reported positive
outcomes of hybridization. In contrast, some negative outcomes, such as genetic swamp-
ing, can be detected using a small number of neutral markers. Given that until recently
microsatellite loci were the most frequently chosen markers in hybridization studies, and
they were used in 50% of studies considered in this systematic review, the frequency of
negative outcomes of hybridization may be overestimated.
A combination of neutral loci and those located within coding genes is better suited to
provide an unbiased insight into the relative frequencies of positive and negative hybridiza-
tion outcomes and identify factors that affect them. Single Nucleotide Polymorphisms
(SNPs) can be genotyped in large numbers (hundreds of thousands to millions) using arrays
or next generation sequencing, which makes them suitable for identification of adaptive
loci [
231
,
232
] as well as detection of small proportions of hybrid ancestry and identification
of F2-F4 backcrosses [
233
,
234
]. Therefore, the application of this type of genetic markers
creates an opportunity to identify both positive and negative impacts of hybridization.
In some circumstances, hybridization can be used as a conservation tool to facilitate
adaptation of populations to changing habitat conditions and to increase individual fitness
in populations experiencing inbreeding depression [
12
,
13
]. To use hybridization this
way, we need to achieve a better understanding on how to prevent negative effects of
hybridization without eliminating the potential for the positive effects. This will require
comprehensive studies focusing on the genetic effects of hybridization on both neutral
and functional parts of the genome and fitness effects of cross-breeding on F1 hybrids and
several generations of back-crosses. Experimental studies simulating different evolutionary
scenarios may be the best way to achieve an unbiased assessment of the frequency of
different hybridization outcomes.
Supplementary Materials:
The following are available online at https://www.mdpi.com/article/10
.3390/genes13010050/s1, Table S1: A list of papers considered in the systematic review.
Author Contributions:
R.A. carried out the literature review and wrote the first draft of the manuscript.
M.P. designed the study, supervised its implementation, and revised the manuscript. All authors
have read and agreed to the published version of the manuscript.
Funding:
This study was funded by the Polish National Science Centre (grant no. 2019/34/E/NZ8/
00246 to M.P.) and the Polish National Agency for Scientific Exchange—NAWA (Polish Returns
Fellowship PPN/PPO/2018/1/00037 to M.P.).
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement:
The references of 115 papers used as data source in the systematic
review are provided in the reference list. In addition, the list of these 115 papers is provided in the
Supplementary Table S1. The summary data from these studies is provided in the Results section.
Acknowledgments:
We thank three anonymous reviewers for their helpful comments on the
manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. Mayr, E. Animal Species and Evolution; Belknap: Cambridge, MA, USA, 1963.
2.
Taylor, S.A.; Larson, E. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat.
Ecol. Evol. 2019,3, 170–177. [CrossRef] [PubMed]
3. Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 2005,20, 229–237. [CrossRef] [PubMed]
4. Arnold, M.L. Natural Hybridization and Evolution; Oxford University Press on Demand: Oxford, UK, 1997.
Genes 2022,13, 50 18 of 26
5.
Nesi, N.; Nakoune, E.; Cruaud, C.; Hassanin, A. DNA barcoding of African fruit bats (Mammalia, Pteropodidae). The mitochon-
drial genome does not provide a reliable discrimination between Epomophorus Gamb and Micropteropus pusillus.C. R. Biol.
2011
,
334, 544–554. [CrossRef] [PubMed]
6.
Abbott, R.; Barton, N.H.; Good, J.M. Genomics of hybridization and its evolutionary consequences. Mol. Ecol.
2016
,25, 2325–2332.
[CrossRef]
7.
Goulet, B.E.; Roda, F.; Hopkins, R. Hybridization in Plants: Old Ideas, New Techniques. Plant Physiol.
2017
,173, 65–78. [CrossRef]
[PubMed]
8.
Wayne, R.K.; Shaffer, H.B. Hybridization and endangered species protection in the molecular era. Mol. Ecol.
2016
,25, 2680–2689.
[CrossRef]
9.
Mota, M.R.; Pinheiro, F.; Leal, B.S.S.; Wendt, T.; Palma-Silva, C. The role of hybridization and introgression in maintaining species
integrity and cohesion in naturally isolated inselberg bromeliad populations. Plant Biol.
2019
,21, 122–132. [CrossRef] [PubMed]
10.
Brennan, A.C.; Woodward, G.; Seehausen, O.; Muñoz-Fuentes, V.; Moritz, C.; Guelmami, A.; Abbott, R.J.; Edelaar, P. Hybridization
due to changing species distributions: Adding problems or solutions to conservation of biodiversity during global change? Evol.
Ecol. Res. 2015,16, 475–491.
11.
Lavrenchenko, L.A.; Bulatova, N.S. The role of hybrid zones in speciation: A case study on chromosome races of the house mouse
Mus domesticus and common shrew Sorex araneus.Biol. Bull. Rev. 2016,6, 232–244. [CrossRef]
12.
Chan, W.Y.; Peplow, L.M.; Menéndez, P.; Hoffmann, A.; van Oppen, M. Interspecific Hybridization May Provide Novel
Opportunities for Coral Reef Restoration. Front. Mar. Sci. 2018,5, 160. [CrossRef]
13.
Hamilton, J.A.; Miller, J. Adaptive introgression as a resource for management and genetic conservation in a changing climate.
Conserv. Biol. 2016,30, 33–41. [CrossRef]
14. Hoffmann, A.A.; Sgro, C. Climate change and evolutionary adaptation. Nature 2011,470, 479–485. [CrossRef]
15.
Olano-Marin, J.; Plis, K.; Sönnichsen, L.; Borowik, T.; Niedziałkowska, M.; J˛edrzejewska, B. Weak population structure in
European roe deer (Capreolus capreolus) and evidence of introgressive hybridization with Siberian roe deer (C. pygargus) in
northeastern Poland. PLoS ONE 2014,9, e109147.
16. Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 2004,19, 198–207. [CrossRef] [PubMed]
17.
Abbott, R.; Albach, D.; Ansell, S.; Arntzen, J.W.; Baird, S.J.; Bierne, N.; Boughman, J.; Brelsford, A.; Buerkle, C.A.; Buggs, R.
Hybridization and speciation. J. Evol. Biol. 2013,26, 229–246. [CrossRef]
18. Mallet, J. Hybrid speciation. Nature 2007,446, 279–283. [CrossRef]
19. Lavrenchenko, L. Hybrid speciation in mammals: Illusion or reality? Biol. Bull. Rev. 2014,4, 198–209. [CrossRef]
20.
Canu, A.; Vilaça, S.; Iacolina, L.; Apollonio, M.; Bertorelle, G.; Scandura, M. Lack of polymorphism at the MC1R wild-type allele
and evidence of domestic allele introgression across European wild boar populations. Mamm. Biol.
2016
,81, 477–479. [CrossRef]
21.
Zemanová, B.; Hájková, P.; Hájek, B.; Martínková, N.; Mikulíˇcek, P.; Zima, J.; Bryja, J. Extremely low genetic variation in
endangered Tatra chamois and evidence for hybridization with an introduced Alpine population. Conserv. Genet.
2015
,16, 729–741.
[CrossRef]
22.
Ruiz-García, M.; Pinedo-Castro, M.; Shostell, J.M. Small spotted bodies with multiple specific mitochondrial DNAs: Existence of
diverse and differentiated tigrina lineages or species (Leopardus spp.: Felidae, Mammalia) throughout Latin America. Mitochondrial
DNA Part A 2018,29, 993–1014. [CrossRef]
23.
Draper, D.; Laguna, E.; Marques, I. Demystifying Negative Connotations of Hybridization for Less Biased Conservation Policies.
Front. Ecol. Evol. 2021,9, 268. [CrossRef]
24.
Cairns, K.M.; Nesbitt, B.J.; Laffan, S.W.; Letnic, M.; Crowther, M.S. Geographic hot spots of dingo genetic ancestry in southeastern
Australia despite hybridisation with domestic dogs. Conserv. Genet. 2020,21, 77–90. [CrossRef]
25. Harris, K.; Nielsen, R. The Genetic Cost of Neanderthal Introgression. Genetics 2016,203, 881–891. [CrossRef] [PubMed]
26.
Beauclerc, K.B.; Bowman, J.; Schulte-Hostedde, A.I. Assessing the cryptic invasion of a domestic conspecific: A merican mink in
their native range. Ecol. Evol. 2013,3, 2296–2309. [CrossRef]
27.
Grobler, P.; van Wyk, A.M.; Dalton, D.L.; van Vuuren, B.J.; Kotzé, A. Assessing introgressive hybridization between blue
wildebeest (Connochaetes taurinus) and black wildebeest (Connochaetes gnou) from South Africa. Conserv. Genet.
2018
,19, 981–993.
[CrossRef]
28.
Koutsogiannouli, E.A.; Moutou, K.A.; Sarafidou, T.; Stamatis, C.; Mamuris, Z. Detection of hybrids between wild boars (Sus scrofa
scrofa) and domestic pigs (Sus scrofa f. domestica) in Greece, using the PCR-RFLP method on melanocortin-1 receptor (MC1R)
mutations. Mamm. Biol. 2010,75, 69–73. [CrossRef]
29.
Colella, J.P.; Wilson, R.E.; Talbot, S.L.; Cook, J.A. Implications of introgression for wildlife translocations: The case of North
American martens. Conserv. Genet. 2019,20, 153–166. [CrossRef]
30.
Drygala, F.; Rode-Margono, J.; Semiadi, G.; Frantz, A.C. Evidence of hybridisation between the common Indonesian banded pig
(Sus scrofa vitattus) and the endangered Java warty pig (Sus verrucosus). Conserv. Genet. 2020,21, 1073–1078. [CrossRef]
31.
Haus, T.; Roos, C.; Zinner, D. Discordance between spatial distributions of Y-chromosomal and mitochondrial haplotypes in
African green monkeys (Chlorocebus spp.): A result of introgressive hybridization or cryptic diversity? Int. J. Primatol.
2013
,34,
986–999. [CrossRef]
32.
Todesco, M.; Pascual, M.A.; Owens, G.L.; Ostevik, K.L.; Moyers, B.T.; Hübner, S.; Heredia, S.M.; Hahn, M.A.; Caseys, C.; Bock,
D.G. Hybridization and extinction. Evol. Appl. 2016,9, 892–908. [CrossRef]
Genes 2022,13, 50 19 of 26
33.
Balao, F.; Casimiro-Soriguer, R.; García-Castaño, J.L.; Terrab, A.; Talavera, S. Big thistle eats the little thistle: Does unidirectional
introgressive hybridization endanger the conservation of Onopordum hinojense?New Phytol. 2015,206, 448–458. [CrossRef]
34.
Lepais, O.; Petit, R.; Guichoux, E.; Lavabre, J.; Alberto, F.; Kremer, A.; Gerber, S. Species relative abundance and direction of
introgression in oaks. Mol. Ecol. 2009,18, 2228–2242. [CrossRef] [PubMed]
35.
Hirashiki, C.; Kareiva, P.; Marvier, M. Concern over hybridization risks should not preclude conservation interventions. Conserv.
Sci. Pract. 2021,3, e424. [CrossRef]
36.
Eva, S.N.; Yamazaki, Y. Hybridization between native and introduced individuals of sika deer in the central part of Toyama
Prefecture. Mammal Study 2018,43, 269–274. [CrossRef]
37.
Sagua, M.I.; Figueroa, C.; Acosta, D.; Fernández, G.; Carpinetti, B.; Birochio, D.; Merino, M.L. Inferring the origin and genetic
diversity of the introduced wild boar (Sus scrofa) populations in Argentina: An approach from mitochondrial markers. Mammal
Res. 2018,63, 467–476. [CrossRef]
38.
Pilot, M.; Greco, C.; vonHoldt, B.M.; Randi, E.; J˛edrzejewski, W.; Sidorovich, V.E.; Konopi´nski, M.K.; Ostrander, E.A.; Wayne,
R.K. Widespread, long-term admixture between grey wolves and domestic dogs across Eurasia and its implications for the
conservation status of hybrids. Evol. Appl. 2018,11, 662–680. [CrossRef]
39.
Iacolina, L.; Scandura, M.; Gazzola, A.; Cappai, N.; Capitani, C.; Mattioli, L.; Vercillo, F.; Apollonio, M. Y-chromosome
microsatellite variation in Italian wolves: A contribution to the study of wolf-dog hybridization patterns. Mamm. Biol.
2010
,75,
341–347. [CrossRef]
40.
Hulva, P.; ˇ
CernáBolfíková, B.; Woznicová, V.; Jindˇrichová, M.; Benešová, M.; Mysłajek, R.W.; Nowak, S.; Szewczyk, M.;
Nied´zwiecka, N.; Figura, M. Wolves at the crossroad: Fission–fusion range biogeography in the Western Carpathians and Central
Europe. Divers. Distrib. 2018,24, 179–192. [CrossRef]
41.
Munoz-Fuentes, V.; Darimont, C.T.; Paquet, P.C.; Leonard, J.A. The genetic legacy of extirpation and re-colonization in Vancouver
Island wolves. Conserv. Genet. 2010,11, 547–556. [CrossRef]
42.
Santostasi, N.L.; Gimenez, O.; Caniglia, R.; Fabbri, E.; Molinari, L.; Reggioni, W.; Ciucci, P. Estimating Admixture at the Population
Scale: Taking Imperfect Detectability and Uncertainty in Hybrid Classification Seriously. J. Wildl. Manag. 2021. [CrossRef]
43.
Cairns, K.M.; Newman, K.D.; Crowther, M.S.; Letnic, M. Pelage variation in dingoes across southeastern Australia: Implications
for conservation and management. J. Zool. 2021,314, 104–115. [CrossRef]
44.
Mattucci, F.; Oliveira, R.; Lyons, L.A.; Alves, P.C.; Randi, E. European wildcat populations are subdivided into five main
biogeographic groups: Consequences of Pleistocene climate changes or recent anthropogenic fragmentation? Ecol. Evol.
2016
,6,
3–22. [CrossRef] [PubMed]
45.
Beutel, T.; Reineking, B.; Tiesmeyer, A.; Nowak, C.; Heurich, M. Spatial patterns of co-occurrence of the European wildcat Felis
silvestris silvestris and domestic cats Felis silvestris catus in the Bavarian Forest National Park. Wildl. Biol. 2017,2017. [CrossRef]
46.
Oliveira, R.; Randi, E.; Mattucci, F.; Kurushima, J.; Lyons, L.A.; Alves, P. Toward a genome-wide approach for detecting hybrids:
Informative SNPs to detect introgression between domestic cats and European wildcats (Felis silvestris). Heredity
2015
,115,
195–205. [CrossRef]
47.
Le Roux, J.J.; Foxcroft, L.C.; Herbst, M.; MacFadyen, S. Genetic analysis shows low levels of hybridization between A frican
wildcats (Felis silvestris lybica) and domestic cats (F. s. catus) in South Africa. Ecol. Evol. 2015,5, 288–299. [CrossRef]
48. Boitani, L. Genetic considerations on wolf conservation in Italy. Ital. J. Zool. 1984,51, 367–373. [CrossRef]
49.
Gottelli, D.; Sillero-Zubiri, C.; Applebaum, G.D.; Roy, M.S.; Girman, D.J.; Garcia-Moreno, J.; Ostrander, E.A.; Wayne, R.K.
Molecular genetics of the most endangered canid: The Ethiopian wolf Canis simensis.Mol. Ecol.
1994
,3, 301–312. [CrossRef]
[PubMed]
50. Randi, E. Genetics and conservation of wolves Canis lupus in Europe. Mammal Rev. 2011,41, 99–111. [CrossRef]
51.
Torres, R.T.; Ferreira, E.; Rocha, R.G.; Fonseca, C. Hybridization between wolf and domestic dog: First evidence from an
endangered population in central Portugal. Mamm. Biol. 2017,86, 70–74. [CrossRef]
52.
Popova, E.; Zlatanova, D. Living a dog’s life: A putative gray wolf in a feral dog group. Mammalia
2020
,84, 115–120. [CrossRef]
53.
Saetre, P.; Lindberg, J.; Leonard, J.A.; Olsson, K.; Pettersson, U.; Ellegren, H.; Bergström, T.F.; Vila, C.; Jazin, E. From wild wolf to
domestic dog: Gene expression changes in the brain. Mol. Brain Res. 2004,126, 198–206. [CrossRef]
54.
Lounsberry, Z.T.; Quinn, C.B.; Statham, M.J.; Angulo, C.L.; Kalani, T.J.; Tiller, E.; Sacks, B.N. Investigating genetic introgression
from farmed red foxes into the wild population in Newfoundland, Canada. Conserv. Genet. 2017,18, 383–392. [CrossRef]
55. Arnold, M.L.; Martin, N.H. Hybrid fitness across time and habitats. Trends Ecol. Evol. 2010,25, 530–536. [CrossRef] [PubMed]
56.
McFarlane, S.E.; Pemberton, J.M. Detecting the true extent of introgression during anthropogenic hybridization. Trends Ecol. Evol.
2019,34, 315–326. [CrossRef] [PubMed]
57. Shurtliff, Q.R. Mammalian hybrid zones: A review. Mammal Rev. 2013,43, 1–21. [CrossRef]
58. Petit, R.J.; Excoffier, L. Gene flow and species delimitation. Trends Ecol. Evol. 2009,24, 386–393. [CrossRef]
59.
Iacolina, L.; Corlatti, L.; Buzan, E.; Safner, T.; Šprem, N. Hybridisation in European ungulates: An overview of the current status,
causes, and consequences. Mammal Rev. 2019,49, 45–59. [CrossRef]
60.
Morgan-Richards, M.; Smissen, R.D.; Shepherd, L.D.; Wallis, G.P.; Hayward, J.J.; Chan, C.H.; Chambers, G.K.; Chapman, H.M. A
review of genetic analyses of hybridisation in New Zealand. J. R. Soc. N. Z. 2009,39, 15–34. [CrossRef]
61.
Sinclair, A.R.E. Mammal population regulation, keystone processes and ecosystem dynamics. Philos. Trans. R. Soc. B Biol. Sci.
2003,358, 1729–1740. [CrossRef]
Genes 2022,13, 50 20 of 26
62.
Wilson, D.E.; Reeder, D.M. Mammal Species of the World: A Taxonomic and Geographic Reference; JHU Press: Baltimore, MD, USA,
2005; Volume 1.
63.
Tolesa, Z.; Bekele, E.; Tesfaye, K.; Ben Slimen, H.; Valqui, J.; Getahun, A.; Hartl, G.B.; Suchentrunk, F. Mitochondrial and nuclear
DNA reveals reticulate evolution in hares (Lepus spp., Lagomorpha, Mammalia) from Ethiopia. PLoS ONE
2017
,12, e0180137.
[CrossRef]
64. Grobler, J.P.; Hayter, K.N.; Labuschagne, C.; Nel, E.; Coetzer, W.G. The genetic status of naturally occurring black-nosed impala
from northern South Africa. Mamm. Biol. 2017,82, 27–33. [CrossRef]
65.
Moura, A.E.; Tsingarska, E.; D ˛abrowski, M.J.; Czarnomska, S.D.; J˛edrzejewska, B.; Pilot, M. Unregulated hunting and genetic
recovery from a severe population decline: The cautionary case of Bulgarian wolves. Conserv. Genet.
2014
,15, 405–417. [CrossRef]
66.
Cairns, K.M.; Brown, S.K.; Sacks, B.N.; Ballard, J.W.O. Conservation implications for dingoes from the maternal and paternal
genome: Multiple populations, dog introgression, and demography. Ecol. Evol. 2017,7, 9787–9807. [CrossRef]
67.
Canu, A.; Apollonio, M.; Scandura, M. Unmasking the invader: Genetic identity of invasive wild boar from three minor islands
off Sardinia (Italy). Mamm. Biol. 2018,93, 29–37. [CrossRef]
68.
Artyushin, I.; Bannikova, A.; Lebedev, V.; Kruskop, S. Mitochondrial DNA relationships among North Palaearctic Eptesicus
(Vespertilionidae, Chiroptera) and past hybridization between common serotine and northern bat. Zootaxa 2009,2262, 40–52.
69.
Berthier, P.; Excoffier, L.; Ruedi, M. Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species
Myotis myotis and Myotis blythii.Proc. R. Soc. B Biol. Sci. 2006,273, 3101–3123. [CrossRef]
70.
Bogdanowicz, W.; Van Den Bussche, R.A.; Gajewska, M.; Postawa, T.; Harutyunyan, M. Ancient and contemporary DNA sheds
light on the history of mouse-eared bats in Europe and the Caucasus. Acta Chiropterol. 2009,11, 289–305. [CrossRef]
71.
Hoffmann, F.G.; Owen, J.G.; Baker, R.J. mtDNA perspective of chromosomal diversification and hybridization in Peters’ tent-
making bat (Uroderma bilobatum: Phyllostomidae). Mol. Ecol. 2003,12, 2981–2993. [CrossRef]
72.
Afonso, E.; Goydadin, A.-C.; Giraudoux, P.; Farny, G. Investigating hybridization between the two sibling bat species Myotis
myotis and M. blythii from guano in a natural mixed maternity colony. PLoS ONE 2017,12, e0170534. [CrossRef]
73.
Vallo, P.; Benda, P.; ˇ
Cervený, J.; Koubek, P. Conflicting mitochondrial and nuclear paraphyly in small-sized West African house
bats (Vespertilionidae). Zool. Scr. 2013,42, 1–12. [CrossRef]
74. Bogdanowicz, W.; Piksa, K.; Tereba, A. Hybridization hotspots at bat swarming sites. PLoS ONE 2012,7, e53334. [CrossRef]
75.
Arlettaz, R.; Christe, P.; Lugon, A.; Perrin, N.; Vogel, P. Food availability dictates the timing of parturition in insectivorous
mouse-eared bats. Oikos 2001,95, 105–111. [CrossRef]
76.
Linnell, J.D.; Swenson, J.E.; Andersen, R. Conservation of biodiversity in Scandinavian boreal forests: Large carnivores as
flagships, umbrellas, indicators, or keystones? Biodivers. Conserv. 2000,9, 857–868. [CrossRef]
77.
Macdonald, E.; Burnham, D.; Hinks, A.; Dickman, A.; Malhi, Y.; Macdonald, D. Conservation inequality and the charismatic cat:
Felis felicis. Glob. Ecol. Conserv. 2015,3, 851–866. [CrossRef]
78.
Tensen, L. Biases in wildlife and conservation research, using felids and canids as a case study. Glob. Ecol. Conserv.
2018
,15,
e00423. [CrossRef]
79.
Tisdell, C.; Nantha, H.S.; Wilson, C. Endangerment and likeability of wildlife species: How important are they for payments
proposed for conservation? Ecol. Econ. 2007,60, 627–633. [CrossRef]
80. Nyhus, P.J. Human–wildlife conflict and coexistence. Annu. Rev. Environ. Resour. 2016,41, 143–171. [CrossRef]
81.
Caniglia, R.; Fabbri, E.; Galaverni, M.; Milanesi, P.; Randi, E. Noninvasive sampling and genetic variability, pack structure, and
dynamics in an expanding wolf population. J. Mammal. 2014,95, 41–59. [CrossRef]
82.
Smeds, L.; Aspi, J.; Berglund, J.; Kojola, I.; Tirronen, K.; Ellegren, H. Whole-genome analyses provide no evidence for dog
introgression in Fennoscandian wolf populations. Evol. Appl. 2021,14, 721–734. [CrossRef] [PubMed]
83.
Boggiano, F.; Ciofi, C.; Boitani, L.; Formia, A.; Grottoli, L.; Natali, C.; Ciucci, P. Detection of an East European wolf haplotype
puzzles mitochondrial DNA monomorphism of the Italian wolf population. Mamm. Biol. 2013,78, 374–378. [CrossRef]
84.
Pilot, M.; Moura, A.E.; Okhlopkov, I.M.; Mamaev, N.V.; Alagaili, A.N.; Mohammed, O.B.; Yavruyan, E.G.; Manaseryan, N.H.;
Hayrapetyan, V.; Kopaliani, N. Global phylogeographic and admixture patterns in grey wolves and genetic legacy of an ancient
Siberian lineage. Sci. Rep. 2019,9, 1–13. [CrossRef]
85.
Zwijacz-Kozica, T.; Wa ˙
zna, A.; Muñoz-Fuentes, V.; Tiesmeyer, A.; Cichocki, J.; Nowak, C. Not European wildcats, but domestic
cats inhabit Tatra National Park. Pol. J. Ecol. 2017,65, 415–421. [CrossRef]
86.
Nussberger, B.; Wandeler, P.; Weber, D.; Keller, L.F. Monitoring introgression in European wildcats in the Swiss Jura. Conserv.
Genet. 2014,15, 1219–1230. [CrossRef]
87.
Leonard, J.A.; Echegaray, J.; Rand, E.; Vilà, C. Impact of hybridization with domestic dogs on the conservation of wild canids.
Free Ranging Dogs Wildl. Conserv. 2013,170, 170–184. [CrossRef]
88.
Ottoni, C.; Van Neer, W.; De Cupere, B.; Daligault, J.; Guimaraes, S.; Peters, J.; Spassov, N.; Prendergast, M.E.; Boivin, N.;
Morales-Muñiz, A. The palaeogenetics of cat dispersal in the ancient world. Nat. Ecol. Evol. 2017,1, 1–7. [CrossRef]
89. Vigne, J.-D.; Guilaine, J.; Debue, K.; Haye, L.; Gérard, P. Early taming of the cat in Cyprus. Science 2004,304, 259. [CrossRef]
90.
Gompper, M.E. The dog-human-wildlife interface: Assessing the scope of the problem. Free Ranging Dogs Wildl. Conserv.
2014
,
9–54. [CrossRef]
91.
Adams, J.R.; Leonard, J.A.; Waits, L.P. Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern
US coyotes. Mol. Ecol. 2003,12, 541–546. [CrossRef]
Genes 2022,13, 50 21 of 26
92.
Vilà, C.; Maldonado, J.E.; Wayne, R.K. Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J. Hered.
1999,90, 71–77. [CrossRef]
93.
Dzialuk, A.; Zastempowska, E.; Skórzewski, R.; Twaru˙
zek, M.; Grajewski, J. High domestic pig contribution to the local gene pool
of free-living European wild boar: A case study in Poland. Mammal Res. 2018,63, 65–71. [CrossRef]
94.
Apollonio, M.; Andersen, R.; Putman, R. European Ungulates and Their Management in the Twenty-First Century; Cambridge
University Press: Cambridge, UK, 2010.
95.
Herrero, J.; García-Serrano, A.; García-González, R. Reproductive and demographic parameters in two Iberian wild boar Sus
scrofa populations. Mammal Res. 2008,53, 355–364. [CrossRef]
96.
Massei, G.; Kindberg, J.; Licoppe, A.; Gaˇci´c, D.; Šprem, N.; Kamler, J.; Baubet, E.; Hohmann, U.; Monaco, A.; Ozoli
n
,
š, J. Wild boar
populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag. Sci.
2015
,71, 492–500.
[CrossRef]
97.
Vetter, S.G.; Ruf, T.; Bieber, C.; Arnold, W. What is a mild winter? Regional differences in within-species responses to climate
change. PLoS ONE 2015,10, e0132178. [CrossRef]
98.
Waithman, J.D.; Sweitzer, R.A.; Van Vuren, D.; Drew, J.D.; Brinkhaus, A.J.; Gardner, I.A.; Boyce, W.M. Range expansion, population
sizes, and management of wild pigs in California. J. Wildl. Manag. 1999,63, 298–308. [CrossRef]
99.
Frantz, A.C.; Zachos, F.E.; Kirschning, J.; Cellina, S.; Bertouille, S.; Mamuris, Z.; Koutsogiannouli, E.A.; Burke, T. Genetic evidence
for introgression between domestic pigs and wild boars (Sus scrofa) in Belgium and Luxembourg: A comparative approach with
multiple marker systems. Biol. J. Linn. Soc. 2013,110, 104–115. [CrossRef]
100.
García, G.; Vergara, J.; Lombardi, R. Genetic characterization and phylogeography of the wild boar Sus scrofa introduced into
Uruguay. Genet. Mol. Biol. 2011,34, 329–337. [CrossRef]
101.
Chai, Z.X.; Xin, J.W.; Zhang, C.F.; Zhang, Q.; Li, C.; Zhu, Y.; Cao, H.W.; Wang, H.; Han, J.L.; Ji, Q.M. Whole-genome resequencing
provides insights into the evolution and divergence of the native domestic yaks of the Qinghai–Tibet Plateau. BMC Evol. Biol.
2020,20, 1–10. [CrossRef]
102. Anderson, E.; Stebbins, G.L., Jr. Hybridization as an evolutionary stimulus. Evolution 1954,8, 378–388. [CrossRef]
103.
Flores-Manzanero, A.; Valenzuela-Galván, D.; Cuarón, A.D.; Vázquez-Domínguez, E. Conservation genetics of two critically
endangered island dwarf carnivores. Conserv. Genet. 2021, 1–15. [CrossRef]
104. Baskin, Y. A Plague of Rats and Rubbervines: The Growing Threat of Species Invasions; Island Press: Washington, DC, USA, 2013.
105. McNeely, J.A. The Great Reshuffling: Human Dimensions of Invasive Alien Species; IUCN: Gland, Switzerland, 2001.
106. Wittenberg, R.; Cock, M.J. Invasive Alien Species: A Toolkit of Best Prevention and Management Practices; CABI: Egham, UK, 2001.
107.
Queirós, J.; Gortázar, C.; Alves, P.C. Deciphering anthropogenic effects on the genetic background of the Red deer in the Iberian
Peninsula. Front. Ecol. Evol. 2020,8, 147. [CrossRef]
108.
Csányi, S.; Carranza, J.; Pokorny, B.; Putman, R.; Ryan, M. Valuing ungulates in Europe. In Behaviour and Management of European
Ungulates; Whittles: Dunbeath, UK, 2014; pp. 13–45.
109. Lever, C. Naturalized Mammals of the World; Longman: Harlow, UK, 1985.
110.
Kalb, D.M.; Bowman, J.L. A complete history of the establishment of Japanese sika deer on the Delmarva Peninsula: 100 years
post-introduction. Biol. Invasions 2017,19, 1705–1713. [CrossRef]
111.
Krojerová-Prokešová, J.; Baranˇceková, M.; Kawata, Y.; Oshida, T.; Igota, H.; Koubek, P. Genetic differentiation between introduced
Central European sika and source populations in Japan: Effects of isolation and demographic events. Biol. Invasions
2017
,19,
2125–2141. [CrossRef]
112.
Takagi, T.; Matsumoto, Y.; Koda, R.; Tamate, H.B. Bi-directional movement of deer between Tomogashima islands and the western
part of the Kii Peninsula, Japan, with special reference to hybridization between the Japanese sika deer (Cervus nippon centralis)
and the introduced exotic deer. Mammal Study 2020,45, 133–141. [CrossRef]
113.
´
Swisłocka, M.; Czajkowska, M.; Matosiuk, M.; Saveljev, A.P.; Ratkiewicz, M.; Borkowska, A. No evidence for recent introgressive
hybridization between the European and Siberian roe deer in Poland. Mamm. Biol. 2019,97, 59–63. [CrossRef]
114.
Mucci, N.; Mattucci, F.; Randi, E. Conservation of threatened local gene pools: Landscape genetics of the Italian roe deer (Capreolus
c. italicus) populations. Evol. Ecol. Res. 2012,14, 897–920.
115.
Do Nascimento Schaurich, M.; Lopes, F.R.V.; de Oliveira, L.R. Hybridization phenomenon in cetacean and pinniped species.
Neotrop. Biol. Conserv. 2012,7, 199–209.
116.
Glover, K.A.; Kanda, N.; Haug, T.; Pastene, L.A.; Øien, N.; Seliussen, B.B.; Sørvik, A.G.; Skaug, H.J. Hybrids between common
and Antarctic minke whales are fertile and can back-cross. BMC Genet. 2013,14, 1–11. [CrossRef]
117.
Crossman, C.A.; Taylor, E.B.; Barrett-Lennard, L.G. Hybridization in the Cetacea: Widespread occurrence and associated
morphological, behavioral, and ecological factors. Ecol. Evol. 2016,6, 1293–1303. [CrossRef]
118.
Miralles, L.; Lens, S.; Rodriguez-Folgar, A.; Carrillo, M.; Martin, V.; Mikkelsen, B.; Garcia-Vazquez, E. Interspecific introgression
in cetaceans: DNA markers reveal post-F1 status of a pilot whale. PLoS ONE 2013,8, e69511. [CrossRef] [PubMed]
119.
Guo, W.; Sun, D.; Cao, Y.; Xiao, L.; Huang, X.; Ren, W.; Xu, S.; Yang, G. Extensive Interspecific Gene Flow Shaped Complex
Evolutionary History and Underestimated Species Diversity in Rapidly Radiated Dolphins. J. Mamm. Evol.
2021
, 1–15. [CrossRef]
120.
Bérubé, M.; Palsbøll, P.J. Hybridism. In Encyclopedia of Marine Mammals; Elsevier: Amsterdam, The Netherlands, 2018; pp. 496–501.
121.
Willis, P.M.; Crespi, B.J.; Dill, L.M.; Baird, R.W.; Hanson, M.B. Natural hybridization between Dall’s porpoises (Phocoenoides dalli)
and harbour porpoises (Phocoena phocoena). Can. J. Zool. 2004,82, 828–834. [CrossRef]
Genes 2022,13, 50 22 of 26
122.
Brown, A.M.; Kopps, A.M.; Allen, S.J.; Bejder, L.; Littleford-Colquhoun, B.; Parra, G.J.; Cagnazzi, D.; Thiele, D.; Palmer, C.; Frere,
C.H. Population differentiation and hybridisation of Australian snubfin (Orcaella heinsohni) and Indo-Pacific humpback (Sousa
chinensis) dolphins in north-western Australia. PLoS ONE 2014,9, e101427. [CrossRef]
123.
Pampoulie, C.; Gíslason, D.; Ólafsdóttir, G.; Chosson, V.; Halldórsson, S.D.; Mariani, S.; Elvarsson, B.Þ.; Rasmussen, M.H.; Iversen,
M.R.; Daníelsdóttir, A.K. Evidence of unidirectional hybridization and second-generation adult hybrid between the two largest
animals on Earth, the fin and blue whales. Evol. Appl. 2021,14, 314–321. [CrossRef]
124.
Quilodrán, C.S.; Montoya-Burgos, J.I.; Currat, M. Harmonizing hybridization dissonance in conservation. Commun. Biol.
2020
,3,
1–10. [CrossRef] [PubMed]
125.
Allendorf, F.W.; Leary, R.F.; Spruell, P.; Wenburg, J.K. The problems with hybrids: Setting conservation guidelines. Trends Ecol.
Evol. 2001,16, 613–622. [CrossRef]
126.
Frankham, R.; Ballou, J.D.; Eldridge, M.D.; Lacy, R.C.; Ralls, K.; Dudash, M.R.; Fenster, C.B. Predicting the probability of
outbreeding depression. Conserv. Biol. 2011,25, 465–475. [CrossRef]
127.
Brekke, T.D.; Henry, L.A.; Good, J.M. Genomic imprinting, disrupted placental expression, and speciation. Evolution
2016
,70,
2690–2703. [CrossRef]
128.
van Wyk, A.M.; Kotzé, A.; Randi, E.; Dalton, D.L. A hybrid dilemma: A molecular investigation of South African bontebok
(Damaliscus pygargus pygargus) and blesbok (Damaliscus pygargus phillipsi). Conserv. Genet. 2013,14, 589–599. [CrossRef]
129.
Bozarth, C.A.; Hailer, F.; Rockwood, L.L.; Edwards, C.W.; Maldonado, J.E. Coyote colonization of northernVirginia and admixture
with Great Lakes wolves. J. Mammal. 2011,92, 1070–1080. [CrossRef]
130.
Garcia-Elfring, A.; Barrett, R.; Combs, M.; Davies, T.; Munshi-South, J.; Millien, V. Admixture on the northern front: Population
genomics of range expansion in the white-footed mouse (Peromyscus leucopus) and secondary contact with the deer mouse
(Peromyscus maniculatus). Heredity 2017,119, 447–458. [CrossRef]
131.
Brekke, T.D.; Good, J.M. Parent-of-origin growth effects and the evolution of hybrid inviability in dwarf hamsters. Evolution
2014
,
68, 3134–3148. [CrossRef] [PubMed]
132.
Neaves, L.E.; Zenger, K.; Cooper, D.W.; Eldridge, M. Molecular detection of hybridization between sympatric kangaroo species in
south-eastern Australia. Heredity 2010,104, 502–512. [CrossRef]
133.
Templeton, A.R.; Hemmer, H.; Mace, G.; Seal, U.S.; Shields, W.M.; Woodruff, D.S. Local adaptation, coadaptation, and population
boundaries. Zoo Biol. 1986,5, 115–125. [CrossRef]
134.
Bell, D.A.; Robinson, Z.L.; Funk, W.C.; Fitzpatrick, S.W.; Allendorf, F.W.; Tallmon, D.A.; Whiteley, A.R. The exciting potential and
remaining uncertainties of genetic rescue. Trends Ecol. Evol. 2019,34, 1070–1079. [CrossRef]
135.
Mallil, K.; Justy, F.; Rueness, E.K.; Dufour, S.; Totis, T.; Bloch, C.; Baarman, J.; Amroun, M.; Gaubert, P. Population genetics of the
African wolf (Canis lupaster) across its range: First evidence of hybridization with domestic dogs in Africa. Mamm. Biol.
2020
,100,
645–658. [CrossRef]
136.
Smith, S.L.; Senn, H.V.; Pérez-Espona, S.; Wyman, M.T.; Heap, E.; Pemberton, J.M. Introgression of exotic Cervus (nippon and
canadensis) into red deer (Cervus elaphus) populations in Scotland and the English Lake District. Ecol. Evol.
2018
,8, 2122–2134.
[CrossRef]
137.
Bifolchi, A.; Picard, D.; Lemaire, C.; Cormier, J.; Pagano, A. Evidence of admixture between differentiated genetic pools at a
regional scale in an invasive carnivore. Conserv. Genet. 2010,11, 1–9. [CrossRef]
138.
Zhigileva, O.N.; Uslamina, I.M.; Gimranov, D.O.; Chernova, A.A. Mitochondrial DNA markers for the study of introgression
between the sable and the pine marten. Conserv. Genet. Resour. 2020,12, 329–336. [CrossRef]
139.
Pilot, M.; Moura, A.E.; Okhlopkov, I.M.; Mamaev, N.V.; Manaseryan, N.H.; Hayrapetyan, V.; Kopaliani, N.; Tsingarska, E.;
Alagaili, A.N.; Mohammed, O.B. Human-modified canids in human-modified landscapes: The evolutionary consequences of
hybridisation for grey wolves and free-ranging domestic dogs. Evol. Appl. 2021,14, 2433–2456. [CrossRef]
140.
Gómez, J.M.; González-Megías, A.; Lorite, J.; Abdelaziz, M.; Perfectti, F. The silent extinction: Climate change and the potential
hybridization-mediated extinction of endemic high-mountain plants. Biodivers. Conserv. 2015,24, 1843–1857. [CrossRef]
141.
La Morgia, V.; Venturino, E. Understanding hybridization and competition processes between hare species: Implications for
conservation and management on the basis of a mathematical model. Ecol. Model. 2017,364, 13–24. [CrossRef]
142.
Godwin, J.L.; Lumley, A.J.; Michalczyk, Ł.; Martin, O.Y.; Gage, M.J. Mating patterns influence vulnerability to the extinction
vortex. Glob. Chang. Biol. 2020,26, 4226–4239. [CrossRef] [PubMed]
143.
Soulé, M.; Gilpin, M.; Conway, W.; Foose, T. The millenium ark: How long a voyage, how many staterooms, how many
passengers? Zoo Biol. 1986,5, 101–113. [CrossRef]
144.
Ralls, K.; Ballou, J.D.; Frankham, R. Inbreeding and outbreeding. In Encyclopedia of Biodiversity; Elsevier: Amsterdam,
The Netherlands, 2001.
145.
Biedrzycka, A.; Solarz, W.; Okarma, H. Hybridization between native and introduced species of deer in Eastern Europe. J.
Mammal. 2012,93, 1331–1341. [CrossRef]
146.
Muhlfeld, C.C.; Kalinowski, S.T.; McMahon, T.E.; Taper, M.L.; Painter, S.; Leary, R.F.; Allendorf, F.W. Hybridization rapidly
reduces fitness of a native trout in the wild. Biol. Lett. 2009,5, 328–331. [CrossRef]
147.
Templeton, A.R. Coadaptation and outbreeding depression. In Conservation Biology: The Science of Scarcity and Diversity; Sinauer
Associates: Sunderland, MA, USA, 1986; pp. 105–116.
Genes 2022,13, 50 23 of 26
148.
Piorno, V.; Villafuerte, R.; Branco, M.; Carneiro, M.; Ferrand, N.; Alves, P. Low persistence in nature of captive reared rabbits after
restocking operations. Eur. J. Wildl. Res. 2015,61, 591–599. [CrossRef]
149.
Berejikian, B.A.; Ford, M.J. Review of Relative Fitness of Hatchery and Natural Salmon. 2004. Available online: https://www.
webapps.nwfsc.noaa.gov/assets/25/6429_02012005_154209_fitnesstm61final.pdf (accessed on 11 November 2021).
150. Fraser, D. Understanding animal welfare. Acta Vet. Scand. 2008,50, 1–7. [CrossRef] [PubMed]
151.
Kiik, K.; Maran, T.; Nagl, A.; Ashford, K.; Tammaru, T. The causes of the low breeding success of European mink (Mustela lutreola)
in captivity. Zoo Biol. 2013,32, 387–393. [CrossRef]
152.
Maran, T.; Põdra, M.; Põlma, M.; Macdonald, D.W. The survival of captive-born animals in restoration programmes–Case study
of the endangered European mink Mustela lutreola.Biol. Conserv. 2009,142, 1685–1692. [CrossRef]
153.
Randi, E. Detecting hybridization between wild species and their domesticated relatives. Mol. Ecol.
2008
,17, 285–293. [CrossRef]
154.
Wierzbicki, H.; Zato´n-Dobrowolska, M.; Mucha, A.; Moska, M. Insight into the Genetic Population Structure of Wild Red Foxes in
Poland Reveals Low Risk of Genetic Introgression from Escaped Farm Red Foxes. Genes 2021,12, 637. [CrossRef] [PubMed]
155.
Feulner, P.G.; Gratten, J.; Kijas, J.W.; Visscher, P.M.; Pemberton, J.M.; Slate, J. Introgression and the fate of domesticated genes in a
wild mammal population. Mol. Ecol. 2013,22, 4210–4221. [CrossRef] [PubMed]
156.
Grossen, C.; Keller, L.; Biebach, I.; Consortium, I.G.G.; Croll, D. Introgression from domestic goat generated variation at the major
histocompatibility complex of alpine ibex. PLoS Genet. 2014,10, e1004438. [CrossRef]
157.
Ackermann, R.R.; Brink, J.S.; Vrahimis, S.; De Klerk, B. Hybrid wildebeest (Artiodactyla: Bovidae) provide further evidence for
shared signatures of admixture in mammalian crania. S. Afr. J. Sci. 2010,106, 1–5. [CrossRef]
158.
Tobler, M.; Carson, E.W. Environmental variation, hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes.J.
Evol. Biol. 2010,23, 1475–1489. [CrossRef] [PubMed]
159.
Orr, H.A. Developmental anomalies in Drosophila hybrids are apparently caused by loss of microchromosome. Heredity
1990
,64,
255–262. [CrossRef]
160.
Ackermann, R.R. Phenotypic traits of primate hybrids: Recognizing admixture in the fossil record. Evol. Anthropol. Issues News
Rev. 2010,19, 258–270. [CrossRef]
161. Falconer, D.S. Introduction to Quantitative Genetics; Pearson Education India: London, UK, 1996.
162.
Stelkens, R.B.; Schmid, C.; Selz, O.; Seehausen, O. Phenotypic novelty in experimental hybrids is predicted by the genetic distance
between species of cichlid fish. BMC Evol. Biol. 2009,9, 1–13. [CrossRef]
163.
Tung, J.; Charpentier, M.J.; Mukherjee, S.; Altmann, J.; Alberts, S.C. Genetic effects on mating success and partner choice in a
social mammal. Am. Nat. 2012,180, 113–129. [CrossRef]
164.
Zorenko, T.A.; Atanasov, N.; Golenishchev, F.N. Behavioral differentiation and hybridization of the European and Asian forms of
Harting’vole Microtus hartingi (Rodentia, Arvicolinae). Russ. J. Theriol. 2016,15, 133–150. [CrossRef]
165.
Chan, W.Y.; Hoffmann, A.A.; van Oppen, M.J. Hybridization as a conservation management tool. Conserv. Lett.
2019
,12, e12652.
[CrossRef]
166.
Whiteley, A.R.; Fitzpatrick, S.W.; Funk, W.C.; Tallmon, D.A. Genetic rescue to the rescue. Trends Ecol. Evol.
2015
,30, 42–49.
[CrossRef]
167.
Ralls, K.; Sunnucks, P.; Lacy, R.C.; Frankham, R. Genetic rescue: A critique of the evidence supports maximizing genetic diversity
rather than minimizing the introduction of putatively harmful genetic variation. Biol. Conserv. 2020,251, 108784. [CrossRef]
168.
Salzburger, W.; Baric, S.; Sturmbauer, C. Speciation via introgressive hybridization in East African cichlids? Mol. Ecol.
2002
,11,
619–625. [CrossRef] [PubMed]
169.
Mohammadi, Z.; Aliabadian, M.; Ghorbani, F.; Moghaddam, F.Y.; Lissovsky, A.A.; Obst, M.; Olsson, U. Unidirectional Introgres-
sion and Evidence of Hybrid Superiority over Parental Populations in Eastern Iranian Plateau Population of Hares (Mammalia:
Lepus Linnaeus, 1758). J. Mamm. Evol. 2020,27, 723–743. [CrossRef]
170.
Chen, Z.-H.; Xu, Y.-X.; Xie, X.-L.; Wang, D.-F.; Aguilar-Gómez, D.; Liu, G.-J.; Li, X.; Esmailizadeh, A.; Rezaei, V.; Kantanen, J.
Whole-genome sequence analysis unveils different origins of European and Asiatic mouflon and domestication-related genes in
sheep. Commun. Biol. 2021,4, 1–15. [CrossRef]
171.
Okarma, H.; J˛edrzejewska, B.; J˛edrzejewski, W.; Krasi´nski, Z.A.; Miłkowski, L. The roles of predation, snow cover, acorn crop,
and man-related factors on ungulate mortality in Białowie˙
za Primeval Forest, Poland. Acta Theriol.
1995
,40, 197–217. [CrossRef]
172.
Kays, R.; Curtis, A.; Kirchman, J.J. Rapid adaptive evolution of northeastern coyotes via hybridization with wolves. Biol. Lett.
2010,6, 89–93. [CrossRef]
173.
Barlow, A.; Cahill, J.A.; Hartmann, S.; Theunert, C.; Xenikoudakis, G.; Fortes, G.G.; Paijmans, J.L.; Rabeder, G.; Frischauf, C.;
Grandal-d’Anglade, A. Partial genomic survival of cave bears in living brown bears. Nat. Ecol. Evol.
2018
,2, 1563–1570. [CrossRef]
[PubMed]
174.
Racimo, F.; Sankararaman, S.; Nielsen, R.; Huerta-Sánchez, E. Evidence for archaic adaptive introgression in humans. Nat. Rev.
Genet. 2015,16, 359–371. [CrossRef]
175.
Wang, M.-S.; Wang, S.; Li, Y.; Jhala, Y.; Thakur, M.; Otecko, N.O.; Si, J.-F.; Chen, H.-M.; Shapiro, B.; Nielsen, R. Ancient
hybridization with an unknown population facilitated high-altitude adaptation of canids. Mol. Biol. Evol.
2020
,37, 2616–2629.
[CrossRef]
176.
Ferreira, M.S.; Jones, M.R.; Callahan, C.M.; Farelo, L.; Tolesa, Z.; Suchentrunk, F.; Boursot, P.; Mills, L.S.; Alves, P.C.; Good, J.M.
The legacy of recurrent introgression during the radiation of hares. Syst. Biol. 2021,70, 593–607. [CrossRef]
Genes 2022,13, 50 24 of 26
177.
Sankararaman, S.; Mallick, S.; Patterson, N.; Reich, D. The combined landscape of Denisovan and Neanderthal ancestry in
present-day humans. Curr. Biol. 2016,26, 1241–1247. [CrossRef] [PubMed]
178.
Schumer, M.; Rosenthal, G.G.; Andolfatto, P. How common is homoploid hybrid speciation? Evolution
2014
,68, 1553–1560.
[CrossRef]
179.
Macholán, M. Hybrid Zone, Mouse. In Brenner’s Encyclopedia of Genetics, 2nd ed.; Maloy, S., Hughes, K., Eds.; Academic Press:
Cambridge, MA, USA, 2013; pp. 588–591.
180.
Chang, S.W.; Oshida, T.; Endo, H.; Nguyen, S.; Dang, C.; Nguyen, D.; Jiang, X.; Li, Z.J.; Lin, L.K. Ancient hybridization and
underestimated species diversity in Asian striped squirrels (genus Tamiops): Inference from paternal, maternal and biparental
markers. J. Zool. 2011,285, 128–138. [CrossRef]
181.
Detwiler, K.M. Mitochondrial DNA analyses of Cercopithecus monkeys reveal a localized hybrid origin for C. mitis doggetti in
Gombe National Park, Tanzania. Int. J. Primatol. 2019,40, 28–52. [CrossRef]
182.
Macholán, M.; Baird, S.J.; Dufková, P.; Munclinger, P.; Bímová, B.V.; Piálek, J. Assessing multilocus introgression patterns: A case
study on the mouse X chromosome in central Europe. Evol. Int. J. Org. Evol. 2011,65, 1428–1446. [CrossRef]
183.
Allen, W.L.; Stevens, M.; Higham, J.P. Character displacement of Cercopithecini primate visual signals. Nat. Commun.
2014
,5,
1–10. [CrossRef] [PubMed]
184.
Komárek, J.; Komárková-Legnerová, J. Phenotype diversity of the cyanoprokaryotic genus Cylindrospermopsis (Nostocales). Czech
Phycol. 2003,3, 1–30.
185.
Ito, T.; Kawamoto, Y.; Hamada, Y.; Nishimura, T.D. Maxillary sinus variation in hybrid macaques: Implications for the genetic
basis of craniofacial pneumatization. Biol. J. Linn. Soc. 2015,115, 333–347. [CrossRef]
186.
Grant, P.R.; Grant, B.R. Phenotypic and genetic effects of hybridization in Darwin’s finches. Evolution
1994
,48, 297–316. [CrossRef]
187.
Gridley, T.; Elwen, S.H.; Harris, G.; Moore, D.; Hoelzel, A.; Lampen, F. Hybridization in bottlenose dolphins—A case study of
Tursiops aduncus
×
T. truncatus hybrids and successful backcross hybridization events. PLoS ONE
2018
,13, e0201722. [CrossRef]
[PubMed]
188.
Cserkész, T.; Kiss, C.; Barkaszi, Z.; Görföl, T.; Zagorodniuk, I.; Sramkó, G.; Csorba, G. Intra-and interspecific morphological
variation in sympatric and allopatric populations of Mustela putorius and M. eversmanii (Carnivora: Mustelidae) and detection of
potential hybrids. Mammal Res. 2021,66, 103–114. [CrossRef]
189.
Balcarcel, A.; Sánchez-Villagra, M.R.; Segura, V.; Evin, A. Singular patterns of skull shape and brain size change in the domestica-
tion of South American camelids. J. Mammal. 2021,102, 220–235. [CrossRef]
190.
Frare, C.F.; Matocq, M.D.; Feldman, C.R.; White, A.M.; Manley, P.N.; Jermstad, K.D.; Hekkala, E.R. Landscape disturbance and
sporadic hybridization complicate field identification of chipmunks. J. Wildl. Manag. 2017,81, 248–258. [CrossRef]
191. Barton, N.H.; Hewitt, G.M. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 1985,16, 113–148. [CrossRef]
192. Barton, N.H.; Hewitt, G.M. Adaptation, speciation and hybrid zones. Nature 1989,341, 497–503. [CrossRef]
193. Harrison, R. Hybrid Zones and the Evolutionary Process; Oxford University Press: New York, NY, USA, 1993.
194. Woodruff, D.S. Natural hybridization and hybrid zones. Syst. Biol. 1973,22, 213–218. [CrossRef]
195.
Mauldin, M.R.; Haynie, M.L.; Hanson, J.D.; Baker, R.J.; Bradley, R.D. Multilocus characterization of a woodrat (genus Neotoma)
hybrid zone. J. Hered. 2014,105, 466–476. [CrossRef]
196.
Shurtliff, Q.R.; Murphy, P.J.; Matocq, M.D. Ecological segregation in a small mammal hybrid zone: Habitat-specific mating
opportunities and selection against hybrids restrict gene flow on a fine spatial scale. Evolution 2014,68, 729–742. [CrossRef]
197.
ˇ
Dureje, L’.; Macholán, M.; Baird, S.J.; Piálek, J. The mouse hybrid zone in Central Europe: From morphology to molecules. J.
Vertebr. Biol. 2012,61, 308–318. [CrossRef]
198.
Coyner, B.S.; Murphy, P.J.; Matocq, M.D. Hybridization and asymmetric introgression across a narrow zone of contact between
Neotoma fuscipes and N. macrotis (Rodentia: Cricetidae). Biol. J. Linn. Soc. 2015,115, 162–172. [CrossRef]
199.
Jahner, J.P.; Parchman, T.L.; Matocq, M.D. Multigenerational backcrossing and introgression between two woodrat species at an
abrupt ecological transition. Mol. Ecol. 2021,30, 4245–4258. [CrossRef]
200.
Mauldin, M.R.; Haynie, M.L.; Vrla, S.C.; Bradley, R.D. Temporal evaluation of a woodrat (genus Neotoma) hybrid zone based on
genotypic and georeferenced data. J. Mammal. 2021,102, 541–557. [CrossRef]
201.
Brandler, O.; Kapustina, S.; Nikol’skii, A.; Kolesnikov, V.; Badmaev, B.; Adiya, Y. A study of hybridization between Marmota
baibacina and M. sibirica in their secondary contact zone in Mongolian Altai. Front. Ecol. Evol. 2021,9, 363. [CrossRef]
202.
Gravena, W.; Da Silva, V.M.; Da Silva, M.N.; Farias, I.P.; Hrbek, T. Living between rapids: Genetic structure and hybridization in
botos (Cetacea: Iniidae: Inia spp.) of the Madeira River, Brazil. Biol. J. Linn. Soc. 2015,114, 764–777. [CrossRef]
203.
Campbell, C.D.; Cowan, P.; Gruber, B.; MacDonald, A.J.; Holleley, C.E.; Sarre, S.D. Has the introduction of two subspecies
generated dispersal barriers among invasive possums in New Zealand? Biol. Invasions 2021,23, 3831–3845. [CrossRef]
204.
Eldridge, M.D.; Pearson, D.J.; Potter, S. Identification of a novel hybrid zone within the black-footed rock-wallaby (Petrogale
lateralis) in Western Australia. Aust. J. Zool. 2021,68, 98–107. [CrossRef]
205.
Kinoshita, E.; Abramov, A.V.; Soloviev, V.A.; Saveljev, A.P.; Nishita, Y.; Kaneko, Y.; Masuda, R. Hybridization between the
European and Asian badgers (Meles, Carnivora) in the Volga-Kama region, revealed by analyses of maternally, paternally and
biparentally inherited genes. Mamm. Biol. 2019,94, 140–148. [CrossRef]
Genes 2022,13, 50 25 of 26
206.
Baird, A.B.; Braun, J.K.; Engstrom, M.D.; Holbert, A.C.; Huerta, M.G.; Lim, B.K.; Mares, M.A.; Patton, J.C.; Bickham, J.W. Nuclear
and mtDNA phylogenetic analyses clarify the evolutionary history of two species of native Hawaiian bats and the taxonomy of
Lasiurini (Mammalia: Chiroptera). PLoS ONE 2017,12, e0186085. [CrossRef]
207.
Lorenzini, R.; Fanelli, R.; Grifoni, G.; Scholl, F.; Fico, R. Wolf-dog crossbreeding: “Smelling” a hybrid may not be easy. Mamm.
Biol. 2014,79, 149–156. [CrossRef]
208.
Thompson, C.W.; Pfau, R.; Choate, J.R.; Genoways, H.H.; Finck, E.J. Identification and characterization of the contact zone
between short-tailed shrews (Blarina) in Iowa and Missouri. Can. J. Zool. 2011,89, 278–288. [CrossRef]
209.
Andriollo, T.; Ashrafi, S.; Arlettaz, R.; Ruedi, M. Porous barriers? Assessment of gene flow within and among sympatric
long-eared bat species. Ecol. Evol. 2018,8, 12841–12854. [CrossRef]
210.
Arbogast, B.S.; Schumacher, K.I.; Kerhoulas, N.J.; Bidlack, A.L.; Cook, J.A.; Kenagy, G. Genetic data reveal a cryptic species of
New World flying squirrel: Glaucomys oregonensis.J. Mammal. 2017,98, 1027–1041. [CrossRef]
211.
Yannic, G.; Statham, M.J.; Denoyelle, L.; Szor, G.; Qulaut, G.Q.; Sacks, B.N.; Lecomte, N. Investigating the ancestry of putative
hybrids: Are Arctic fox and red fox hybridizing? Polar Biol. 2017,40, 2055–2062. [CrossRef]
212.
Mengoni, C.; Mucci, N.; Randi, E. Genetic diversity and no evidences of recent hybridization in the endemic Italian hare (Lepus
corsicanus). Conserv. Genet. 2015,16, 477–489. [CrossRef]
213.
Prevosti, F.J.; Ramírez, M.A.; Schiaffini, M.; Martin, F.; Udrizar Sauthier, D.E.; Carrera, M.; Sillero-Zubiri, C.; Pardiñas, U.F.
Extinctions in near time: New radiocarbon dates point to a very recent disappearance of the South American fox Dusicyon avus
(Carnivora: Canidae). Biol. J. Linn. Soc. 2015,116, 704–720. [CrossRef]
214.
Bell, K.C.; Van Gunst, J.; Teglas, M.B.; Hsueh, J.; Matocq, M.D. Lost in a sagebrush sea: Comparative genetic assessment of an
isolated montane population of Tamias amoenus.J. Mammal. 2021,102, 173–187. [CrossRef]
215.
Zeng, L.; Liu, H.-Q.; Tu, X.-L.; Ji, C.-M.; Gou, X.; Esmailizadeh, A.; Wang, S.; Wang, M.-S.; Wang, M.-C.; Li, X.-L. Genomes reveal
selective sweeps in kiang and donkey for high-altitude adaptation. Zool. Res. 2021,42, 450. [CrossRef]
216.
Fabbri, E.; Velli, E.; D’Amico, F.; Galaverni, M.; Mastrogiuseppe, L.; Mattucci, F.; Caniglia, R. From predation to management:
Monitoring wolf distribution and understanding depredation patterns from attacks on livestock. Hystrix Ital. J. Mammal.
2018
,29,
101–110.
217.
Inoue, T.; Murakami, T.; Abramov, A.V.; Masuda, R. Mitochondrial DNA control region variations in the sable Martes zibellina of
Hokkaido Island and the Eurasian continent, compared with the Japanese marten M. melampus.Mammal Study
2010
,35, 145–155.
[CrossRef]
218.
Thomsen, C.L.; Andersen, L.W.; Stronen, A.V. Forensic DNA analyses suggest illegal trade of canid skins. Mammal Res.
2016
,61,
423–426. [CrossRef]
219.
Eckert, I.; Suchentrunk, F.; Markov, G.; Hartl, G.B. Genetic diversity and integrity of German wildcat (Felis silvestris) populations
as revealed by microsatellites, allozymes, and mitochondrial DNA sequences. Mamm. Biol. 2010,75, 160–174. [CrossRef]
220.
Leite, J.V.; Álvares, F.; Velo-Antón, G.; Brito, J.C.; Godinho, R. Differentiation of North African foxes and population genetic
dynamics in the desert—Insights into the evolutionary history of two sister taxa, Vulpes rueppellii and Vulpes vulpes.Org. Divers.
Evol. 2015,15, 731–745. [CrossRef]
221.
Sierra, A.B.A.; Castillo, E.R.; Labaroni, C.; Barrandeguy, M.E.; Martí, D.A.; Ojeda, R.; Lanzone, C. Genetic studies in the recently
divergent Eligmodontia puerulus and E. moreni (Rodentia, Cricetidae, Sigmodontinae) from Puna and Monte deserts of South
America. Mamm. Biol. 2017,87, 93–100. [CrossRef]
222.
Lawson, L.P.; Castruita, J.A.S.; Haile, J.S.; Vernesi, C.; Rovero, F.; Lorenzen, E.D. Unraveling elephant-shrews: Phylogenetic
relationships and unexpected introgression among giant sengis. Mol. Phylogenet. Evol. 2021,154, 107001. [CrossRef] [PubMed]
223.
Morales, A.E.; Fenton, M.B.; Carstens, B.C.; Simmons, N.B. Comment on “Population genetics reveal Myotis keenii (Keen’s myotis)
and Myotis evotis (long-eared myotis) to be a single species”. Can. J. Zool. 2021,99, 415–422. [CrossRef]
224.
Nagata, J.; Yasuda, M.; Yamashiro, A. Genetic analysis of a newly established deer population expanding in the Sasebo area
in Nagasaki Prefecture, Japan reveals no evidence of genetic disturbance by Formosan sika deer. Mamm. Study
2021
,46, 1–13.
[CrossRef]
225.
Sarver, B.A.; Herrera, N.D.; Sneddon, D.; Hunter, S.S.; Settles, M.L.; Kronenberg, Z.; Demboski, J.R.; Good, J.M.; Sullivan, J.
Diversification, introgression, and rampant cytonuclear discordance in rocky mountains chipmunks (sciuridae: Tamias). Syst. Biol.
2021,70, 908–921. [CrossRef]
226.
Korablev, M.P.; Korablev, N.P.; Korablev, P.N. Genetic diversity and population structure of the grey wolf (Canis lupus Linnaeus,
1758) and evidence of wolf×dog hybridisation in the centre of European Russia. Mamm. Biol. 2021,101, 91–104. [CrossRef]
227.
van Wyk, A.M.; Dalton, D.L.; Hoban, S.; Bruford, M.W.; Russo, I.R.M.; Birss, C.; Grobler, P.; van Vuuren, B.J.; Kotzé, A. Quantitative
evaluation of hybridization and the impact on biodiversity conservation. Ecol. Evol. 2017,7, 320–330. [CrossRef]
228.
Furman, A.; Coraman, E.; Çelik, Y.E.; Postawa, T.; Bachanek, J.; Ruedi, M. Cytonuclear discordance and the species status of
Myotis myotis and Myotis blythii (Chiroptera). Zool. Scr. 2014,43, 549–561. [CrossRef]
229.
Furman, A.; Çelik, Y.E.; Çoraman, E.; Bilgin, R. Reproductive isolation and morphological discrimination of Myotis myotis
macrocephalicus and M. blythii sl (Chiroptera: Vespertilionidae) in Turkey. Acta Chiropterol. 2020,22, 21–28. [CrossRef]
230.
Burgarella, C.; Barnaud, A.; Kane, N.A.; Jankowski, F.; Scarcelli, N.; Billot, C.; Vigouroux, Y.; Berthouly-Salazar, C. Adaptive
introgression: An untapped evolutionary mechanism for crop adaptation. Front. Plant Sci. 2019,10, 4. [CrossRef] [PubMed]
Genes 2022,13, 50 26 of 26
231. Beaumont, M.A.; Balding, D.J. Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 2004,
13, 969–980. [CrossRef]
232.
Excoffier, L.; Hofer, T.; Foll, M. Detecting loci under selection in a hierarchically structured population. Heredity
2009
,103, 285–298.
[CrossRef]
233.
Browett, S.S.; O’Meara, D.B.; McDevitt, A.D. Genetic tools in the management of invasive mammals: Recent trends and future
perspectives. Mamm. Rev. 2020,50, 200–210. [CrossRef]
234.
Mattucci, F.; Galaverni, M.; Lyons, L.A.; Alves, P.C.; Randi, E.; Velli, E.; Pagani, L.; Caniglia, R. Genomic approaches to identify
hybrids and estimate admixture times in European wildcat populations. Sci. Rep. 2019,9, 1–15.
