- Research Article
- Open Access
Patterns of homozygosity in insular and continental goat breeds
- Taina F. Cardoso†1, 2,
- Marcel Amills†1, 3Email authorView ORCID ID profile,
- Francesca Bertolini4,
- Max Rothschild4,
- Gabriele Marras5,
- Geert Boink6,
- Jordi Jordana3,
- Juan Capote7,
- Sean Carolan8,
- Jón H. Hallsson9,
- Juha Kantanen10,
- Agueda Pons11,
- Johannes A. Lenstra12Email author and
- The AdaptMap Consortium
© The Author(s) 2018
- Received: 22 November 2017
- Accepted: 15 October 2018
- Published: 19 November 2018
Genetic isolation of breeds may result in a significant loss of diversity and have consequences on health and performance. In this study, we examined the effect of geographic isolation on caprine genetic diversity patterns by genotyping 480 individuals from 25 European and African breeds with the Goat SNP50 BeadChip and comparing patterns of homozygosity of insular and nearby continental breeds.
Among the breeds analysed, number and total length of ROH varied considerably and depending on breeds, ROH could cover a substantial fraction of the genome (up to 1.6 Gb in Icelandic goats). When compared with their continental counterparts, goats from Iceland, Madagascar, La Palma and Ireland (Bilberry and Arran) displayed a significant increase in ROH coverage, ROH number and FROH values (P value < 0.05). Goats from Mediterranean islands represent a more complex case because certain populations displayed a significantly increased level of homozygosity (e.g. Girgentana) and others did not (e.g. Corse and Sarda). Correlations of number and total length of ROH for insular goat populations with the distance between islands and the nearest continental locations revealed an effect of extremely long distances on the patterns of homozygosity.
These results indicate that the effects of insularization on the patterns of homozygosity are variable. Goats raised in Madagascar, Iceland, Ireland (Bilberry and Arran) and La Palma, show high levels of homozygosity, whereas those bred in Mediterranean islands display patterns of homozygosity that are similar to those found in continental populations. These results indicate that the diversity of insular goat populations is modulated by multiple factors such as geographic distribution, population size, demographic history, trading and breed management.
The advent of next-generation sequencing and high throughput genotyping techniques has made it possible to identify, in the genomes of multiple species, continuous homozygous stretches of sequence, which are named runs of homozygosity (ROH) . The genomic distribution, abundance, and length of ROH are modulated by multiple factors including local recombination rate, guanine-cytosine content, positive selection and demography [2, 3]. A high frequency of long ROH is often caused by recent inbreeding, whereas a high frequency of short ROH can be explained by the occurrence of an ancient founder effect or population bottleneck. After the first pioneering study of Ferenčaković et al. , the patterns of ROH have been characterized for multiple domestic species and breeds with the goal of making inferences about their history and demography as well as of identifying the genomic footprint of natural and artificial selection .
Geographic isolation of populations may lead to a considerable loss of diversity, an increase in inbreeding and vulnerability to stochastic events . For instance, human populations with a history of prolonged isolation on the Orkney or Dalmatian Islands or in Sardinia have longer ROH than continental populations, which indicates an elevated relatedness [7, 8]. A high frequency of ROH can have detrimental effects on biological fitness and reproductive success because ROH are often enriched in deleterious mutations . Indeed, mitochondrial encephalomyopathy is relatively frequent in people from the Faroe Islands due to homozygosity of the SUCLA2 gene . In cattle, Zhang et al.  reported that deleterious variations are overrepresented in ROH regions, particularly in those longer than 3 Mbp. However, geographically isolated populations may have retained ancient alleles or variants that are not found in other populations [12, 13], which reflects adaptation to harsh environments and/or a practice of breed management that are not common for mainland populations [13–15].
Recently, genome-wide single nucleotide polymorphism (SNP) data for a comprehensive panel of goats breeds has become available . For the same panel of breeds, signatures of selection  and the effects of population size, breed management and crossbreeding on the patterns of ROH as well as chromosomal ROH hotspots have been reported . The aim of our study was to investigate if goat breeds that are raised in islands have higher levels of homozygosity than their continental counterparts. In order to achieve this goal, we compared the number and genomic coverage of ROH in 25 caprine breeds from 16 European and African islands with those of nine continental populations.
Goat sampling and genotyping
ROH number, ROH length and FROH mean, minimum (min) and maximum (max) values calculated for the 25 goat populations used in this study (SE = standard error)
Number of animals
Mean ± SE
Mean ± SE
Mean ± SE
478.44 ± 19.43
259.67 ± 7.88
0.19 ± 0.01
47.01 ± 9.21
21.79 ± 1.15
0.02 ± 0.00
733.63 ± 47.82
178.00 ± 7.05
0.30 ± 0.02
135.05 ± 30.77
35.61 ± 4.40
0.05 ± 0.01
533.28 ± 44.00
67.00 ± 5.33
0.22 ± 0.02
155.39 ± 29.90
30.63 ± 4.12
0.06 ± 0.01
93.72 ± 14.29
34.86 ± 1.68
0.04 ± 0.01
636.87 ± 60.53
265.79 ± 4.88
0.26 ± 0.02
401.18 ± 28.00
67.06 ± 1.94
0.16 ± 0.01
622.60 ± 15.80
125.27 ± 1.96
0.25 ± 0.01
225.46 ± 32.00
80.75 ± 2.77
0.09 ± 0.01
218.30 ± 42.49
47.46 ± 3.69
0.09 ± 0.02
363.58 ± 37.61
93.71 ± 2.60
0.15 ± 0.02
1625.59 ± 57.30
366.45 ± 12.60
0.66 ± 0.02
334.68 ± 63.06
74.39 ± 4.61
0.14 ± 0.03
797.36 ± 21.95
392.63 ± 4.70
0.32 ± 0.01
287.56 ± 36.34
73.42 ± 6.71
0.12 ± 0.01
151.03 ± 40.45
32.43 ± 2.94
0.06 ± 0.02
146.35 ± 14.97
84.55 ± 1.37
0.06 ± 0.01
323.02 ± 33.76
74.50 ± 5.42
0.13 ± 0.01
Spain (La Palma)
571.80 ± 14.11
276.13 ± 4.86
0.23 ± 0.01
Blanca de Rasquera
246.55 ± 37.98
56.45 ± 5.33
0.10 ± 0.02
97.19 ± 17.14
34.81 ± 2.35
0.04 ± 0.01
854.77 ± 30.68
363.95 ± 4.65
0.35 ± 0.01
564.73 ± 16.40
300.63 ± 7.40
0.23 ± 0.01
The Zanardi software  was used to identify ROH. Runs of homozygosity were defined as homozygous genomic stretches that are at least 1 Mb long and that contain a minimum number of 15 SNPs. We allowed one heterozygous SNP per ROH to account for genotyping errors. Coordinates of principal component analysis (PCA) and allele-sharing distances (ASD) were calculated with the PLINK program . A neighbor-joining tree was built and visualized with the Splitstree program .
Genomic inbreeding derived from ROH coverage (FROH) was calculated by dividing total ROH length per individual by total genome length across all 29 autosomes (2456.50 Mb). Inbreeding coefficients i.e. Fhet, Fhat1, Fhat2, and Fhat3 were calculated with the PLINK software  for populations with at least 20 individuals. On the one hand, the—het command of PLINK  was used to compute observed and expected autosomal homozygous genotype counts (Fhet) and on the other hand, we used the—ibc command of PLINK  to calculate Fhat, Fhat2 and Fhat3 parameters. Observed heterozygosity (Ho) and effective size (Ne) parameters were retrieved from estimates provided by Colli and coworkers .
Statistical analyses were performed by using the R software v.2.15.3 . The values and statistical significances of Spearman’s rank correlations (ρ) of FROH with Ho and Ne were computed. We also calculated Spearman’s rank correlations (ρ) of number and total length of ROH for insular goat populations with the distance between each island and the nearest continental location.
A neighbor-joining tree of ASD distances (Fig. 1b) shows a clear clustering of goats from the same breed, except for two Maltese Sarda goats that cluster with the Sarda and vice versa. Girgentana, Palmera and Sofia are nested within the Aspromontana, Morocco and Diana populations, respectively, while both Menabe and Sud-Ouest populations are within the Androy population. Most breeds appear to be homogeneous, except for Danish Landrace, Mallorquina and Aspromontana, which show some heterogeneity. For Icelandic, Irish, Palmera and Malagasy goats, we observed a decrease in genetic distances between individuals from the same breed (Fig. 1b) but not for goats from Mediterranean islands. Apart from the extremely inbred Icelandic goats , genetic isolation was most intense for the Irish Arran, Dutch, Palmeran (Canary Islands) and Malagasy (Androy, Sofia, Diana, Menabe and Sud-Ouest) populations. As shown in Figure S3 (see Additional file 3: Figure S3), the within-breed ASD distances correlate closely with Ho, which indicates that a tree as that shown in Fig. 1b faithfully illustrates the diversity patterns and at the same time reproduces the regional clustering of breeds .
We also calculated Spearman correlations coefficients of ROH length and number with the distance of insular goat populations to the nearest continental coastal site. For goats raised in distant islands, such as Iceland (1277 km from Norway) or Madagascar (1051 km from Mozambique), ROH number and total length had the largest values. Spearman correlation coefficients of the distances with ROH number (ρ = 0.54 and, P value = 0.023) and total length (ρ = 0.63 and, P value = 0.007) were positive and significant.
In insular and other isolated populations, homozygosity is often increased by founder effects and geographic isolation. In our study, the larger numbers and longer total lengths of ROH and higher FROH in goats from Iceland, Ireland, La Palma and Madagascar than in their continental counterparts illustrate this increase in the level of homozygosity (Table 1 and Figs. 2, 3 and 4). In contrast, Mediterranean insular and continental populations form a tight cluster. Although goat populations that are raised in remote islands tend to have higher levels of homozygosity, other factors are also involved, such as breed management, history and demography, which could have strong effects on breed diversity. We were not able to analyse the impact of some of these factors because of lack of information (historic and demographic records are scarce or completely absent for most of the breeds under analysis).
The analysis illustrated in Fig. 1a reveals a strong separation between Malagasy and Matebele (Zimbabwe) and between Icelandic and Nordic Landrace goat populations and, to a lesser extent, between Palmeran and Moroccan goats. This result probably reflects the extreme geographic isolation of these three insular populations. Indeed, we found that ROH number and total length were correlated positively with distance between each island and the nearest continental location. Effects of insularization and/or small effective populations sizes were previously reported in a comparison between Japanese wild boars and Asian mainland pigs , and for several insular and/or inbred cattle populations .
We observed the most extreme combined effects of founder events, geographic isolation and small population size for the Icelandic goats with 324 to 455 ROH that cover between 1263 and 1979 Mb, a high frequency of very long ROH (> 30 Mb) and a very high FROH of 0.66 (Table 1 and Figs. 3, 4, 5). Icelandic goats have a North-European (most likely Norwegian) origin and were imported during the colonization of Iceland over 1100 years ago [12, 29]. The lack of evidence for subsequent goat importations suggests a scenario of strong geographic isolation. Moreover, there were less than 100 Icelandic goats at the end of the nineteenth century and again in 1960, but, in 1994, the estimated census was equal to 348 heads distributed over 48 flocks . Small population size combined with a fragmented distribution probably favoured the maintenance of high levels of inbreeding in this goat population. Old Irish goats, most notably those from Arran and Bilberry, also show increased ROH coverage, but not as extreme as that observed in Icelandic goats (Figs. 3, 4, 5). The extremely small population (27 in 2006, ) of Bilberry goats has led to the emergence of relatively long ROH (Figs. 3, 5), which indicates recent consanguinity. Old Irish goats have been subjected to casual hunting and indiscriminate culling of feral herds, which has led this population to the verge of extinction .
Increased homozygosity was also observed in goat populations that have large population sizes but, as for the Icelandic and Irish goats, have endured a prolonged geographic isolation. For both Palmera and Malagasy goats, a relatively large number of ROH, high ROH coverage (Fig. 2) and elevated FROH (0.19–0.35, Table 1) were found, but short ROH (1–5 Mb) were predominant (Fig. 5). This is probably the consequence of an ancient founder effect and geographic isolation, whereas their large population size (1.2 million in Madagascar and more than 6000 in La Palma) prevents consanguinity and the generation of long ROH. Madagascar, the fourth largest island in the world, was settled by Austronesians, who arrived from Borneo during the fifth to seventh centuries, and subsequently by Bantu people , but it is clear that Malagasy goats are of African origin (Fig. 1). The patterns of ROH observed in our study suggest that, after an initial founder effect, Malagasy goats were subject to a history of prolonged geographic isolation, with the distance of 1000 km between Madagascar and the African landmass constituting an effective barrier to gene flow. La Palma, in the Canarian archipelago, was settled 2500 YBP by colonists with probably a Berber ancestry and remained isolated from the main maritime routes until its colonization by the Spanish in the fifteenth century . This North African ancestry of Palmeran goats is reflected in the neighbor-joining tree shown in Fig. 1, with Palmeran goats displaying a close relationship with Moroccan goats. In the La Palma island, a limited number of founders in combination with geographic isolation resulted in a low level of diversity of caprine mtDNA  and a high ROH coverage.
The above results are in strong contrast with the majority of the Mediterranean insular goat breeds showing ROH patterns and FROH values that are similar to those observed in nearby continental populations (Table 1 and Figs. 2, 3, 4, 5). Mallorca, Corsica, Sicily and Sardinia are relatively close (5–300 km) to continental Europe and are located along maritime routes that were used intensively by the Phoenicians, Carthaginians, Greeks, Romans, Arabs and many other seafaring civilizations . This situation probably favoured the recurrent admixture of goat populations with different genetic backgrounds, thus counteracting the decrease in genetic variation produced by the initial founder effect. This is also illustrated by the segregation of the mtDNA G haplogroup in Mallorquina goats, which so far has only been identified in goats from Egypt, Iran and Turkey . Furthermore, a mixed ancestry with a major influence of Maltese goats has been mentioned for Sarda goat . However, Mallorquina and Girgentana goats are exceptions with a high frequency of long ROH (> 30 Mb, Fig. 5) and FROH values of 0.14 and 0.15, respectively. The highly endangered Mallorquina goats have suffered strong population bottlenecks (current census = 150 individuals) . The Girgentana breed has also experienced a strong demographic recession from 30,000 individuals in 1983 to 461 in 1993 . Thus, for both these breeds, long ROH (> 30 Mb) are explained by population bottlenecks and recent inbreeding.
As illustrated by the Finnish, Danish and Dutch Landrace breeds, genetic isolation may also occur in continental populations that are raised in remote locations from Finland and Denmark or subject to a strict breeding management and selection in combination with the occurrence of founder effects (Netherlands). The Dutch goat population has been revived since 1958: it started with two remaining individuals, involved undocumented crossbreeding and resulted in the current population of ca. 2000 animals . Genetic distances show a relatedness to the Danish and Finnish Landrace populations, which was not detected by a panel of 26 microsatellites . Remarkably, the numbers and length distributions of ROH for these populations are similar to those reported for British cattle breeds Angus, Hereford, Jersey and Guernsey , and larger than those reported for central European continental goats (this study) or European continental cattle .
A common finding in several studies of ROH [14, 28, 38] is the considerable variation in patterns of ROH within breeds. We observed this also in our dataset, in spite of the high level of within-breed homogeneity (Fig. 1b). The genomic coverage of ROH—up to 1.6 Gb in the Iceland breed and less than 100 Mb only for three breeds—indicates that a substantial part of the genes are homozygous, which may have detrimental consequences on the biological viability of isolated populations due to inbreeding depression and increased frequency of recessive hereditary diseases [1, 9, 11]. However, small population sizes promote the loss of recessive gene defects. Thus, future work should investigate the consequences of high ROH coverage based on whole-genome sequence data.
Our data show that insularization generally involves increased levels of homozygosity. At the same time, patterns of ROH are highly divergent among insular (and also continental) goat breeds: whereas goats that are raised in Madagascar, Iceland and La Palma, show high levels of homozygosity, those bred in Mediterranean islands display homozygosity patterns that are comparable to those found in continental populations. These results indicate that the effects of isolation are modulated by a complex network of factors including population size, breed history and demography, geographic distribution, trading and breed management, which either maintain strict isolation or allow cross-breeding.
AdaptMap Consortium, JAL and MA designed the experiment. AdaptMap Consortium, GB, JC, JJ, SC, JHH, JK and AP performed breed sampling. All members of the AdaptMap Consortium were involved in the genotyping of goats. TFC, FB, MR and GM performed the analyses of runs of homozygosity and JAL the phylogenetic analyses. MA and JAL wrote the manuscript. All authors helped to draft and revise the manuscript. All authors read and approved the final manuscript.
We are indebted to all the people involved in the collection of goat samples. We thank Laura Zingaretti for her assistance with statistical analysis.
The authors declare that they have no competing interests.
Availability of supporting data
Genotyping data obtained in the current work are deposited in Figshare: https://doi.org/10.6084/m9.figshare.7272854.v1.
Consent for publication
Sampling was performed by trained veterinarians following standard procedures and relevant national guidelines to ensure appropriate animal care.
We acknowledge financial support from the Spanish Ministry of Economy and Competitiveness (Project AGL2016-76108-R), the “Severo Ochoa Programme for Centres of Excellence in R&D” 2016-2019 (SEV-2015-0533), the CERCA Programme/Generalitat de Catalunya and the Dutch Stichting Zeldzame Huisdierrassen. Funding for FB and MR were provided by the Ensminger endowment, Hatch and State of Iowa funds. Tainã F Cardoso was funded with a fellowship from the CAPES Foundation-Coordination of Improvement of Higher Education, Ministry of Education (MEC) of the Federal Government of Brazil.
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