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J. Anim. Breed. Genet.

ISSN 0931-2668

ORIGINAL ARTICLE

Mitochondrial DNA variation of indigenous goats in Narok and


Isiolo counties of Kenya
F.M. Kibegwa1, K.E. Githui2, J.O. Junga1, M.S. Badamana1 & M.N. Nyamu2
1 Department of Animal Production, University of Nairobi, Nairobi, Kenya
2 Molecular Genetics Laboratory, National Museums of Kenya, Nairobi, Kenya

Summary

Keywords
Goat; genetic variability; Kenya; mitochondrial
control region.
Correspondence
F.M. Kibegwa, Department of Animal
Production, University of Nairobi, PO
Box 29053, Nairobi 00625, Kenya.
Tel: +254723382047;
Fax: 020-2501258;
E-mail: mkibegwa@gmail.com
Received: 22 September 2014;
accepted: 1 February 2015

Phylogenetic relationships among and genetic variability within 60 goats


from two different indigenous breeds in Narok and Isiolo counties in
Kenya and 22 published goat samples were analysed using mitochondrial
control region sequences. The results showed that there were 54 polymorphic sites in a 481-bp sequence and 29 haplotypes were determined. The
mean haplotype diversity and nucleotide diversity were 0.981  0.006
and 0.019  0.001, respectively. The phylogenetic analysis in combination with goat haplogroup reference sequences from GenBank showed
that all goat sequences were clustered into two haplogroups (A and G), of
which haplogroup A was the commonest in the two populations. A very
high percentage (99.90%) of the genetic variation was distributed within
the regions, and a smaller percentage (0.10%) distributed among regions
as revealed by the analysis of molecular variance (AMOVA). This AMOVA
results showed that the divergence between regions was not statistically
significant. We concluded that the high levels of intrapopulation diversity
in Isiolo and Narok goats and the weak phylogeographic structuring suggested that there existed strong gene flow among goat populations probably caused by extensive transportation of goats in history.

Introduction
Goats (Capra hircus) form an integral component of
the livestock sector in Kenya, and the goat population
size of 27 million spreads throughout all the agroecological zones (KNBS 2010). The majority of these
goats are found in the arid and semi-arid uncultivatable zones that comprise over 80% of Kenyas land
(Wekesa et al. 2006).
Indigenous goats (C. hircus), when compared with
their exotic counterparts, are better adapted to survive
and reproduce under the regions harsh environmental conditions (Jimmy et al. 2010). These indigenous
goats also often possess valuable traits such as disease
tolerance/resistance, high fertility, good maternal
qualities and longevity, all of which are qualities that
form the basis for low-input, sustainable agriculture
(Bruford & Wayne 1993). In addition, they play an
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important role in African culture as they are used for


gifts, dowry and cultural rituals (Okomo-Adhiambo
2002). Some of their products like milk and bile are
also medicinal (Bruford & Wayne 1993).
There is a general concern that the genetic diversity
within Africas goats is disappearing through breed
substitution, indiscriminate cross-breeding and the
absence of breed development programmes (Wollny
2003).
Genetic erosion reduces the adaptive potential of
any species, and this narrows the scope to respond to
changes in the environment, disease challenges or
market demand. The gradual disappearance of indigenous breeds that can survive in extreme environments undermines food and livelihood security of the
poor and the capacity of people to survive in marginal
areas. For this reason, immediate steps must be taken
to conserve these goats (Bruford & Wayne 1993).
doi:10.1111/jbg.12182

F. M. Kibegwa et al.

Mitochondrial DNA variation

An important strategy for the conservation and


utilization of animal genetic resources is the dissemination of information on these resources. However,
the indigenous goat breeds are not well characterized
or have been scantily defined with very limited information available regarding the number of breeds, size
of population of each breed and amount of genetic
variation present in the breeds (Okomo-Adhiambo
2002). The available information regarding the
indigenous goat breeds in mostly based on the phenotypic characteristics making it to a large extent subjective as it can be affected by the environment
consequently making implementation of rational and
effective conservation and utilization strategies difficult. Thus, genetic characterization of these goat
breeds based on DNA techniques is necessary as it is
more reliable because it is based on precise genotypic
information.
This study is therefore carried out to analyse mitochondrial DNA variation and establish the possible
maternal lineages of indigenous goat breeds in Narok
and Isiolo counties of Kenya.

Materials and methods


Sample collection and DNA extraction

A total of 60 blood samples were obtained from the


two sampling sites: Narok (30) and Isiolo (30)
(Figure 1). A modified 2-stage random sampling procedure was used. In the first step, five villages were
selected randomly from a sampling frame of all the
villages in each of the two counties and this was followed by the selection of homesteads and animals in
the second step. Fifteen homesteads in total, three
from each village were selected randomly from each
sampling site. From each homestead two goats, a male
and a female were randomly chosen, manually
restrained and bled through jugular venipuncture to
obtain blood that was collected in 9-ml vacutainers
tubes with anticoagulant (EDTA). The blood was then
stored in a cool box containing ice bricks and transported to the laboratory for analysis. Total genomic
DNA was then extracted from blood by standard phenolchloroform extraction method. An endeavour
was made to collect samples from unrelated individuals based on the information provided by the owners
and local farmers.
PCR amplification and sequencing

All the 60 DNA samples were used for amplification


and mitochondrial control region sequencing. The
2

primers were designed as follows: Forward Primer


50 - ACATGAATTGGAGGACAGCCAGTC -30 and
reverse Primer 50 - CTGTAATGCCCATGCCTACC -30 .
PCR amplifications were conducted in a 25 ll volume with 10 lM of each primer, 2.5 mM of each
dNTP, 0.5 unit Taq DNA polymerase enzyme
(TaKaRa Ex Taq Polymerase, Mountain View, California, USA), 2.5 ll of 10X PCR buffer, 50 ng DNA
template and ddH2O. The PCR amplifications were
conducted in a GenaAmp PCR System 4200 thermocycler, Applied Biosystems, Foster City, California, USA. After a 7-min period at 94C for
polymerase activation, 35 cycles were run with the
following steps 94C, 30 s, 52C, 45 s, 72C, 30 s.
A final extension of 72C, 3 min was also included.
PCR target fragments were recovered in low-melting agarose gel, and purification and sequencing
were carried out by the Beckman Coulter Genomics
Company in France. The samples were sequenced
in a reverse direction. All sequences were deposited
in the GenBank with Accession Numbers:
KP120622KP120651 (Narok) and KP120652
KP120681 (Isiolo).
Data analysis

All the 60 mtDNA control region sequences belonging


to goats from Narok and Isiolo counties in Kenya were
used in this analysis. We included already published
mtDNA control region sequences from GenBank of
domestic goats from 11 African countries Table 1.
Sequences were aligned by the ClustalW method, a
component of the program MEGA 6.0 (Tamura et al.
2013) and saved as a MEGA alignment file. To facilitate the recognition of haplogroup status of each individual, 22 goat mtDNA control region reference
sequences belonging to the six known haplogroups/
lineages that were recommended by Naderi et al.
(2007) were also downloaded from GenBank and
included in our analysis. These sequences were GenBank Accession numbers: AB044303, AJ317833,
AJ317838, AY155708, AY155721, AY155952,
DQ121578, DQ188892, DQ188893, DQ241349,
DQ241351,
EF617701,
EF617706,
EF617727,
EF617779,
EF617945,
EF617965,
EF618084,
EF618134, EF618200, EF618413 and EF618535. For
further analyses, only the region used by Luikart et al.
(2001), which formed part of the sequence available
for most of the GenBank records, was used. This
region is 481-bp long and corresponded to the positions 15 709 to 16 190 (Accession Number
GU295658.1) on the C. hircus mitochondrial reference
sequence (Accession number GU295658.1).
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F. M. Kibegwa et al.

Mitochondrial DNA variation

Figure 1 Geographical location of the sampling sites.

The haplotype diversity (h) and its standard error


(SE) and nucleotide diversity (p) and its standard
error (SE) for each goat breed/population were also
estimated using DNASP programme, version 5.10.01
(Librado & Rozas 2009). The phylogenetic trees were
constructed using the neighbour-joining method (NJ)
in the program MEGA 6.0 with a Kimura 2-parameters
model and a bootstrap (number of replications =
1000) test (Saitou & Nei 1987). Median-joining
network (Bandelt et al. 1999) and mismatch analysis
were carried out using NETWORK 4.1 (http://www.
fluxus-engineering.com/sharenet.htm), in which
transitions, transversions and insertions/deletions
were equally weighted. To examine whether there
were genetic differences within breeds, among regions
and among breeds within regions, the goats were
grouped according to their geographical distribution
and an analyses of molecular variance AMOVA was
performed using ARLEQUIN v3. 5 (Excoffier & Lischer
2010). Tajimas D (Tajima 1989) and Fus Fs
(Fu 1997) tests were also conducted to determine
whether patterns of mitochondrial sequence variation
were consistent with predictions of the neutral model
(Santos et al. 2010) and to infer the demographic
history of these two goat breeds.

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Results
mtDNA control region variation and haplotype
analysis in African goats

There were 110 polymorphic sites found in the 216


mtDNA control region sequences used in this study.
No deletion/insertion of base pairs was detected, and
among these polymorphic sites, 33 were singleton
polymorphic sites and 77 parsimony informative polymorphic sites. There was a high bias towards transition in the assessed goats as the overall ratio of
transitions versus transversions was 17.2:1. The haplotype diversity was very high in the studied goats
with a value above 0.97 in nine of the 12 studied
countries. The nucleotide diversity values ranged
from 0.00334  0.00085 in Mozambique to
1.000  0.000 in Libya and Zimbabwe (Table 1).
However, it is important to point out that the nucleotide diversity values for Libya and Zimbabwe obtained
in this study were from one sample in each of the two
countries, and this may change if more samples are
used.
All 216 goat mtDNA sequences were grouped into
159 haplotypes. The largest haplotype group consisted
of nine individuals, followed by one haplotype group

F. M. Kibegwa et al.

Mitochondrial DNA variation

Table 1 Geographic origin and characteristics of African goat breeds/populations

Breed/population

No. of
individuals

Number of
breeds

Number of
haplotypes

Haplotype diversity
(h) (SD)

Nucleotide diversity
(p) (SD)

3
29

1
3

3
25

1.000  0.272
0.990  012

0.01528  0.00477
0.02067  0.00270

1
6

1
1

1
5

1.000  0.000
0.933  0.122

1.000  0.000
0.01635  0.00278

69

65

0.998  0.003

0.01556  0.00356

Senegal
Tunisia
Mozambique

3
6
8

1
1
1

3
6
5

1.000  0.272
1.000  0.096
0.857  0.108

0.02079  0.00573
0.02384  0.00319
0.00334  0.00085

Namibia
South Africa

4
26

2
4

4
17

1.000  0.177
0.948  0.028

0.03924  0.01143
0.02990  0.00376

1.000  0.000

1.000  0.000

60
216

2
23

36
159

0.973  0.007
0.9953  0.0013

0.02702  0.00711
0.02573  0.00391

Algeria
Egypt

Libya
Morocco
Nigeria

Zimbabwe
Kenya
Total

consisting of five individuals, five haplotype groups


included four individuals, two haplotype groups had
three individuals, 26 haplotype groups were composed of two individuals, and 124 haplotypes represented by a single sequence.
When only 60 samples from Narok and Isiolo
counties were considered, a total of 54 polymorphic
sites and 29 different haplotypes were detected.
Haplotype diversity values were 0.959  0.015 in
the Narok County and 0.954  0.019 in Isiolo. The
Isiolo goat population displayed a nucleotide diversity value of 0.02692  0.019 compared to the
value shown by goats in Narok population of
0.02709  0.0001.
Phylogenetic relationship

Neighbour-joining tree constructed with all the 216


individual mitochondrial DNA sequences in this study
indicated that African goat populations were classified
into three distinct lineages A, B and G, with 146, 5
and 8 haplotypes corresponding to 185, 11 and 20
individuals, respectively (Figure 2a). On a separate
analysis of the sequences of goats from Narok and Isiolo Counties and 22 reference sequences from Naderi
et al. (2007), the 60 individuals of this study clearly

Accession numbers
AJ317777-79 (Luikart et al. 2001)
AJ317780-83; AJ317795-801
(Luikart et al. 2001); EF617711-28;
EF618220 (Naderi et al. 2007)
EF61822 (Naderi et al. 2007)
AJ317784-88 (Luikart et al. 2001);
EF618233 (Naderi et al. 2007)
AJ317810-811; AJ317823-25
(Luikart et al. 2001); EF618246-52
(Naderi et al. 2007); KJ466206-62
(Awotunde et al. 2015)
AJ317816-18 (Luikart et al. 2001)
AJ317789-794 (Luikart et al. 2001)
AJ317804-809 (Luikart et al. 2001);
EF618240-1 (Naderi et al. 2007)
EF618242-5 (Naderi et al. 2007)
AJ317812-15; AJ317819-20; AJ317844;
AJ317821-22 (Luikart et al. 2001);
EF618351-56 (Naderi et al. 2007);
KJ466263-73 (Awotunde et al. 2015)
AJ317802-803 (Luikart et al. 2001);
EF618545-6 (Naderi et al. 2007)
KP120622KP120681

showed that this goats were divided into two distinct


mtDNA Lineages A and G (Figure 2b). Lineage A had
a total of 42 individuals with Narok and Isiolo contributing 20 and 22 individuals, respectively, while G
had 18 individuals, 10 from Narok and eight from
Isiolo counties.
Population structure

An overall AMOVA estimated that 14.16% (p = 0.0020)


of the variation was among countries, and
81.16% (p < 0.0001) of the variation was within
breeds. In contrast, no significant differentiation
among breeds within countries was found, 4.68%
(p = 0.0753). The AMOVA of goats from Narok and
Isiolo counties on the other hand showed that the
variation among the two regions was not statistically
significant (Table 2). The lack of variation among
regions was further supported by the topology of the
median-joining network constructed using 29 haplotypes from Isiolo and Narok goat sequences
(Figure 3). These results showed that breeds from
these two different geographic regions did not cluster
together and separate from other region. Some haplotypes were also shared by individuals from different
geographical regions.
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Mitochondrial DNA variation

(a)

(b)

Figure 2 (a) Phylogenetic tree of 216 African Goat mtDNA control region sequences and 22 goat reference sequences. The phylogenetic positions of
the 22 reference sequences, which were defined by Naderi et al. (2007), were marked by black dots in the neighbour-joining tree. (b) Neighbour-joining tree constructed with 60 individual mtDNA control region sequences of goats from Narok and Isiolo Counties and 22 reference sequences defined
by Naderi et al. (2007). The phylogenetic positions of the 22 reference sequences were marked by black dots, Isiolo by black triangles and Narok by
white triangles.

Population demographic history

Mismatch distributions and Fus Fs statistic which


are the two main methods used to assess population
expansion events were used in this study. The mismatch distributions (pairwise comparisons) of
mtDNA have been widely used to explore such
demographic events (Rogers & Harpending 1992).
The Fus Fs statistic, which is based on the probability of having a number of alleles greater or equal to
the observed number in a sample drawn from a stationary population (Fu 1997), is considered to be
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more sensitive in detecting population expansion


(Liao et al. 2010). The mismatch distributions (Figure 4) generally showed a characteristic multimodal
distribution for all the data sets. This was similar to
the peaks identified previously by Chen et al.
(2005). Thus, it is not surprising that the Tajimas D
values = and the Fus F values were statistically
non-significant (Table 3). The Tajimas D and Fus
Fs neutrality test estimates from the current study
were comparable with estimates from other goat
populations (Chen et al. 2005) and were consistent
with a demographic population expansion, such as
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AMOVA

countries

AMOVA

Isiolo and Narok

Source of
variation

Among countries

Among breeds
within countries

Within breeds

Among
populations

Within
populations

d.f.
% of variation
p Value

11
14.16
0.0020

11
4.68
0.0753

193
81.16
<0.0001

1
0.10
0.3353

58
99.90

would be expected for populations expanding after


the domestication of relatively few founder individuals (Luikart et al. 2001).

Discussion
mtDNA control region diversity

Haplotype diversity and nucleotide diversity of


mtDNA are two important indices for assessing population polymorphism and genetic differentiation
(Pereira et al. 2005).
The overall haplotype diversity and nucleotide diversity indices of 0.9923  0.002 and 0.02510  0.00145,
respectively, served to show that extreme diversity
existed in all goat populations in our study. The new
sequences in our study from Isiolo and Narok counties
also proved to be extremely diverse. This finding was
consistent with other genetic diversity studies on
domestic goat breeds in other studies in Africa
(Gorkhali et al. 2014; Awotunde et al. 2015). Several
theories have been put forward to explain the
observed high genetic diversity among these goat populations. Naderi et al. (2007) suggested that this may
be due to multiple maternal lineages in goats, possibly
arising through independent domestications or originating via introgression from wild species. Agha et al.
(2008) on the other hand speculated that overlapping
generations, mixing of populations from different geographical locations or subdivision accompanied by
genetic drift may have caused this diversity. However,
some countries indicated poor genetic diversity which
might have been caused by the limited number of
samples per breed.
Origins of African domestic goats

To date, many studies addressing different aspects of


phylogenetic relationships of economically important
livestock species, including the goat (C. hircus), have
been conducted (MacHugh & Bradley 2001). Many of
these studies have been geared towards addressing
the origin of modern domestic livestock, and evidence
of intense maternal diversity has been seen in many
6

Table 2 The hierarchical components of


mtDNA control region variation computed
under AMOVA framework

domesticated animals (Guo et al. 2005). The phylogenetic analysis of the 60 goat mtDNA control region
sequences from Isiolo and Narok counties showed
clustering into haplogroups that was in agreement
with previous studies on goat maternal haplogroups
(Luikart et al. 2001; Chen et al. 2005; Naderi et al.
2007).
The frequency distribution of the haplogroups in all
the published African goats and goats in this study
was consistent with the reported patterns in other
studies (Joshi et al. 2004; Awotunde et al. 2015), in
which haplogroups A is the major component (91%
of the goat haplotypes at the worldwide scale Naderi
et al. 2007). The different mtDNA haplogroups found
in goat breeds in our study further support the previous view of multiple maternal origins of domestic
goats (Chen et al. 2005). Nonetheless, it should be
noted that might have had a more complex history of
domestication than indicated by a previous study by
Joshi et al. (2004).
Phylogeographic structure of mtDNA control region

The overall hierarchical analysis of molecular variance


revealed that the bulk of the total mtDNA variation
existed within breeds (85.23%), a smaller percentage
was seen among breeds within countries (4.29%) and
among countries (10.48%). The variations among
countries and within breeds were statistically significant while the variation among breeds within countries showed no statistical significance. This finding
was consistent with what had been reported earlier by
Naderi et al. (2007) who reported 12.06% among
regions and 77.14% within breeds.
AMOVA of the 60 samples from Isiolo and Narok
counties showed that divergence between regions was
not statistically significant. Almost 99.90% of the
genetic variation was observed within population
variance component while only 0.10% of the genetic
variation was included among the goat populations in
the two geographic regions. This observation was
further supported by a median-joining network in
which the haplotype distribution pattern did not
cluster according to populations. This result was
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Figure 3 Median-joining network for the 29 mtDNA haplotypes of Isiolo and Narok goats represented by white and black circles, respectively. The
area of circle is proportional to haplotype frequency.

similar to what had been reported in other previous


studies (Joshi et al. 2004; Naderi et al. 2007; Awotunde et al. 2015).
Two possible hypotheses can be used to explain our
result. First, mtDNA variation seems to be a poor assay
for analysing population genetic structure at the breed
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level (Bradley et al. 1996). When the latter authors


conducted a mitochondrial diversity study of African
and European cattle, excluding Indian breeds, they
found that the variation within-continent and
between-breed could account for only <4% of variance, despite the presence of very distinct Zebu and
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Mitochondrial DNA variation

(a)

(b)

Figure 4 Mismatch distribution graphs for goat populations of Kenya.


(a) Mismatch distributions for goat mtDNA from Isiolo and Narok Counties, (b) mismatch distributions for goat mtDNA from haplogroup A and
(c) mismatch distributions for goat mtDNA from haplogroup G.

Taurine breeds in the African sample. However, this


case was not true for Chinese domestic goat breeds
because Joshi et al. (2004) found significant genetic
structure among Indian goat breeds using the mitochondrial first hypervariable region sequences. Second, there existed strong gene flow among goat
populations in history. As our samples included only
breeds collected from far-flung geographic locations
as Luikart et al. (2001), it was unreasonable that no
significant geographical structuring in these goat
breeds was due to the very recent transport of goats
among different regions. Therefore, it would be
expected that transport of goats occurred commonly
in history and was likely linked to human history
(Joshi et al. 2004).
Thus, more information on human history is important as it can provide indirect clues for goat evolutionary history. As this goat populations are
predominantly owned by nomadic pastoralists, there
is a very high likelihood that these two groups
encountered each other while looking for pasture and
water for their animals. Additionally, it is justifiable
that people would prefer to carry goats during their
migratory movements because goats are portable food
resources, and they have the ability to survive in the
most adverse circumstances while supplying a full
range of useful products (Porter 1996). Thus, the commercial trade and extensive transport of goats would
account for the observed pattern by having favoured
genetic exchange (Liu et al. 2009).

(c)

Conclusions
In conclusion, we analysed the mtDNA control region
fragments from Narok and Isiolo indigenous goat populations and sequences from African countries to
assess the goat phylogeny as well as to discern the
genetic diversity of the goat breeds/populations
within Kenya and at the continental level. We
observed high mtDNA diversity at a continental level
and within indigenous domestic goat breeds in Isiolo
and Narok Counties of Kenya which was in general
agreement with the pattern described in previous
studies (Chen et al. 2005; Naderi et al. 2007). We
speculated that gene flow among goat populations
facilitated by the traditional seasonal pastoralism and
annual long-distance migrations in history as well as

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Table 3 Results of Tajimas D and Fus Fs neutrality tests including associated p-values
Regions

Tajimas D (p)

Fus Fs (p)

Haplogroup A
Haplogroup G
Overall

0.724 (0.266)
0.453 (0.360)
0.406 (0.762)

5.217 (0.051)
0.061 (0.497)
2.708 (0.244)

trade would account for the pattern discerned in


regional goat pools. It is therefore prudent to take
measures that promote a sustainable management of
these genetic resources (Taberlet et al. 2011).
Recommendations
More such studies should be carried out to include
goats from regions of Kenya that were not sampled in
this study. This will give a better understanding of the
local goat populations and their uniqueness. This
information will further help in making decisions on
the conservation and rational utilization of the Kenyan local goat breeds.
Second, the goat domestication history still remains
an unsolved puzzle increasing the number of independent studies like the present one are required to
sample more goats within this locations and other
areas including wild goat species for uncovering the
true history of domestication in goats.
We should also recognize the limitation of mtDNA
when used for phylogenetic analysis that only information from maternal lineage was analysed. To make
up the gap, paternally derived Y chromosome can be
used in future studies. Surveys of variation in the nonrecombining portion of this chromosome have been
immensely valuable in complementing and adding to
the picture of mammalian evolution (Knijff 2000).
Autosomes should not be neglected, although they
are more likely influenced by evolutionary forces.
Studies of microsatellites and SNPs have shown that
highly polymorphic diploid markers can also shed
light on recent population dynamics and reveal
the fine grain of admixture between divergent
populations.
Finally, there is need to assess the levels of inbreeding within this indigenous goat breeds if we are going
to utilize them rationally.
Acknowledgements
This research was supported by a grant from the
National Commission on Science and Technology of
Kenya.

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