Title: Reconstruction of phylogenetic history to resolve the subspecies anomaly of
Pantherine cats
Authors: Ranajit Das
1
, Priyanka Upadhyai
2
1
Manipal Centre for Natural Sciences, Manipal University, Manipal, Karnataka 576104,
India
2
Department of Medical Genetics, Kasturba Medical College, Manipal University,
Manipal, Karnataka 576104, India
Email address:
ranajit.das@manipal.edu
Running title: Mitogenome phylogeny of Pantherine cats
Abstract
All charismatic big cats including tiger (Panthera tigris), lion (Panthera leo), leopard
( Panthera pardus), snow leopard ( Panthera uncial), and jaguar ( Panthera onca) are
grouped into the subfamily Pantherinae. Several mitogenomic approaches have been
employed to reconstruct the phylogenetic history of the Pantherine cats but the phylogeny
has remained largely unresolved till date. One of the major reasons for the difficulty in
resolving the phylogenetic tree of Pantherine cats is the small sample size. While
previous studies included only 5-10 samples, we have used 43 publically available taxa to
reconstruct Pantherine phylogenetic history. Complete mtDNA sequences were used
from all individuals excluding the control region (15,489bp). A Bayesian MCMC
approach was employed to investigate the divergence times among different Pantherine
clades. Both maximum likelihood and Bayesian phylogeny generated a dendrogram:
Neofelis nebulosa ( Panthera tigris ( Panthera onca ( Panthera uncia ( Panthera leo,
Panthera pardus)))), grouping lions with leopards and placing snow leopards as an
outgroup to this clade. The phylogeny revealed that lions split from their sister species
leopard ~3 Mya and the divergence time between snow leopards and the clade including
lions and leopards was estimated to be ~5 Mya. Our study revealed that the morphology-
based subspecies designation for both lions and tigers is largely not valid. The estimated
tMRCA of 2.9 Mya between Barbary lions and Sub-Saharan African lions depicts the
restriction of female-mediated gene flow between the lion populations in the backdrop of
the habitat fragmentation taking place from late Pliocene to early to mid-Pleistocene
creating islands of forest refugia in central Africa.
Key words: Panthera, Bayesian MCMC, mitogenome, subspecies anomaly
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Introduction
The charismatic big cats: tiger (Panthera tigris), lion (Panthera leo), leopard (Panthera
pardus), snow leopard ( Panthera uncial), and jaguar ( Panthera onca) are grouped into
the subfamily Pantherinae (Bagatharia, et al., 2013). All of these big cats are endangered
and are found in small fragmented populations in the world. Tigers are given an
endangered status by IUCN (IUCN, 2015). They are currently found in Siberian taiga and
grasslands (Siberian tiger,
P. t. altaica)
, small pockets in Southeast Asia (Indochinese
tiger,
P. t. corbetti
, and Malayan tiger,
P. t. jacksoni),
Southern China (South China tiger,
P. t. amoyensis
), island of Sumatra (Sumatran tiger,
P. t. sumatrae)
, and the mangrove
swamps of Indian subcontinent (Bengal tiger,
P. t. tigris) (Luo, et al., 2004)
. Lions are
given a vulnerable conservation status (IUCN, 2015). They are found in two widely
isolated geographical areas: various parts of Africa (African lion), and the Gir forest of
Southwestern Gujarat, India (Asiatic lion) (Hemmer, 1966). While all Asiatic lion belong
to the same subspecies (P. l. persica), the African lions are grouped into five separate
subspecies: Barbary lion (Northern Africa, P. l. leo), Senegal lion (West-central Africa,
P. l. senegalensis), Masai lion (East African lion, P. l. nubica), Katanga lion (Southwest
Africa,
P. l. bleyenberghi), and Transvaal lion (Southeast Africa, P. l. krugeri) (Hemmer,
1966)
. Leopards are designated as near threatened by IUCN (IUCN, 2015). These
charismatic cats have a wide range of distribution from in sub-Saharan Africa to
Southeast Asia and Siberia. There are currently nine recognized subspecies of leopard:
African leopard (P. p. pardus), Arabian leopard (P. p. nimr), Persian leopard (P. p.
saxicolor), Indian leopard ( P. p. fusca), Sri Lankan leopard ( P. p. kotiya), Indochinese
leopard (P. p. delacouri), North-Chinese leopard (P. p. japonensis), Siberian leopard (P.
p. orientalis), and Javan leopard ( P. p. melas) (Uphyrkina , et al., 2001). Snow leopards
are listed as endangered in IUCN Red List of Threatened Species (IUCN, 2015). They are
native to mountains of Central and South Asia. Jaguars are nearly endangered according
to IUCN Red List (IUCN, 2015) and they are native to southern North America, Central
and South America. There are three recognized subspecies of jaguar: Amazon jaguar (P.
o. onca), Mexican jaguar (P. o. hernandesii), and Brazilian jaguar (P. o. palustris)
(Seymour, 1989).
Reconstruction of the phylogenetic history of these charismatic cats can provide us a
plethora of information about their species, subspecies, and population genetic status,
which can be helpful for the conservation of these threatened animals.
Several morphological, biochemical, and molecular approaches have been
employed to resolve the phylogenetic history of the Pantherine cats such as
morphological (Salles, 1992), cytogenetic (Wurster-Hill and Gray, 1975), immunological
(Collier and O'Brien, 1985), biochemical (Slattery, et al., 1994), sex-chromosome based
(Slattery and O'Brien, 1998), chemical (Bininda Emonds, Decker Flum and
Gittleman, 2001), and molecular genetic (Bagatharia, et al., 2013; Johnson, et al., 2006;
Johnson and O’brien, 1997; Wei, et al., 2011). In spite of several trials to reconstruct the
phylogenetic history of Pantherine cats, their phylogeny has remained largely unresolved.
Johnson et al. (2006) grouped snow leopards with tigers based on
18,853 bp of nuclear
DNA concatenated data
(Johnson, et al., 2006)
. In contrast, a later phylogenetic analysis
grouped snow leopards with lions based on their complete mtDNA sequences (Wei, et
al., 2011). They estimated that
N. nebulosa shared a common ancestor with other
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Pantherine cats about 8.66 Mya and that the leopards shared a common ancestor with the
lion-snow leopard clade about 4.35 Mya. Recently, another mitogenomic study grouped
lion and leopards together and placed snow leopard as the sister taxa to this clade
(Bagatharia, et al., 2013). Although Panthera phylogeny has been reconstructed multiple
times, none of these studies used multiple subspecies of Pantherine cats. So, the
subspecies anomaly remained unresolved.
All previous phylogenetic studies were performed using 5-10 Pantherine cats,
taking one individual from each species, which made it difficult to assess the
phylogenetic tree at a high resolution and determine the subspecies level genetic
diversity. In the present study we have used complete mitochondrial DNA sequences
excluding the control region (15,489bp) from 43 publicly available Pantherine taxa
including multiple individuals and subspecies of big cats to resolve the phylogenetic
history of the gennus Panthera and to genetically validate the ‘subspecies’ status of
various Pantherine taxa. This study thus offers an unparalleled and in-depth view of
Pantherine phylogeny and genetically assess the ‘subspecies’ question that has remained
elusive till date, which can aid in providing more effective conservation measures for
these charismatic big cats.
Methods
Molecular phylogenetic analysis
We retrieved 43 publicly available Pantherine mitogenomes including all available
subspecies of six charismatic cats: tiger, lion, leopard, snow leopard, jaguar, and Neofelis
from GenBank (Benson, et al., 2004) (Table 1). The mitogenome sequences were first
aligned using Clustal Omega online server (Sievers, et al., 2011). The fasta alignment of
the complete mitogenome sequences was then exported to MEGA v6.06, where the
control region (D-loop) sequences were eliminated. Pair-wise genetic distances among
the Pantherine taxa were calculated in MEGA v6.06 (Tamura, et al. 2013). A model test
was performed to determine the best fitting nucleotide substitution model for the dataset,
using Akaike’s information criteria with correction (AICc) and Bayesian information
criteria (BIC) using jModelTest v2.1.4 (Guindon and Gascuel, 2003). The alignment of
43 Pantherine taxa was used for maximum likelihood phylogenetic reconstruction, with
1000 bootstrap replicates, using MEGA v6.06. Bayesian phylogenetic tree was
reconstructed using MrBayes v3.2.5 (Huelsenbeck and Ronquist, 2001).
Dating the phylogenetic tree
!
For dating, we used a Bayesian Markov Chain Monte Carlo approach (MCMC)
implemented in BEAST v1.8.2 (Drummond , et al., 2012). The BEAST input file was
generated using BEAUTi v1.8.2 (Drummond, et al., 2012). An uncorrelated lognormal
relaxed molecular clock was used to allow the evolutionary rate to vary from branch to
branch. Previous studies have shown that has showed that relaxed molecular clock
provides better estimate of time to most recent common ancestor (tMRCA) over the strict
molecular clock that does not allow the evolutionary rate to vary among branches
(Drummond, et al., 2006). SRD06 model of nucleotide substitution was used to partition
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the nucleotide data by codon position. The rate of evolution was calibrated using
lognormally distributed priors with lognormal means of zero and lognormal standard
deviation of 0.56. Since lognormally distributed priors sample values from the more
distant past more frequently than recent values, it performs better than both normally
distributed and exponentially distributed priors, when using fossil calibration points for
dating a phylogenetic tree (Ho, 2007). We offset the lognormal distributions of the priors
at the internal node of Panthera-Neofelis split by 7 Mya, so that the median values of the
sampled distributions were equal to and the mean values were slightly greater than the
split date of ~8 Mya between the two. This calibration method has been previously
employed for reconstructing phylogenetic history of other mammalian subfamily level
taxa (Bjork, et al., 2011; Das, et al., 2014; Raaum, et al., 2005). Yule speciation process,
which has been shown to be more appropriate when analyzing sequences from different
species, was used for the divergence estimation (Stone, et al., 2010).
MCMC simulation ran for 10 million generations, sampling every 500 steps. 10%
of the trees were removed as ‘burnin’. The maximum clade credibility (MCC) tree was
identified and annotated using TreeAnnotator v1.8.2 (Drummond, et al., 2012). Nodes
with posterior probabilities exceeding 90% (P > 0.9) were used for the tree building. The
MCC tree generated by TreeAnnotator v1.8.2 was visualized and graphically represented
using FigTree v1.4.2 (
http://tree.bio.ed.ac.uk/software/figtree
). The posterior estimates of
the parameters sampled by the Markov Chain was summarized in Tracer v1.6 (Rambaut
and Drummond, 2013). tMRCA means, medians, and 95% highest posterior density
(95% HPD) intervals (all in Myr) were also calculated in Tracer v1.6.
Results
Sequence divergence and the subspecies dilemma
Among lions, identical nucleotide sequences were observed among P. l. senegalensis
(KP001502), P. l. azandica (KP001506), P. l. nubica (KP001495), and P. leo
(NC_028302), raising questions about the validity of the different subspecies status for
these individuals. The two Barbary lions (KF776494 and KF907306) are genetically most
distant from the rest of the clade, showing 2.2 - 3% divergence of the mitogenome. The
remaining lion subspecies shows 0 - 0.6% genetic divergence among each other. Our
results thus indicate that the morphological variation among the different African lion
populations may not be enough to consider them as different ‘subspecies’.
The validity of the subspecies status is also questionable in case of the tigers with
P. t. amoyensis (HM589215) and P. t. altaica (HM185182) showing identical nucleotide
sequences. The mean tiger mitogenome divergence was 0.5% and the largest divergence
was observed between the Amoy tigers (HM589214 and HM589215) and the rest of the
tree (1.2%). Thus, similar to lions, most of the tiger subspecies are also potentially not
valid genetically.
Leopard subspecies show 0 – 0.9% genetic divergence among each other with the
highest divergence between P. p. pardus (KP001507) and P. p. japonensis (EF551002)
(0.9%).
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Phylogenetic analyses
!
The maximum likelihood (ML) tree was constructed using Hasegawa-Kishino-Yano
model of nucleotide substitution with gamma distribution and invariable sites
(HKY+G+I), which was selected to be the best fitting model for the dataset by
jModelTest v2.1.4. The ML based phylogeny grouped lions (N = 16) and leopards (N =
5) together with 100% bootstrap support and placed show leopards (N = 3) as the sister
taxa to this clade (100% bootstrap support) (Figure 1). Jaguars (N = 4) were designated to
be the sister taxa of the lion-leopard-snow leopard clade (Figure 1). The deepest root
within the lions was observed between the Barbary lions (P. l. leo) and the rest of the
subspecies with 100% bootstrap support (Figure 1). For the tigers (N = 13), the deepest
root was observed between the Amoy tigers and the rest (100% bootstrap support)
(Figure 1). Similar grouping of the Patherine taxa was revealed in the Bayesian
phylogenetic tree (Figure 2). Overall, the phylogenetic analyses revealed a dendrogram:
Neofelis nebulosa (Panthera tigris (Panthera onca (Panthera uncia (Panthera leo,
Panthera pardus)))).
Estimates of divergence dates
As mentioned before (see methods) a single calibration point of Neofelis-Panthera split
of 8 Mya was used to estimate the divergence time. Similar to the ML tree, the Bayesian
tree also grouped lions and leopards together and placed snow leopard as the sister taxa to
this clade. The MCMC analysis employed in BEAST revealed that lions split from its
sister species leopard 3.45 Mya (1.75 – 5.17) (Table 2). The divergence time between
snow leopards and the clade including lions and leopards was estimated to be 4.97 Mya
(2.9 -7.24) (Table 2). Tigers appeared to split from the rest four charismatic big cats 7.47
Mya (4.97 – 9.24) (Table 2). The deepest roots within the tigers was estimated to be ~2
Mya between the Amur tiger and the remainder of the tiger clade (Table 2). As revealed
by the ML tree, the deepest split within lions was between the Barbary lions and the
remainder of the subspecies (including all Sub-Saharan African and Asian subspecies)
(2.87 Mya). The divergence between the Asian lions from the East-Central African
subspecies is relatively new 1.39 Mya (0.63 – 4.2) (Table 2).
Discussion
mtDNA based phylogeny: advantages of large sample size
For the last two decades mtDNA is being used to reconstruct Pantherine phylogeny.
However, all previous phylogenetic analyses in this regard were employed using 5 – 10
Pantherine taxa. Moreover, none of them included multiple subspecies and/or individuals
from a species. Consequently, the deepest root within the species remained largely
unknown. Also, due to low resolution, the Pantherine species were often wrongly
grouped, often generating contrasting results. For instance, Johnson et al (2006) grouped
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snow leopards with tigers and Wei et al. (2011) grouped
them with lions
(Johnson, et al.,
2006; Wei, et al., 2011)
.
We used 43 Pantherine taxa in this study, including individuals and subspecies
from all charismatic big cats. Complete mtDNA sequences excluding the control regions
(15,489bp) were used for phylogenetic analysis. The control regions were excluded in
this study on two major accounts: i) this area of the mitogenome is very difficult to align
across the big cats and ii) the repeat sequences found in this region results in different
mitogenome sizes across the Pantherine cats (Bagatharia, et al., 2013). Therefore several
recent phylogenetic studies on Pantherine cats have either included only the protein
coding genes or the complete mtDNA sequence excluding the control region (Bagatharia,
et al., 2013; Wei, et al., 2011). Proper and systematic sampling method employed here
aids to the robustness of the analyses by increasing the statistical power. Both ML and
Bayesian based phylogeny revealed the same grouping of all Pantherine taxa.
Overall, the current study revealed a dendrogram: Neofelis nebulosa (Panthera
tigris ( Panthera onca ( Panthera uncia ( Panthera leo, Panthera pardus)))). The inclusion
of multiple individuals and subspecies from all species and incorporation of jaguars has
helped to reconstruct hitherto unresolved Pantherine phylogeny with high confident.
Snow leopards are genetically distant from the tigers with 7.5 – 8.1% sequence
divergence and therefore grouping them with tigers is potentially an artifact of improper
and inadequate sampling (Johnson, et al., 2006). Lions are genetically close to both
leopards (4 – 5% sequence divergence) and snow leopards (5.5 – 6.1% sequence
divergence). So, if multiple individuals from all species are not included in the analyses,
lions can be, at random, wrongly grouped with snow leopards, and this is what has
potentially occurred in case of the phylogeny described in Wei et al. (2011)
who used
only six Pantherine taxa in their study (Wei, et al., 2011). Unlike the aforementioned
studies, the recent-most Pantherine tree described in Bagatharia et al. (2013) revealed
correct species level phylogeny by grouping lions and leopards together and placing snow
leopards as the sister species to the lion-leopard clade. But
the low sample size (six
Pantherine cats) of the study and the exclusion of jaguars in all analyses resulted in a low-
resolution phylogeny.
Subspecies anomaly
Our study raised question on ‘subspecies’ designation based on morphology. In most
cases we found that the current ‘subspecies’ designation is not genetically valid and
needs serious taxonomic change.
For instance, current lion subspecies status is largely based on morphological
characteristics mentioned in Hemmer (1966) (Hemmer, 1966). The current study raises
questions about the authenticity of the subspecies status of various Sub-Saharan African
lion subspecies based on morphology. Although currently geographically isolated, P. l.
senegalensis (KP001502), P. l. azandica (KP001506), P. l. nubica (KP001495), and P.
leo (NC_028302) share identical nucleotide sequences. In contrast, the two P. l.
senegalensis individuals (KP001497 and KP001502) show 0.3% nucleotide divergence.
Similar nucleotide divergence (0.4%) was observed between the two P. l. bleyenberghi
individuals (KP001504 and KP001505). These results indicate recent geographical
isolation of Sub-Saharan African lion populations, who potentially have not yet
accumulated subspecies level genetic divergence. For decades’ authors have debated on
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the exact number of lion subspecies (eight vs. ten). Our study conclusively revealed that
there are potentially only three ‘subspecies’ of lion currently exists in this planet: North
African Barbary Lion, Sub-Saharan African Lion, and Asiatic Lion. The genetic
variations observed among the Sub-Saharan African Lions are potentially mere individual
variations.
The validity of the subspecies status is also questionable in case of the tigers with
P. t. amoyensis (HM589215) and P. t. altaica (HM185182) showing identical nucleotide
sequences and two P. t. altaica individuals (HM185182 and JF357973) showing high
(1.1%) nucleotide divergence. The aforementioned results clearly indicate more
individual level variation (intra-population) than subspecies level variation (inter-
population), raising questions about the validity of morphology-based subspecies
designation. It can be speculated that if more samples were analyzed, individuals from
different populations would have grouped together disobeying their current ‘subspecies’
status.
Migration and isolation of Pantherine taxa
!
Tigers potentially split from other five big cats sometime in late Miocene. As speculated
in previous studies, Panthera species such as lions potentially migrated into America and
Africa from Asia in the Pliocene (Werdelin and Lewis, 2005). The migration path of the
Pantherine cats mentioned in Johnson et al. (2006) fits with the divergence times of
Pantherine cats mentioned in this study
(Johnson, et al., 2006). Snow leopards potentially
got isolated from lions and leopards in early Pliocene (~5Mya), when these cats started
migrating to Africa.
The estimated tMRCA of 2.9 Mya between Barbary lions and the
Sub-Saharan African lions is an indication of potential restriction of female-mediated
gene flow between these populations. The habitat fragmentation from late Pliocene to
early to mid-Pleistocene resulted in the islands of forest refugia in central Africa,
isolating Barbary lions from other lion populations. However, migration and intermixing
potentially continued among the Sub-Saharan African subspecies till forests were
converted into the savannas during late Pleistocene. Additionally it is interesting to note
that be noted here that the mitogenome divergence among the lion populations potentially
began at the same time as other African mammals such as chimpanzees, bonobos, and
gorillas. Overall, this study provides a holistic and in-depth view of Pantherine
phylogeny, indicating the importance of using large number of samples for confident
resolution of mammalian phylogenetic history.
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Table 1. Gen Bank IDs, common, and scientific names of the Pantherine samples used in this study
Species
Common name
Subspecies
Common name
Gen Bank IDs
1. Panthera tigris (N = 13)
Tiger
a) Panthera tigris amoyensis (N= 2)
Amoy tiger
HM589214, HM589215
b) Panthera tigris altaica (N= 4)
Siberian tiger
HM185182, JF357973, JF357974, KF297576
c) Panthera tigris tigris (N= 3)
Bengal tiger
JF357967, JF357968, NC_010642
d) Panthera tigris sumatrae (N= 1)
Sumatran tiger
JF357969
e) Panthera tigris jacksoni (N= 1)
Malayan tiger
KJ508413
f) Panthera tigris corbetti (N= 1)
Indochinese tiger
KJ508412
g) Not mentioned (N= 1)
Not mentioned
KP202268
2. Panthera leo (N = 16)
Lion
a) Panthera leo leo (N= 2)
Barbary lion
KF776494, KF907306
b) Panthera leo persica (N= 4)
Asiatic lion
JQ904290, KC834784, KP001501, NC_018053
c) Panthera leo senegalensis (N= 2)
West African lion
KP001502, KP001497
d) Panthera leo azandica (N= 1)
Congo lion
KP001506
e) Panthera leo nubica (N= 3)
Masai lion
KP001495, KP001498, KP001499
f) Panthera leo bleyenberghi (N= 2)
Southwast African lion
KP001504, KP001505
g) Panthera leo krugeri (N= 1)
Transvaal lion
KP001500
h) Not mentioned (N= 1)
Not mentioned
NC_028302
3. Panthera pardus (N = 5)
Leopard
a) Panthera pardus pardus (N= 1)
African leopard
KP001507
b) Panthera pardus japonensis (N= 2)
North-Chinese leopard
EF551002, KJ866876
h) Not mentioned (N= 2)
Not mentioned
KP202265, NC_010641
4. Panthera uncia (N = 3)
Snow leopard
NA
NA
EF551004, KP202269, NC_010638
5. Panthera onca (N = 4)
Jaguar
NA
NA
KF483864, KM236783, KP202264, NC_022842
6. Neofelis nebulosa (N = 2)
Clouded leopard
NA
NA
KP202291, NC_008450
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Table 2. tMRCA dates with confidence intervals
Taxon divergence
tMRCA mean
a
95% HPD
b
Median
Neofelis - Panthera
8.03
7.222 - 9.213
7.894
Tiger - Lion/Leopard/Snow leopard/Jaguar
7.467
4.972 - 9.236
7.655
Jaguar - Lion/Leopard/Snow leopard
6.708
3.923 - 8.850
6.94
Snow leopard - Lion/Leopard
4.968
2.9 - 7.243
4.852
Lion - Leopard
3.45
1.746 - 5.166
3.398
Deepest root within tiger
2.333
0.932 - 3.868
2.252
Asian and East-Central African lions
1.39
0.63 - 4.2
0.85
a
Time to most recent common ancestor, in Myr.
b
95% highest posterior density
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Figure 1. Consensus maximum likelihood tree (HKY+I+G model) of 43 Pantherine taxa.
Percentage of bootstrapped replicates supporting each node (out of 1,000 bootstraps) are
shown. The nodes with less than 50% bootstrap support are not shown. The Neofelis cats
were used as the outgroup to the genus Panthera. The individuals with unknown
subspecies status are marked with an asterisk.
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Figure 2. Phylogeny of 43 Pantherine taxa based on complete mtDNA sequences
excluding the control region. The dates were inferred using a Bayesian MCMC approach
implemented in BEAST with Neofelis-Panthera divergence offset by 7 Myr to
approximate a 8 Mya date for Neofelis-Panthera split. Individuals with uknown
subspecies status are indicated with an asterisk.
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