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Poissant J, Hogg JT, Davis CS, Miller JM, Maddox JF, Coltman DW.. Genetic linkage map of a wild genome: genomic structure, recombination and sexual dimorphism in bighorn sheep. BMC Genomics 11: 524

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The construction of genetic linkage maps in free-living populations is a promising tool for the study of evolution. However, such maps are rare because it is difficult to develop both wild pedigrees and corresponding sets of molecular markers that are sufficiently large. We took advantage of two long-term field studies of pedigreed individuals and genomic resources originally developed for domestic sheep (Ovis aries) to construct a linkage map for bighorn sheep, Ovis canadensis. We then assessed variability in genomic structure and recombination rates between bighorn sheep populations and sheep species. Bighorn sheep population-specific maps differed slightly in contiguity but were otherwise very similar in terms of genomic structure and recombination rates. The joint analysis of the two pedigrees resulted in a highly contiguous map composed of 247 microsatellite markers distributed along all 26 autosomes and the X chromosome. The map is estimated to cover about 84% of the bighorn sheep genome and contains 240 unique positions spanning a sex-averaged distance of 3051 cM with an average inter-marker distance of 14.3 cM. Marker synteny, order, sex-averaged interval lengths and sex-averaged total map lengths were all very similar between sheep species. However, in contrast to domestic sheep, but consistent with the usual pattern for a placental mammal, recombination rates in bighorn sheep were significantly greater in females than in males (~12% difference), resulting in an autosomal female map of 3166 cM and an autosomal male map of 2831 cM. Despite differing genome-wide patterns of heterochiasmy between the sheep species, sexual dimorphism in recombination rates was correlated between orthologous intervals. We have developed a first-generation bighorn sheep linkage map that will facilitate future studies of the genetic architecture of trait variation in this species. While domestication has been hypothesized to be responsible for the elevated mean recombination rate observed in domestic sheep, our results suggest that it is a characteristic of Ovis species. However, domestication may have played a role in altering patterns of heterochiasmy. Finally, we found that interval-specific patterns of sexual dimorphism were preserved among closely related Ovis species, possibly due to the conserved position of these intervals relative to the centromeres and telomeres. This study exemplifies how transferring genomic resources from domesticated species to close wild relative can benefit evolutionary ecologists while providing insights into the evolution of genomic structure and recombination rates of domesticated species.
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RESEARC H ARTIC LE Open Access
Genetic linkage map of a wild genome: genomic
structure, recombination and sexual dimorphism
in bighorn sheep
Jocelyn Poissant
1*
, John T Hogg
2
, Corey S Davis
1
, Joshua M Miller
1
, Jillian F Maddox
3
, David W Coltman
1
Abstract
Background: The construction of genetic linkage maps in free-living populations is a promising tool for the study
of evolution. However, such maps are rare because it is difficult to develop both wild pedigrees and corresponding
sets of molecular markers that are sufficiently large. We took advantage of two long-term field studies of pedigreed
individuals and genomic resources originally developed for domestic sheep (Ovis aries) to construct a linkage map
for bighorn sheep, Ovis canadensis. We then assessed variability in genomic structure and recombination rates
between bighorn sheep populations and sheep species.
Results: Bighorn sheep population-specific maps differed slightly in contiguity but were otherwise very similar in
terms of genomic structure and recombination rates. The joint analysis of the two pedigrees resulted in a highly
contiguous map composed of 247 microsatellite markers distributed along all 26 autosomes and the X
chromosome. The map is estimated to cover about 84% of the bighorn sheep genome and contains 240 unique
positions spanning a sex-averaged distance of 3051 cM with an average inter-marker distance of 14.3 cM. Marker
synteny, order, sex-averaged interval lengths and sex-averaged total map lengths were all very similar between
sheep species. However, in contrast to domestic sheep, but consistent with the usual pattern for a placental
mammal, recombination rates in bighorn sheep were significantly greater in females than in males (~12%
difference), resulting in an autosomal female map of 3166 cM and an autosomal male map of 2831 cM. Despite
differing genome-wide patterns of heterochiasmy between the sheep species, sexual dimorphism in recombination
rates was correlated between orthologous intervals.
Conclusions: We have developed a first-generation bighorn sheep linkage map that will facilitate future studies of
the genetic architecture of trait variation in this species. While domestication has been hypothesized to be
responsible for the elevated mean recombination rate observed in domestic sheep, our results suggest that it is a
characteristic of Ovis species. However, domestication may have played a role in altering patterns of heterochiasmy.
Finally, we found that interval-specific patterns of sexual dimorphism were preserved among closely related Ovis
species, possibly due to the conserved position of these intervals relative to the centromeres and telomeres. This
study exemplifies how transferring genomic resources from domesticated species to close wild relative can benefit
evolutionary ecologists while providing insights into the evolution of genomic structure and recombination rates
of domesticated species.
Background
The construction of genetic linkage maps in model
organisms and domesticated species enables studies of
the genetic architecture of trait variation and genome
evolution. However, such resources for free-living popu-
lations of non-model species are still rare because it is
difficult to acquire large enough pedigrees and asso-
ciated sets of molecular markers [1,2]. The utility of
genetic linkage maps developed using pedigreed wild
populations has been demonstrated by pioneering stu-
dies on the genetic architecture of trait variation [3-8],
genetic constraints [9] and patterns of linkage
* Correspondence: poissant@ualberta.ca
1
Department of Biological Sciences, University of Alberta, Edmonton, Alberta,
T6G 2E9, Canada
Full list of author information is available at the end of the article
Poissant et al.BMC Genomics 2010, 11:524
http://www.biomedcentral.com/1471-2164/11/524
© 2010 Poissant et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution L icense (http://creati vecommons.org/licenses/by/2.0), which perm its unrestricted use, di stribution, and reproduction in
any medium, provided the original work is properly cited.
disequilibrium [10,11] under semi-natural settings. Yet,
we still know very little about these specific topics and
the potential to address a variety of additional subjects
remains largely unexploited [12]. The development of
linkage maps for additional natural populations is there-
fore clearly desirable.
The bighorn sheep (Ovis canadensis), a mountain
ungulate inhabiting western North America [13], is one
species for which linkage map construction using free-
living individuals is possible. DNA samples from inten-
sively studied pedigreed populations have been collected
over many decades by field biologists (e.g. [14,15]) and a
large set of polymorphic microsatellite markers was
recently derived from domestic sheep genomic resources
[16]. A bighorn sheep linkage map would enable one to
dissect the molecular genetic basis of fitness-related
traits, study the molecular basis of inbreeding depression
and genetic rescue [14], and potentially reveal the mole-
cular genetic basis of human-influenced evolution [17].
In addition to generating species-specific research
opportunities, a bighorn sheep map would shed light on
the levels of genomic re-organization between bighorn
and domestic sheep. While few differences are expected
between these species due to their recent divergence
(~3 million years [18]), shared karyotype [19] and ability
to produce fertile hybrids [20], enough time has elapsed
for rearrangements to accumulate [21]. For example,
numerous small-scale rearrangements have been docu-
mented between domestic sheep and the slightly more
genetically distant domestic goat, Capra hircus [22],
which can also interbreed with domestic sheep [23].
Reorganization has also been observed among domestic
sheep breeds [4,24]. A bighorn sheep linkage map could
therefore be used to detect recent chromosomal rearran-
gements in sheep species and would help with inferring
ancestral marker order for regions showing intra-specific
variation.
While genome structure is anticipated to be similar
between closely related sheep species, expectations for
sex-averaged and sex-specific recombination rates are
less clear. This is because domestication may have led
to an increase in recombination rates and unusual male-
biased heterochiasmy in domestic sheep [25,26].
However,theroleofdomesticationintheevolutionof
mammalian recombination rates remains unclear due to
the absence of data on wild relatives [27,28]. A bighorn
sheep linkage map would enable such a comparison and
help to determine if domestication played a role in the
evolution of the atypical recombination patterns seen in
domestic sheep.
In this article, we report on the development of a first-
generation bighorn sheep genetic linkage map based on
the genotyping of 252 polymorphic microsatellites in
498 animals from two pedigreed wild populations:
National Bison Range (NBR), Montana, USA [14], and
Ram Mountain (RM), Alberta, Canada [15]. The avail-
ability of multiple mapping populations permitted a
comparison of intra-specific variability in map character-
istics as well as the construction of a more contiguous
map that should in principle be more representative of
the species as a whole. Marker synteny and order were
then compared between bighorn sheep and domestic
sheep to test for recent chromosomal rearrangements.
Finally, we contrasted intervals between species in terms
of sex-averaged length and sexual dimorphism to gain
insights into the impacts of domestication on the evolu-
tion of mammalian recombination rates.
Results
Genotyping success and marker polymorphism
Genotyping success was high (~95%) in both popula-
tions and is summarised in Table 1 with additional
details available in Additional file 1: List of markers,
map position and variability. Marker diversity (number
of alleles and observed heterozygosity) and the number
of informative meioses tended to be greater in the NBR
population despite a smaller number of genotyped
individuals.
Population-specific maps
Linkage analysis for population-specific datasets yielded
very similar outcomes. For this reason, only salient fea-
tures of these maps are presented here while specific
details are made available in Additional file 1 and Addi-
tional file 2: Comparison of bighorn sheep population-
specific maps. In brief, all markers assigned to a linkage
group (LG) appeared to be part of the same chromo-
some in both populations. Map contiguity was slightly
greater in the NBR map, with 230 markers distributed
along 29 LGs compared to 232 markers distributed
along 34 LGs in the RM map. The NBR sex-averaged
map spanned 2910 cM while the RM sex-averaged map
Table 1 Marker variability in bighorn sheep mapping
populations (range and mean ± 1 SD)
National Bison Range Ram Mountain
Marker typing success (%) 42.0 - 100
(95.8 ± 7.8)
52.5 - 100
(94.7 ± 8.8)
Number of alleles 2 - 12
(5.40 ± 1.89)
2-12
(4.65 ± 1.73)
Observed heterozygosity 0.06 - 0.90
(0.66 ± 0.13)
0.14 - 0.84
(0.60 ± 0.15)
Total informative meiosis 16 - 310
(225.9 ± 54.4)
42 - 285
(171.3 ± 54.1)
Female informative meiosis 15 - 146
(106.3 ± 25.6)
20 - 142
(83.2 ± 26.6)
Male informative meiosis 1 - 181
(118.1 ± 31.6)
18 - 154
(86.4 ± 28.9)
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spanned 2581.4 cM. For both populations, while the
overall female autosomal map was longer than the
equivalentmalemap(ratioof1.13inNBRand1.06in
RM), two chromosomes (5 and 15) had longer male
maps than female maps. In addition, NBR linkage
groups 10, 21, 24 and 25 were longer in the male map
while RM linkage groups 2a, 2b, 3c, 8a, 9, 11, 12, 13, 15,
16a, 18, and 19 were longer in the male map.
The most likely marker order differed between maps
in only one instance. This involved two tightly linked
markers on chromosome 1 (MCM137 and BM7145) for
which order was reversed between maps. However,
while support for the inferred order was moderate in
the NBR map (log
10
likelihood difference of 2.02,
MCM137-BM7145, 0.47 cM), support for the alternate
order in the RM map was weak (log
10
likelihood differ-
ence of 0.34, BM7145-MCM137, 0.86 cM).
A comparison of the intervals present in both maps
revealed that localized sex-averaged recombination rates
were generally similar between populations (r
2
= 0.61,
Additional file 3: Comparison of intervals present in
both population-specific bighorn sheep maps). The sum
of these intervals was accordingly similar (2382.9 cM in
NBR vs. 2427.8 cM in RM). In both populations, inter-
vals were more often longer in the female map than in
the male map (102 vs. 61 in NBR and 92 vs. 72 in RM)
but only significantly so in the NBR population (NBR, p
< 0.01; RM, p = 0.14). Sexual dimorphism in interval
length (sexual dimorphism index, SDI) was significantly
moreofteninthesamedirectionthannot(94outof
160, p < 0.05). However, interval-specific SDI was only
weakly correlated between populations (r
2
= 0.03, 95%
CI = 0 - 0.14).
Integrated bighorn sheep map
Combining the two datasets in a single linkage analysis
produced a highly contiguous map (Figure 1, Additional
file 1). In that analysis, 247 markers were assigned to 27
LGs representing all ovine autosomes and the X chro-
mosome. Since 7 markers were perfectly linked to
another marker, the map only truly depicted the loca-
tions of 240 unique mapped positions for an average of
8.9 ± 4.3 loci per chromosome. Sex-averaged intervals
were on average 14.3 ± 9.1 cM long and usually shorter
than 30 cM (Table 2, Additional file 1). The sex-limited
and pseudo-autosomal regions of chromosome X were
separated by slightly more than 50 cM in the sex-aver-
aged map due to an absence of linkage in the male map
but we decided to leave the LG intact due to evidence
for tighter linkage (21.5 cM) in the female map.
OarFCB11 was excluded from chromosome 2 because it
was estimated to be more than 50 cM away from its clo-
sest neighbouring marker (INHA). BMS1247, BMS1948
and HBB2/ii could not be assigned to a chromosome
while GHRHR was excluded due to having too few
informative meioses. The length of the complete sex-
averaged map was 3050.9 cM while the autosomal
female and male maps were 3166.1 cM and 2832.2 cM
long (1.12 ratio), respectively. Intervals were significantly
more often longer in the female map than in the male
map (119 vs. 87, p < 0.05), however four chromosomes
(5, 15, 18 and 24) had longer male than female chromo-
some maps.
Comparison of bighorn sheep and domestic sheep maps
Synteny was highly similar between the bighorn sheep
and the domestic sheep International Mapping Flock
(IMF) maps with only three observed differences
(Figure 1). First, FCB19 mapped to chromosome X in
bighorn sheep but to chromosome 15 in domestic
sheep. Second, BM4005 mapped to chromosome 2 in
bighorn sheep but to chromosome 24 in domestic
sheep. Finally, neither of the two markers amplified in
bighorn sheep with the primer pair used for MCMA54
in domestic sheep mapped to the location of this marker
predicted from the IMF map (chromosome 21). Instead,
MCMA54/i and MCMA54/ii mapped to bighorn sheep
chromosomes 1 and 9, respectively. For the three other
primer pairs which amplified two unlinked markers in
bighorn sheep (TGLA377, BMS2466, MNS97A), one of
the markers mapped to its predicted position while the
other mapped to a different chromosome (TGLA377/ii,
MNS97A/ii and BMS2466/ii were assigned to chromo-
some 3, 5 and 10, respectively). One additional putative
difference between species was observed on chromo-
some 10 for markers not mapped in the IMF but
mapped in Soay sheep, a feral domestic sheep breed [8].
The most likely order for this region in bighorn sheep
was OarSEJ10, OarSEJ11, AGLA226 and OarSEJ13 ver-
sus AGLA226, OarSEJ10, OarSEJ11 and OarSEJ13 in
Soay sheep. The difference in log
10
likelihood between
marker orders in bighorn sheep was 3.01.
The length of orthologous intervals was highly corre-
lated between species (r
2
= 0.71, p < 0.01, Figure 2,
Additional file 4: Comparison of intervals present in big-
horn sheep and domestic sheep maps) and their sum
very similar (3044 cM in bighorn sheep vs. 3001 cM in
domestic sheep; a difference of ~1.5%). This excluded
the intervals located at the tip of bighorn sheep chromo-
somes 5 (MNS97A/ii to WNT3K13, 6 cM) and 10 (Oar-
SEJ10 to AGLA226, 0.5 cM) that have no equivalent in
the IMF map. Intervals did not tend to be larger in one
species than the other (105 larger in domestic sheep vs.
98 larger in bighorn sheep, p = 0.67). Based on coverage
of these intervals in the version 4.7 IMF map, we esti-
mated the current genome coverage by the integrated
map in bighorn sheep to correspond to ~ 84% of the
domestic sheep linkage map.
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Figure 1 Bighorn sheep sex-average linkage map compared with the domestic sheep IMF map. For each chromosome, the bighorn
sheep linkage groups (LGs) are on the left while the domestic sheep LGs are on the right. Lines connect orthologous loci. Markers not mapping
to the same location in the two species are in bold while markers only mapped in bighorn sheep are italicized. The thin vertical line connecting
OarFCB11to chromosome 2 indicates that this marker was assigned to that chromosome but was excluded from the linkage analysis for being
more than 50 centimorgans (cM) away from the closest neighbouring marker. That interval was not included in the total map length estimate
and its length in the figure is arbitrary. The ruler at the top left corner represents a cM scale.
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Mean SDI in length (± 1 SD) considering only ortho-
logous intervals was 0.10 ± 1.27 in bighorn sheep and
-0.34 ± 1.33 in domestic sheep.ThepositivemeanSDI
in bighorn sheep reflected a tendency for larger intervals
in the female map (114 out of 197, p < 0.05) while the
negative mean SDI in domestic sheep indicated a ten-
dency for larger intervals in the male map (120 out of
197, p < 0.01). Interval-specific SDI was significantly
correlated between species (r
2
= 0.21, p < 0.01, Figure
3). The intercept and slope were both significantly posi-
tive (intercept ± 1 SE: 0.42 ± 0.08, p < 0.01; slope: 0.95
± 0.06, p < 0.01). In general, SDI values in bighorn
sheep tended to be greater than in domestic sheep (124
times out of 189, P < 0.001).
Discussion
As expected, marker synteny and order were generally
congruent between bighorn sheep maps. This suggests
that our dataset was mostly free of errors and justified
combining individual maps. The NBR population was
generally more informative than the RM population.
This was likely a consequence of the more complete
NBR pedigree combined with greater marker variability
resulting from recent admixture [14,16]. Nonetheless,
information provided by both populations was generally
complementary and ultimately allowed construction of a
highly contiguous map covering approximately 84% of
the species genome. This is greater coverage than for a
similar map for free-ranging red deer (Cervus elephus,
39% [3]) and almost on a par with one for Soay sheep
(Ovis aries, 90% [4]) for which virtually all genetic
resources developed for domestic sheep can be used.
The coverage of our map is therefore similar to a first-
generation map for a domestic species and outstanding
for a wild species.
Recombination fractions were very similar between
bighorn sheep populations. Combining pedigrees into a
single analysis therefore likely resulted in map distances
Table 2 Descriptive statistics for the integrated bighorn sheep map
Map length (cM) No. of intervals (Sex-averaged length)
Linkage group No. of markers No. of intervals Sex-averaged Female Male 0 - 15 cM 15 - 30 cM >30 cM
1 22 21 302.8 326.3 284.9 13 7 1
2 18 17 274.3* 290.9* 264* 11 3 3
3 16 15 272.7 303.5 250.1 7 6 2
4 10 8 142.7 167.6 124 3 4 1
5 10 8 132.8 125.2 148.1 3 5 0
6 13 11 138.9 148.3 135.4 8 3 0
7 9 8 125.3 136.8 116.8 4 4 0
8 9 8 127.9 155.6 122.9 6 1 1
9 12 10 115.5 122.5 109.9 7 3 0
10 10 8 64.2 65 64 8 0 0
11 6 5 108.2 118.3 99.2 2 1 2
12 9 8 102.9 107.3 99.5 4 4 0
13 9 8 120.6 122.5 119.7 5 2 1
14 9 7 82.5 92.2 75.3 6 1 0
15 11 10 112.8 110.5 118.8 9 1 0
16 5 4 67.6 77.4 62.3 2 2 0
17 9 7 97.3 100.5 97.3 3 4 0
18 10 9 96.9 94.4 97.4 6 3 0
19 6 5 75.5 75.5 74.8 3 2 0
20 6 5 71.5 77.9 66.3 4 1 0
21 3 2 16.3 16.6 16 2 0 0
22 5 4 51.9 60.9 45.8 3 1 0
23 8 7 71.9 82 63.9 6 1 0
24 3 2 44 41.3 47.9 1 0 1
25 4 3 83.3 89 80.8 0 1 2
26 6 5 51.3 58 46 4 1 0
X 9 8 99.2 170.6 1.3** 7 0 1
Total 247 213 3050.8 3336.6 2832.4 137 61 15
*excluding FCB11 which is more than 50 cM away.
**Pseudo-autosomal region.
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that were generally representative of the species as a
whole. While genuine intra-specific differences may
exist in map distances, the integrated map is likely to
more accurately depict recombination fractions of indi-
vidual populations than the estimates derived from the
population-specific maps. This is because interval
estimates for population-specific maps were often based
on relatively few informative meioses, especially in the
RM population. Relying on distances from the integrated
map in future downstream population-specific studies is
therefore advisable.
As predicted, marker synteny and order were generally
congruent between the Ovis species maps. This is in line
with the expectation of 1 to 2 rearrangements per mil-
lion years in most mammalian lineages [20]. However, it
has to be acknowledged that marker coverage was gen-
erally too sparse to detect subtle rearrangements. Cross-
species comparison was also made difficult by the fact
that some primer pairs amplified two loci. For example,
BM4005 mapped to different locations in each species
but we are aware of a second locus for BM4005 in big-
horn sheep that could not be reliably genotyped. Since
primers for BM4005 are also known to amplify multiple
sets of bands in domestic sheep [29], the BM4005 loci
mapped in the two species are probably not ortholo-
gous. Similarly, FCB19 mapped to chromosome X in
bighorn sheep but to chromosome 15 in domestic
sheep. This marker is definitely autosomal in domestic
sheep given that a fraction of males are undoubtedly
heterozygous (J. Maddox, unpublished data) so the dis-
crepancy in map location is not spurious. However,
FCB19 markers amplified in the two species might not
be orthologous given that a single primer pair can
amplify multiple markers. In contrast, convincing evi-
dence for cross-species rearrangement came from the
primers used to amplify MCMA54 in domestic sheep.
In that case, neither of the two markers amplified using
this primer pair in bighorn sheep mapped to the loca-
tion of the MCMA54 locus in domestic sheep (the
MCMA54 primers amplified two band sets that both
mapped to chromosome 21 in domestic sheep vs. 1 and
9 in bighorn sheep). The comparison of our map with
the Soay sheep map [8] also suggested the presence of a
minor rearrangement on chromosome 10. While some
of these cases may depict genuine rearrangements, it is
clear from this study that the organization of the two
species genomes is very similar.
Genomic analysis in a close relative of domestic sheep
offered the opportunity to infer ancestral marker order
for chromosomal regions showing variation among
domestic sheep breeds [4,26]. For chromosome 1, the
order of two loci located in the rearranged region
(MCM137 and BM7145) was similar between the NBR
and the IMF maps [24]. On the other hand, the most
likely marker order in the RM map was similar to an
alternate order documented in Soay sheep [24]. Inferred
marker orders were arguably not significantly more
likely than the alternate orders. Yet, it is worth noting
that this chromosomal region was the only one for
which the most likely marker order differed between
Figure 2 Comparison of sex-averaged interval length (cM) in
bighorn sheep and domestic sheep for 203 pairs of adjacent
markers. The solid line depicts the relationship between bighorn
sheep and domestic orthologous intervals (reduced major axis
regression, y = 1.14 × - 1.83, r
2
= 0.72, 95% CI = 0.60, 0.80) while
the dashed line separates intervals larger in bighorn sheep (above
line, n = 105) from intervals larger in domestic sheep (below line,
n = 98).
Figure 3 Comparison of sexual dimorphism (SDI) in interval
length between orthologous bighorn sheep and domestic
sheep intervals. 192 intervals between adjacent markers were
compared (reduced major axis regression, y = 0.95 × + 0.42, r
2
=
0.21, 95% CI = 0.09, 0.37). SDI values are positive when intervals are
larger in females and negative when intervals are larger in males.
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bighorn sheep maps. If both orders are present in big-
horn sheep, it would mean that this region is either
prone to rearrangements or that polymorphism in mar-
ker order originated millions of years ago rather than
recently as hypothesised by McRae and Beraldi [24]. For
a second putatively varying region located on chromo-
some 12 [4], we only successfully amplified one
(BM4025) of the two markers used to infer rearrange-
ment in domestic sheep (BM4025 and TGLA53). How-
ever, marker order in bighorn sheep for that region
appeared to be the same as in the IMF map based on a
marker located only 2 cM away from TGLA53 in
domestic sheep (CSAP01E). Therefore, the IMF
appeared to portray the ancestral marker order.
The comparison of orthologous intervals suggested
high similarity in localized sex-averaged recombination
rates between the Ovis species. While the near perfect
concordance in total map length (~1%) may be coinci-
dental, given that variation in the order of 10% has been
documented among domestic sheep breeds [4], it none-
theless strongly suggests little difference between spe-
cies. Assuming that results were not unduly biased by
missing and erroneous genotypes (which can be a con-
cern when using CRI-MAP in complex pedigrees
[2,30]), it appears that the elevated recombination rates
observed in domestic sheep are a characteristic of Ovis
species rather than a consequence of domestication.
Alternatively, recombination rates may have increased
rapidly in both species since their recent divergence as a
consequence of domestication in domestic sheep and
for a different reason in bighorn sheep. But, this later
explanation seems unlikely since the evolution of mean
recombination rates in mammals is generally slow and
most likely governed by neutral processes [28].
Contrary to what has been found for domestic sheep,
recombination rates in bighorn sheep tended to be
greater in females than in males. The unusual pattern
observed in domestic sheep therefore appeared to be spe-
cies-specific. This finding is not overly surprising given
the low phylogenetic inertia of the trait [31]. The magni-
tude of heterochiasmy in sheep species is also arguably
modest when compared with species such as the salt-
water crocodile (Crocodylus porosus, ratio of 5.7:1 [32])
or the zebrafish (Danio rerio, ratio of 2.74:1 [33]). Yet,
the presence of male-biased recombination in domestic
sheep remains puzzling given that recombination in pla-
cental mammals is generally female-biased [26]. An intui-
tive explanation is that altered sex-specific recombination
patterns in domesticated mammals (cattle are also atypi-
cal, exhibiting no heterochiasmy [34]) might be an inci-
dental result of strong artificial selection during the
process of domestication. Alternatively, the unusual het-
erochiasmy pattern documented in the domestic IMF
might simply be an artefact resulting from the facts that
the population size was small, all sires descended from a
single grand-sire and there were only three maternal
grandsires compared to 13 granddams. Knowing that
recombination rates can vary substantially among indivi-
duals, and that such differences can have a large genetic
component (e.g. [35]), it could be that the paternal
grand-sire was characterised by an uncommonly high
recombination rate breeding value and/or that some of
the maternal grandsires were characterised by uncom-
monly small recombination rate breeding values (assum-
ing that male and female recombination rates are
positively genetically correlated [36]). A comparison of
sex-specific recombination rates in additional domestic
sheep pedigrees might answer this question.
As in other taxa (e.g. [37,38]), great variability was
observed in patterns of heterochiasmy across and along
chromosomes. For example, recombination appeared to
be male-biased for a few chromosomes despite the pre-
sence of a genome-wide tendency for greater recombi-
nation in females. However, no clear pattern emerged at
the chromosomal level with the NBR and RM maps
yielding mainly inconsistent results. At the interval
scale, patterns of sexual dimorphism were conserved
across populations and species. This means, for exam-
ple, that genomic regions characterized by low SDI
values in one species were mirrored by similarly low
SDI values in the other species. This could be due to
conserved sex-specific and/or sex-biased recombination
hot-spots. However, fine-scale analyses of recombination
rates in other pairs of closely related species (e.g. human
and chimpanzee [39,40]) suggest that this is unlikely at
the inter-specific level. Inter-specific congruence in loca-
lized recombination rate sexual dimorphism could also
be due to the position of intervals along chromosomes
relative to centromeres and telomeres, irrespective of
the exact location of individual hot-spots. For example,
in humans, recombination tends to be greater in females
near centromeres but greater in males near telomeres
(reviewed in [41]). In domestic sheep, recombination in
telomeric and centromeric regions is usually greater in
males (J Maddox, unpublished data). To verify if a simi-
lar pattern was also present in bighorn sheep, we con-
trasted bighorn sheep interval-specific SDI to the
relative distance of these intervals from centromeres and
telomeres inferred from the location of these intervals in
the IMF map. A pattern similar to that seen in domestic
sheep was observed, with recombination being greater
in males near centromeres and telomeres while being
greater in females in more central parts of chromosomes
(Figure 4).
Conclusion
We constructed a first-generation bighorn sheep link-
age map using DNA from two wild pedigreed
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population and genomic resources originally developed
for domestic sheep. Since bighorn sheep and domestic
sheep genomes are very similar, future efforts to
increase marker density in specific chromosomal
regions should be relatively straightforward. This could
be achieved using bighorn sheep single nucleotide
polymorphism (SNP) markers recently discovered
using the OvineSNP50 Beadchip [42], additional
microsatellites already mapped in domestic sheep and/
or by taking advantage of the recently acquired domes-
tic sheep genome sequence [43] to develop novel mar-
kers. The high similarity between the genomes of the
two species should also greatly facilitate future efforts
to assemble a bighorn sheep genome sequence and to
develop additional SNPs.
The main reason for developing genomic resources in
bighorn sheep is to allow studies of complex trait
genetic architecture and evolution under natural set-
tings. In the NBR population, genomic resources will
enable investigations into the genetic basis of fitness,
inbreeding depression and genetic rescue [14]. In RM, it
will be possible to study the genetic architecture of addi-
tional traits including body mass, horn size and animal
personality [15,44]. Finally, genomic information could
eventually be combined with population genetic
approaches to study adaptive population differentiation
[45], especially in the context of parasitism [46] and
selective harvesting [47].
While resources developed for domestic sheep are
obviously highly useful to bighorn sheep research, geno-
mic research in bighorn sheep can also yield valuable
information through comparisons with domestic sheep
in return. For example, we have demonstrated how link-
age mapping in bighorn sheep can be used to infer
ancestral marker order in domestic sheep. Also, by com-
paring the domestic sheep map with the map of a close
wildrelative,wewereabletodeterminethattheele-
vated recombination rates observed in domestic sheep
were likely a characteristic of Ovis species while the
unusual male-biased heterochiasmy might have been a
consequence of domestication. Finally, we have demon-
strated that interval-specific patterns of sexual dimorph-
ism could be conserved among closely related species,
possibly due to the position of these intervals relative to
centromeres and telomeres.
Methods
Study populations
National Bison Range
The NBR population was established by transplanting
four rams and eight potentially pregnant ewes from
Banff National Park (Alberta, Canada) in 1922 [14]. The
population remained isolated until the introduction of
five rams in 1985 and 10 sheep (three rams and seven
ewes) from 1990 to 1994. Fourteen of these more
recently introduced animals were derived from a native
Montana population (Sun River) while one ewe was
from a native Wyoming herd (Whisky Basin). Indivi-
duals from these latter introductions were highly suc-
cessful [14], resulting in relatively high levels genetic
diversity and linkage disequilibrium [16]. All sheep were
individually recognizable through physical characteristics
from 1979 onward and collection of blood/tissue sam-
ples for genetic analysis began in 1988. Our analyses
included a combination of descendants from the original
introduction, recent immigrants and admixed
individuals.
Ram Mountain
The RM population is native to a small isolated moun-
tain range located about 50 km east of the Canadian
Rockies in Alberta, Canada [15]. Immigration and emi-
gration is highly restricted and mainly limited to
exchanges with a smaller unmonitored herd located on
the same mountain range. Animals were captured in a
corral trap baited with salt and marked with unique tags
as lambs or yearlings. Population monitoring began in
the early 1970s and collection of hair/blood/skin sam-
ples for genetic analysis began in 1988.
Mapping pedigrees
In both populations, parentage was originally deter-
mined with ~30 microsatellite loci using the 95% confi-
dence threshold in Cervus [48]. For the RM population,
the markers used are presented in [15] and references
therein. For the NBR population, the markers included
the ones listed in [14] as well as BL25, BM1225,
Figure 4 Relationship between interval length sexual
dimorphism (SDI) and relative distance from centromeres and
telomeres in bighorn sheep. The location of each interval relative
to centromeres (0) and telomeres (1) were inferred using the
position of orthologous intervals in the domestic sheep IMF map
version 4.7. The fitted curve is a second order polynomial (r
2
= 0.16,
quadratic term fitted in a linear model, p < 0.001).
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BM1818, BM4505, BM4630, BM848, BMC1222, MAF92,
OarJMP29, TGLA126, TGLA387, EPCDV21, MCMA54/
i and MCMA54/ii. Laboratory methods are detailed in
[14,15] and references therein. References for primer
sequences are available in Additional file 1. Recon-
structed pedigrees were used to identify animals
expected to contribute the most information for linkage
mapping purposes (e.g. large sibships and their parents)
and these animals were then genotyped at more than
200 microsatellite loci (details below). Once genome-
wide genotypes were obtained, animals for which geno-
typing success was low (< 65%) were discarded and the
pedigrees were updated based on new parentage ana-
lyses. Following these steps, no more than 2-3 mis-
matches were observed between parent-offspring pairs.
The software Pedcheck [49] was then used to identify
Mendelian inconsistencies which were corrected when
possible or otherwise eliminated by deleting the geno-
types of the individuals involved. The resulting NBR and
RM mapping pedigrees spanned seven and six genera-
tions and included 212 and 286 related individuals,
respectively. Pedigree illustrations produced using Pedi-
gree Viewer [50] are available in Additional file 5: Big-
horn sheep mapping pedigrees. The NBR pedigree
contained 184 paternal links (42 sires, mean ± 1 SD of
4.4 ± 3.5 offspring per sire) and 173 maternal links (51
dams, 3.4 ± 2.1 offspring per dam). The RM pedigree
consisted of 168 paternal links (43 sires, 3.9 ± 3.3 off-
spring per sire) and 172 maternal links (71 dams, 2.4 ±
1.3 offspring per dam).
Microsatellite selection and genotyping
In addition to markers used for the initial pedigree
reconstruction, microsatellites putatively distributed
throughout the genome of our focal species were iden-
tified using the domestic sheep IMF map version 4.7
[16,51]. Markers were selected based on their predicted
genomic location and level of polymorphism (assessed
in ~30 individuals/population) with the aim of optimis-
ing genomic coverage and meiotic information. Most
but not all markers were typed in both populations.
Eleven markers were only genotyped in the NBR popu-
lation while 17 were only typed in the RM population
(see Additional file 1). Laboratory methods are avail-
able in [16] and references for primer sequences
[8,16,51-55] are presented in Additional file 1. In total,
252 markers, amplified using 244 pairs of primers (8
primer pairs amplified two markers: BM3212,
BMS2466, HBB2, MCMA54, MNS97A, MNS101A,
TGLA176, TGLA377), were included in the linkage
analysis. Descriptive statistics (typing success, number
of alleles and observed heterozygosity) were obtained
using MSA 4.05 [56].
Linkage analysis
We constructed population-specific linkage maps as well
as an integrated map where populations were treated as
independent families using CRI-MAP [57]. The same
construction procedure was used for all maps. First,
two-point linkage analyses were performed for all pairs
of markers assuming equal recombination rates between
the sexes using a modified version of CRI-MAP devel-
oped by Liu and Grosz [58]. The program AUTO-
GROUP [58] was then used to identify sets of markers
likely residing in the same LG (pairwise LOD scores >
4). For markers unassigned to a LG following that analy-
sis, two-point LOD scores were inspected and in cases
where the most likely linkage was with a marker known
to be adjacent in the domestic sheep IMF map, the mar-
ker was assumed to be part of the same LG in bighorn
sheep. In cases where multiple bighorn sheep LGs were
composed of markers known to be part of the same
chromosome in domestic sheep, two-point LOD scores
between markers residing at the end of each bighorn
sheep LG were inspected and linkage was assumed
when the LOD scores were among the highest for these
respective markers. For each putative LG, the most
likely marker order was recovered using the BUILD and
FLIPSn options of a CRI-MAP version recently devel-
oped by Jill Maddox and Ian Evans (2.503) that more
efficiently deals with large datasets. Specifically, we first
constructed LGs using BUILD and a LOD > 3 threshold.
Markers were then successively added to these LGs
using less stringent LOD thresholds of 2, 1, 0.5 and 0.
The FLIPSn option was then used to compare the likeli-
hood of alternate orders produced by shuffling up to
five adjacent loci and markers were re-ordered when a
more likely order was identified. Doubtful tight double
recombinants were identified using the CHROMPIC
option of CRI-MAP and responsible erroneous geno-
types were corrected when present. Finally, sex-averaged
and sex-specific recombination fractions for individual
LGs were estimated using the FIXED option of CRI-
MAP 2.503 and transformed to centimorgans (cM)
using the Kosambi map function [59]. In cases where
estimated sex-averaged intervals were greater than 50
cM, LGs were broken in two and separate analyses were
performed for markers on each side of the interval.
Comparison of linkage maps
In order to assess intra- and inter-specific variability in
genomic structure and recombination rates, we com-
pared the NBR and RM linkage maps as well as the big-
horn sheep integrated map and domestic sheep IMF
map version 4.7. Differences in marker synteny and
order were identified by visual inspection. In cases
where the most likely marker order differed between
Poissant et al.BMC Genomics 2010, 11:524
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populations/species, support for alternate orders was
determined by comparing log
10
likelihoods. The relative
sex-averaged length of different maps was compared by
summing the length of intervals that were present in
both maps (raw data available in Additional file 3 and
Additional file 4).
To test for a genome-wide difference in sex-averaged
recombination rate between population/species, we used
two-tailed sign tests contrasting the number of shared
intervals greater in length in one map than in the other.
We also used reduced major axis regression to describe
the relationship between interval-specific sex-averaged
recombination rates between populations/species. The
slopes, intercepts and their errors were obtained using
the formula from Sokal and Rohlf [60] implemented in
thesoftwareRMAversion1.17[61].Confidenceinter-
vals including the ones for correlation coefficients were
obtained by performing 10000 bootstraps.
To assess variation in heterochiasmy across popula-
tions and species genomes, we quantified sexual
dimorphism for individual intervals using the sexual
dimorphism index (SDI) of Lovich and Gibbons [62].
This index is considered the best estimator of sexual
dimorphism because it is intuitive, linear, symmetrical,
and directional [63]. The SDI was obtained by sub-
tracting 1 from the ratio of the largest sex-specific
value to the smallest sex-specific value. Following con-
vention, estimates were then made positive when the
female value was largest and negative when the male
value was largest. We tested for the presence of gen-
ome-wide bias in sexual dimorphism using sign tests
and described the relationship in interval-specific sex-
ual dimorphism between maps using reduced major
axis regression.
Since the length of an interval partly depends on the
subset of markers included in a linkage analysis, we
assessed the validity of comparing intervals between
maps constructed using different number of markers
(the domestic sheep IMF map 4.7 contains about 1400
markers). To accomplish this, we repeated cross-species
analyses using information derived from additional link-
age maps based solely on markers mapped in both spe-
cies. Results and conclusions were essentially the same
as for previous analyses and are therefore not presented.
These maps are available in Additional file 6: Bighorn
sheep and domestic sheep linkage maps based on shared
markers only.
Ethics
All research protocols were approved by the University
of Alberta Animal Use and Care Committee, affiliated
with the Canadian Council for Animal Care (Certificate
610901).
Additional material
Additional file 1: List of markers, map position and variability. Excel
document displaying List of markers, map position and variability.
Additional file 2: Comparison of bighorn sheep population-specific
maps. PDF displaying comparison of bighorn sheep population-specific
maps.
Additional file 3: Comparison of intervals present in both
population-specific bighorn sheep maps. XLS file displaying
comparison of intervals present in both population-specific bighorn
sheep maps.
Additional file 4: Comparison of intervals present in bighorn sheep
and domestic sheep maps. XLS file displaying comparison of intervals
present in bighorn sheep and domestic sheep maps.
Additional file 5: Bighorn sheep mapping pedigrees. PDF file
displaying bighorn sheep mapping pedigrees.
Additional file 6: Bighorn sheep and domestic sheep linkage maps
based on shared markers only. XLS bighorn sheep and domestic
sheep linkage maps based on shared markers only.
Acknowledgements
The molecular work presented here was supported by grants from the
Alberta Conservation Association, the Natural Sciences and Engineering
Council of Canada (NSERC) and Alberta Ingenuity (AI). The NBR field study
was supported by grants from The Charles Engelhard Foundation, Eppley
Foundation for Research and National Geographic Society. JPsPh.D.
research was supported by graduate scholarships from NSERC, AI, and the
University of Alberta. We thank the U.S. Fish and Wildlife Service for ongoing
cooperation and assistance at the NBR study site and the numerous field
assistants for their help throughout the years. We thank Jon Jorgenson,
Marco Festa-Bianchet and the numerous field assistants who worked at RM
over the years. Finally, we thank Ian Evans for his assistance with developing
an improved version of CRI-MAP.
Author details
1
Department of Biological Sciences, University of Alberta, Edmonton, Alberta,
T6G 2E9, Canada.
2
Montana Conservation Science Institute, 5200 Upper
Miller Creek Road, Missoula, MT 59803, USA.
3
Department of Veterinary
Science, University of Melbourne, Victoria 3010, Australia.
Authorscontributions
JP designed the study, conducted laboratory work, performed data analysis
and wrote the manuscript. JTH designed and supervised fieldwork at NBR
and performed paternity analyses. CSD implemented laboratory methods
and performed laboratory work. JMM participated in laboratory work and
data analysis. JFM provided marker information and constructed a domestic
sheep linkage map composed solely of markers mapped in bighorn sheep.
DWC planned and supervised the study. All co-authors read and
commented on draft versions of the manuscript. All authors read and
approved the final manuscript.
Received: 20 April 2010 Accepted: 28 September 2010
Published: 28 September 2010
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doi:10.1186/1471-2164-11-524
Cite this article as: Poissant et al.: Genetic linkage map of a wild
genome: genomic structure, recombination and sexual dimorphism in
bighorn sheep. BMC Genomics 2010 11:524.
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Poissant et al.BMC Genomics 2010, 11:524
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... Interestingly, sheep are hypothesized to exhibit higher numbers of COs in comparison to other mammalian species with a similar number of chromosome arms [Maddox et al., 2001;Coop and Przeworski, 2007;Johnston et al., 2016]. Furthermore, according to sex-specific linkage map lengths, male sheep are thought to exhibit a greater number of COs than females [Maddox et al., 2001;Lenormand and Dutheil, 2005;Poissant et al., 2010;. Characterizing meiotic recombination in male sheep will provide valuable information towards a better understanding of recombination in mammals. ...
... Although the total number of COs that occur in a meiotic cell is known to differ between strains of mice, this is only beginning to be evaluated in livestock species [Sandor et al., 2012;Murdoch et al., 2010;Poissant et al., 2010;Vozdova et al., 2013;Fröhlich et al., 2015;Ma et al., 2015;Johnston et al., 2016;Kadri et al., 2016;Sebestova et al., 2016]. In this study, the numbers of COs were quantified and their locations on the SC characterized in males from different breeds of sheep. ...
Article
Full-text available
Meiotic recombination is an important contributor to genetic variation and ensures proper chromosome segregation during gametogenesis. Previous studies suggest that at least 1 crossover (CO) per chromosome arm is important to avoid mis-segregation. While the total number of COs per spermatocyte is known to differ in mice, this is only beginning to be evaluated in sheep. This study used a cytogenetic approach to quantify and compare the number of COs per spermatocyte in rams from 3 breeds of sheep: Suffolk, Icelandic, and Targhee. In total, 2,758 spermatocytes and over 170,000 COs were examined. Suffolk rams exhibited the lowest mean number of COs (61.1 ± 0.15) compared to Icelandic (63.5 ± 0.27) and Targhee (65.9 ± 0.26) rams. Significant differences in the number of COs per spermatocyte were observed between Suffolk, Icelandic, and Targhee breeds as well as within each breed. Additionally, the number and location of COs were characterized for homologous chromosomes in a subset of spermatocytes for each ram. A positive correlation was identified between the number of COs and the length of the homologous chromosome pair. Suffolk and Icelandic rams exhibited up to 7 COs per chromosome, while Targhee rams exhibited up to 9. Further, distinct CO location preferences on homologous chromosome pairs with 1, 2, 3, and 4 COs were observed in all 3 breeds. These data in sheep will aid in elucidating the mechanism of mammalian meiotic recombination, an important contributor to genetic diversity.
... IASC intensity is often measured as the intersexual genetic correlation for fitness (r MF ), which is the fraction of sexually antagonistic genetic variance (between-sex genetic covariance for fitness) relative to total additive genetic variance for fitness (see Table 1). It has been shown that both intersexual genetic covariance (Lyons, Miller & Meagher, 1994;Falconer & Mackay, 1996;Simons & Roff, 1996;Leips & Mackay, 2000;Vieira et al., 2000;Fox et al., 2004;Delcourt et al., 2009;Poissant et al., 2010;Punzalan, Delcourt & Rundle, 2014) and genetic variance (Via & Lande, 1987;Fowler & Whitlock, 2002;Charmantier & Garant, 2005) can be shaped by environment. However, environmental differences in these parameters are hard to predict. ...
Article
Full-text available
Sexual conflict has extremely important consequences for various evolutionary processes including its effect on local adaptation and extinction probability during environmental change. The awareness that the intensity and dynamics of sexual conflict is highly dependent on the ecological setting of a population has grown in recent years, but much work is yet to be done. Here, we review progress in our understanding of the ecology of sexual conflict and how the environmental sensitivity of such conflict feeds back into population adaptivity and demography, which, in turn, determine a population's chances of surviving a sudden environmental change. We link two possible forms of sexual conflict - intralocus and interlocus sexual conflict - in an environmental context and identify major gaps in our knowledge. These include sexual conflict responses to fluctuating and oscillating environmental changes and its influence on the interplay between interlocus and intralocus sexual conflict, among others. We also highlight the need to move our investigations into more natural settings and to investigate sexual conflict dynamics in wild populations.
... Intersex differences in the frequency of a given allele may also be due to intersex differences in recombination rates; up to 75% of species that undergo recombination in their genome have different recombination rates per sex (Burt et al., 1991;Wyman and Wyman, 2013). In the majority of species, the male recombination rate is generally lower than in females (Poissant et al., 2010;Wyman and Wyman, 2013). It is thought that this lower recombination rate is advantageous to males as it maintains combinations of beneficial genes that have undergone sexual selection (Trivers, 1988); however, studies in both cattle (Ma et al., 2015) and sheep (Maddox and Cockett, 2007) reported that the male recombination rate in these species is actually higher than the females. ...
Article
Sexual dimorphism, the phenomenon whereby males and females of the same species are distinctive in some aspect of appearance or size, has previously been documented in cattle for traits such as growth rate and carcass merit using a quantitative genetics approach. No previous study in cattle has attempted to document sexual dimorphism at a genome level; therefore, the objective of the present study was to determine if genomic regions associated with size and muscularity in cattle exhibited signs of sexual dimorphism. Analyses were undertaken on 10 linear type traits that describe the muscular and skeletal characteristics of both males and females of 5 beef cattle breeds; 1,444 Angus (AA), 6,433 Charolais (CH), 1,129 Hereford (HE), 8,745 Limousin (LM), and 1,698 Simmental (SI). Genome wide association analyses were undertaken using imputed whole-genome sequence data for each sex separately by breed. For each SNP that was segregating in both sexes, the difference between the allele substitution effect sizes for each sex, in each breed separately, was calculated. Suggestively (p ≤ 1 x 10 -5) sexually dimorphic SNPs that were segregating in both males and females were detected for all traits in all breeds, although the location of these SNPs differed by both trait and breed. Significantly (p ≤ 1 x 10 -8) dimorphic SNPs were detected in just three traits in the AA, seven traits in the CH and three traits in the LM. The vast majority of all segregating autosomal SNPs (86% in AA to 94% in LM) had the same minor allele in both males and females. Differences (p ≤ 0.05) in allele frequencies between the sexes were observed for between 36% (LM) and 66% (AA) of the total autosomal SNPs that were segregating in both sexes. Dimorphic SNPs were located within a number of genes related to muscularity and/or size including the NAB1, COL5A2, and IWS1 genes on BTA2 that are located close to, and thought to be co-inherited with, the MSTN gene. Overall, sexual dimorphism exists in cattle at the genome level, but it is not consistent by either trait or breed.
... Speciation between domestic and bighorn sheep occurred about three million years ago, but the two species can interbreed to produce viable hybrid offspring (Bunch et al., 2006;Young & Manville, 1960). Domestic and bighorn sheep have the same number of chromosomes and are expected to have high genomic synteny (Poissant et al., 2010). An estimated 24,000 SNPs in the HD Ovine array are informative for Rocky Mountain bighorn sheep, and the domestic sheep reference genome enables mapping SNPs to chromosomes (Kohn et al., 2006;Miller et al., 2015). ...
Article
Full-text available
Wildlife restoration often involves translocation efforts to reintroduce species and supplement small, fragmented populations. We examined the genomic consequences of bighorn sheep (Ovis canadensis) translocations and population isolation to enhance understanding of evolutionary processes that affect population genetics and inform future restoration strategies. We conducted a population genomic analysis of 511 bighorn sheep from 17 areas, including native and reintroduced populations that received 0–10 translocations. Using the Illumina High Density Ovine array, we generated datasets of 6,155 to 33,289 single nucleotide polymorphisms and completed clustering, population tree, and kinship analyses. Our analyses determined that natural gene flow did not occur between most populations, including two pairs of native herds that had past connectivity. We synthesized genomic evidence across analyses to evaluate 24 different translocation events and detected eight successful reintroductions (i.e., lack of signal for recolonization from nearby populations) and five successful augmentations (i.e., reproductive success of translocated individuals) based on genetic similarity with the source populations. A single native population founded six of the reintroduced herds, suggesting that environmental conditions did not need to match for populations to persist following reintroduction. Augmentations consisting of 18–57 animals including males and females succeeded, whereas augmentations of two males did not result in a detectable genetic signature. Our results provide insight on genomic distinctiveness of native and reintroduced herds, information on the relative success of reintroduction and augmentation efforts and their associated attributes, and guidance to enhance genetic contribution of augmentations and reintroductions to aid in bighorn sheep restoration.
... Empirical work on indirect selection of physiology-related traits in Drosophila supports this view (Korol and Iliadi 1994;Aggarwal et al. 2015). However, for domesticated animals that underwent strong directional selection, there seems to be no increase of recombination rate (Munoz-Fuentes et al. 2015), contradicting previous views of elevated recombination in domesticated plants (Ross-Ibarra 2004) and animals (Burt and Bell 1987;Poissant et al. 2010). ...
Article
Full-text available
Theories predict that directional selection during adaptation to a novel habitat results in elevated meiotic recombination rate. Yet the lack of population-level recombination rate data leaves this hypothesis untested in natural populations. Here we examine the population-level recombination rate variation in two incipient ecological species, the microcrustacean Daphnia pulex (an ephemeral-pond species) and D. pulicaria (a permanent-lake species). The divergence of D. pulicaria from D. pulex involved habitat shifts from pond to lake habitats as well as strong local adaptation due to directional selection. Using a novel single-sperm genotyping approach, we estimated the male-specific recombination rate of two linkage groups in multiple populations of each species in common garden experiments and identified a significantly elevated recombination rate in D. pulicaria. Most importantly, population genetic analyses show that the divergence in recombination rate between these two species is most likely due to divergent selection in distinct ecological habitats rather than neutral evolution.
... and bighorn sheep are closely related, sharing a common ancestor approximately 3 million years ago 42,43 , with a high degree of genome synteny 44 . Similarity in host genetic ancestry may facilitate pathogen spillover 45 and this is backed by our phylogenetic analysis, which revealed the majority of bighorn M. ovipneumoniae strains were most closely related to those from domestic sheep. ...
Article
Full-text available
Spillover diseases have significant consequences for human and animal health, as well as wildlife conservation. We examined spillover and transmission of the pneumonia-associated bacterium Mycoplasma ovipneumoniae in domestic sheep, domestic goats, bighorn sheep, and mountain goats across the western United States using 594 isolates, collected from 1984 to 2017. Our results indicate high genetic diversity of M. ovipneumoniae strains within domestic sheep, whereas only one or a few strains tend to circulate in most populations of bighorn sheep or mountain goats. These data suggest domestic sheep are a reservoir, while the few spillovers to bighorn sheep and mountain goats can persist for extended periods. Domestic goat strains form a distinct clade from those in domestic sheep, and strains from both clades are found in bighorn sheep. The genetic structure of domestic sheep strains could not be explained by geography, whereas some strains are spatially clustered and shared among proximate bighorn sheep populations, supporting pathogen establishment and spread following spillover. These data suggest that the ability to predict M. ovipneumoniae spillover into wildlife populations may remain a challenge given the high strain diversity in domestic sheep and need for more comprehensive pathogen surveillance.
... While there are limits to how distantly related a species one can use (Cosart 2013;Miller et al. 2012), and concerns related to potential biases (Powell et al. 2016;Shafer et al. 2016), the genomeenabled nature of ungulates has permitted addressing genome-scale questions in ungulates well before other taxonomic groups. The application of cross-amplified markers has been used to generate relatively dense linkage maps (Poissant et al. 2010;Slate et al. 2002), assess population structure (Miller et al. 2011; Assembly length is reported in megabases (Mb) and N50 scaffold is equal to the length of the longest sequence where the sum of the lengths is greater than or equal to half the length of the genome being assembled and Latch 2012; Iacolina et al. 2016), scan for adaptive loci (Sim et al. 2016;Powell et al. 2016;Roffler et al. 2016a, b), and assay functional gene variation (Slate et al. 2009;Shafer et al. 2012). Moreover, both population monitoring and management of wild ungulates have routinely relied on markers developed in the non-focal species (Corti et al. 2011;Ogden et al. 2012;Olson et al. 2012). ...
Chapter
Humans have long relied on ungulates for food, clothing, manual labor, and transportation. Ungulates were among the first species to be domesticated and managed in the wild, but more than one-third of species are currently of conservation concern. Starting in the late twentieth century, ungulate research and management began employing genetic tools to assess attributes like the degree of population structure, inbreeding, and variation in functionally important genes. As sequencing technology advanced, research on ungulates shifted to now assay variation across the entire genome. More than 20 ungulates have had their genome assembled with a mean length of 2.6 Gb and N50 of 26 Mb. Genomic studies have provided deeper insights into the evolutionary relationships among giraffes and bovids, while camelids and horses have had their entire species demographic histories reconstructed using novel Markovian coalescent models. Moreover, artificial and natural selection has left clear signatures on ungulate genomes with high-throughput sequencing techniques being used to identify the genetic basis to important phenotypic traits. Novel assembly strategies and genomic assays are regularly being employed on ungulates, and research on this ecological and economically valuable group will help chart the course of the emerging field of wildlife genomics.
... Species divergence between domestic sheep and bighorn sheep took place around three million years ago (Bunch, Wu, Zhang, & Wang, 2006), but domestic sheep and bighorn sheep can interbreed and produce viable hybrid offspring (Young & Manville, 1960). In addition, the two species have the same number of chromosomes and are expected to have high genomic synteny (Poissant et al., 2010). An estimated 24,000 SNPs on the HD Ovine array are informative for evaluation of Rocky Mountain bighorn sheep (Miller, Moore, Stothard, Liao, & Coltman, 2015). ...
Article
Inbreeding and relationship metrics among and within populations are useful measures for genetic management of wild populations, but accuracy and precision of estimates can be influenced by the number of individual genotypes analysed. Biologists are confronted with varied advice regarding the sample size necessary for reliable estimates when using genomic tools. We developed a simulation framework to identify the optimal sample size for three widely used metrics to enable quantification of expected variance and relative bias of estimates and a comparison of results among populations. We applied this approach to analyse empirical genomic data for 30 individuals from each of four different free‐ranging Rocky Mountain bighorn sheep (Ovis canadensis canadensis) populations in Montana and Wyoming, USA, through cross‐species application of an Ovine array and analysis of approximately 14,000 single nucleotide polymorphisms (SNPs) after filtering. We examined intra‐ and interpopulation relationships using kinship and identity by state metrics, as well as FST between populations. By evaluating our simulation results, we concluded that a sample size of 25 was adequate for assessing these metrics using the Ovine array to genotype Rocky Mountain bighorn sheep herds. However, we conclude that a universal sample size rule may not be able to sufficiently address the complexities that impact genomic kinship and inbreeding estimates. Thus, we recommend that a pilot study and sample size simulation using R code we developed that includes empirical genotypes from a subset of populations of interest would be an effective approach to ensure rigour in estimating genomic kinship and population differentiation.
Article
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Meiotic recombination plays a critical evolutionary role in maintaining fitness in response to selective pressures due to changing environments. Variation in recombination rate has been observed amongst and between species and populations and within genomes across numerous taxa. Studies have demonstrated a link between changes in recombination rate and selection, but the extent to which fine scale recombination rate varies between evolved populations during the evolutionary period in response to selection is under active research. Here, we utilize a set of three temperature-evolved Drosophila melanogaster populations that were shown to have diverged in several phenotypes, including recombination rate, based on the temperature regime in which they evolved. Using whole genome sequencing data from these populations, we generated LD-based fine scale recombination maps for each population. With these maps, we compare recombination rates and patterns among the three populations and show that they have diverged at fine scales but are conserved at broader scales. We further demonstrate a correlation between recombination rates and genomic variation in the three populations. Lastly, we show variation in localized regions of enhanced recombination rates, termed warm-spots, between the populations with these warm-spots and associated genes overlapping areas previously shown to have diverged in the three populations due to selection. These data support the existence of recombination modifiers in these populations which are subject to selection during evolutionary change.
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Understanding the influence of population attributes on genetic diversity is important to advancement of biological conservation. Because bighorn sheep (Ovis canadensis) populations vary in size and management history, the species provides a unique opportunity to observe the response of average pairwise kinship, inversely related to genetic diversity, to a spectrum of natural and management influences. We estimated average pairwise kinship of bighorn sheep herds and compared estimates with population origin (native/indigenous/extant or reintroduced), historical minimum count, connectivity, and augmentation history, to determine which predictors were the most important. We evaluated 488 bighorn sheep from 19 wild populations with past minimum counts of 16–562 animals, including native and reintroduced populations that received 0–165 animals in augmentations. Using the Illumina High Density Ovine array, we generated a dataset of 7728 single nucleotide polymorphisms and calculated average pairwise kinship for each population. Multiple linear regression analysis determined that connectivity between populations via dispersal, greater number of animals received in augmentations, and greater minimum count were correlated with lower average pairwise kinship at the population level, and whether the population was extant or reintroduced was less important. Thus, our results indicated that genetic isolation of populations can result in increased levels of inbreeding. By determining that natural and human‐assisted gene flow were likely the most important influences of average pairwise kinship at the population level, this study can serve as a benchmark for future management of bighorn sheep populations and aid in identifying populations of genetic concern to define priorities for conservation of wild populations.
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