The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis.
Livestock European diffusion followed different human migration waves from the Fertile Crescent. In sheep, at least two diffusion waves have shaped the current breeds' biodiversity generating a complex genetic pattern composed by either primitive or fine-wool selected breeds. Among primitive br...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2022-01-01
|
| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0275989 |
| _version_ | 1797978061923155968 |
|---|---|
| author | Gabriele Senczuk Marika Di Civita Luigina Rillo Alessandra Macciocchi Mariaconsiglia Occidente Giorgio Saralli Valentina D'Onofrio Tiziana Galli Christian Persichilli Claudio Di Giovannantonio Fabio Pilla Donato Matassino |
| author_facet | Gabriele Senczuk Marika Di Civita Luigina Rillo Alessandra Macciocchi Mariaconsiglia Occidente Giorgio Saralli Valentina D'Onofrio Tiziana Galli Christian Persichilli Claudio Di Giovannantonio Fabio Pilla Donato Matassino |
| author_sort | Gabriele Senczuk |
| collection | DOAJ |
| description | Livestock European diffusion followed different human migration waves from the Fertile Crescent. In sheep, at least two diffusion waves have shaped the current breeds' biodiversity generating a complex genetic pattern composed by either primitive or fine-wool selected breeds. Among primitive breeds, aside from sharing common ancestral genomic components, they also show several traits such as the policeraty, large horns in the ram, short tail, and a moulting fleece, considered as ancestral. Although most of the primitive breeds characterized by these traits are confined on the very edge of Northern Europe, several residual populations are also scattered in the Mediterranean region. In fact, although in Italy a large number of local breeds are already extinct, others are listed as critically endangered, and among these there is the Quadricorna breed which is a four-horned sheep characterized by several ancestral traits. In this context we genotyped 47 individuals belonging to the Quadricorna sheep breed, a relict and endangered breed, from Central and Southern Italy. In doing so we used the Illumina OvineSNP50K array in order to explore its genetic diversity and to compare it with other 33 primitive traits-related, Mediterranean and Middle-East breeds, with the specific aim to reconstruct its origin. After retaining 35,680 SNPs following data filtering, the overall genomic architecture has been explored by using genetic diversity indices, Principal Component Analysis (PCA) and admixture analysis, while the genetic relationships and migration events have been inferred using a neighbor-joining tree based on Reynolds' distances and by the maximum likelihood tree as implemented in treemix. Multiple convergent evidence from all our population genetics analyses, indicated that the two Quadricorna populations differ from all the other Italian breeds, while they resulted to be very close to the Middle Eastern and primitive European breeds. In addition, the genetic diversity indices highlighted values comparable with those of most of the other analyzed breeds, despite the two populations exhibit slightly different genetic indices suggesting different levels of genomic inbreeding and drift (FIS and FROH). The admixture analysis does not suggest any signal of recent gene exchange with other Italian local breeds, highlighting a rather ancestral purity of the two populations, while on the other hand the treemix analysis seems to suggest an ancient admixture with other primitive European breeds. Finally, all these evidences seem to trace back the residual Quadricorna sheep to an early Neolithic spread, probably following a Mediterranean route and that urgent conservation actions are needed in order to keep the breed and all related cultural products alive. |
| first_indexed | 2024-04-11T05:17:03Z |
| format | Article |
| id | doaj.art-268ed2f2d159413bb3b3408ded8cc75d |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-04-11T05:17:03Z |
| publishDate | 2022-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-268ed2f2d159413bb3b3408ded8cc75d2022-12-24T05:33:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-011710e027598910.1371/journal.pone.0275989The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis.Gabriele SenczukMarika Di CivitaLuigina RilloAlessandra MacciocchiMariaconsiglia OccidenteGiorgio SaralliValentina D'OnofrioTiziana GalliChristian PersichilliClaudio Di GiovannantonioFabio PillaDonato MatassinoLivestock European diffusion followed different human migration waves from the Fertile Crescent. In sheep, at least two diffusion waves have shaped the current breeds' biodiversity generating a complex genetic pattern composed by either primitive or fine-wool selected breeds. Among primitive breeds, aside from sharing common ancestral genomic components, they also show several traits such as the policeraty, large horns in the ram, short tail, and a moulting fleece, considered as ancestral. Although most of the primitive breeds characterized by these traits are confined on the very edge of Northern Europe, several residual populations are also scattered in the Mediterranean region. In fact, although in Italy a large number of local breeds are already extinct, others are listed as critically endangered, and among these there is the Quadricorna breed which is a four-horned sheep characterized by several ancestral traits. In this context we genotyped 47 individuals belonging to the Quadricorna sheep breed, a relict and endangered breed, from Central and Southern Italy. In doing so we used the Illumina OvineSNP50K array in order to explore its genetic diversity and to compare it with other 33 primitive traits-related, Mediterranean and Middle-East breeds, with the specific aim to reconstruct its origin. After retaining 35,680 SNPs following data filtering, the overall genomic architecture has been explored by using genetic diversity indices, Principal Component Analysis (PCA) and admixture analysis, while the genetic relationships and migration events have been inferred using a neighbor-joining tree based on Reynolds' distances and by the maximum likelihood tree as implemented in treemix. Multiple convergent evidence from all our population genetics analyses, indicated that the two Quadricorna populations differ from all the other Italian breeds, while they resulted to be very close to the Middle Eastern and primitive European breeds. In addition, the genetic diversity indices highlighted values comparable with those of most of the other analyzed breeds, despite the two populations exhibit slightly different genetic indices suggesting different levels of genomic inbreeding and drift (FIS and FROH). The admixture analysis does not suggest any signal of recent gene exchange with other Italian local breeds, highlighting a rather ancestral purity of the two populations, while on the other hand the treemix analysis seems to suggest an ancient admixture with other primitive European breeds. Finally, all these evidences seem to trace back the residual Quadricorna sheep to an early Neolithic spread, probably following a Mediterranean route and that urgent conservation actions are needed in order to keep the breed and all related cultural products alive.https://doi.org/10.1371/journal.pone.0275989 |
| spellingShingle | Gabriele Senczuk Marika Di Civita Luigina Rillo Alessandra Macciocchi Mariaconsiglia Occidente Giorgio Saralli Valentina D'Onofrio Tiziana Galli Christian Persichilli Claudio Di Giovannantonio Fabio Pilla Donato Matassino The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis. PLoS ONE |
| title | The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis. |
| title_full | The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis. |
| title_fullStr | The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis. |
| title_full_unstemmed | The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis. |
| title_short | The ancestral origin of the critically endangered Quadricorna sheep as revealed by genome-wide analysis. |
| title_sort | ancestral origin of the critically endangered quadricorna sheep as revealed by genome wide analysis |
| url | https://doi.org/10.1371/journal.pone.0275989 |
| work_keys_str_mv | AT gabrielesenczuk theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT marikadicivita theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT luiginarillo theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT alessandramacciocchi theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT mariaconsigliaoccidente theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT giorgiosaralli theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT valentinadonofrio theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT tizianagalli theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT christianpersichilli theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT claudiodigiovannantonio theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT fabiopilla theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT donatomatassino theancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT gabrielesenczuk ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT marikadicivita ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT luiginarillo ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT alessandramacciocchi ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT mariaconsigliaoccidente ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT giorgiosaralli ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT valentinadonofrio ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT tizianagalli ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT christianpersichilli ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT claudiodigiovannantonio ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT fabiopilla ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis AT donatomatassino ancestraloriginofthecriticallyendangeredquadricornasheepasrevealedbygenomewideanalysis |