The genomic comparison between autochthonous and cosmopolitan cows reveals structural variants involved in environmental adaptation

Abstract

Copy Number Variants (CNVs) are structural variants affecting genetic diversity and phenotypic variability of populations. Different authors underlined the relevance of CNV in relation to the adaptation to environmental conditions (e.g., altitude, harsh farming environment). Aosta cattle (Aosta Red Pied - ARP; Aosta Black Pied/Chestnut - ABC and Mixed Chestnut-Héren - ACH) farmed in the Aosta Valley, and the Oropa Red Pied (ORO), farmed in the Piedmont region, are autochthonous dual-purpose breeds well adapted to the natural Alpine environment. In contrast, the Holstein (HOL) breed is a specialized dairy breed raised in intensive farming systems, representing an artificial environment. The aim of this study is to use CNVs to characterize these breeds and explore the relationship between structural genomic variability and adaptation to mountain farming systems (natural environment) vs. intensive farming systems (artificial environment). Using the GeneSeek Genomic Profiler Bovine 100K data, a total of 160,798 CNVs were identified across 5,610 individuals. Principal Component Analysis (PCA) using CNV Regions (CNVRs) revealed that Aosta breeds clustered into two separate groups, with one smaller cluster including part of ORO cows, while the Holstein formed a distinct cluster. These results suggest that CNVs may act as markers of adaptive selection, influencing both Aosta and ORO breeds, though to a different extent compared to the intensively farmed HOL breed. A total of 526 CNVRs were identified in at least 2% of the samples. Annotated genes and overlapping QTL were functionally associated with production, functional traits, and health-related characteristics. V_ST analysis revealed candidate genes linked to environmental adaptation, reproduction, and metabolic efficiency in Aosta, ORO, and HOL cattle. Key findings include TCF12 and SRGAP1 deletions in Aosta, suggesting trade-offs between muscle growth and endurance, while ELF2 and ARID5B gains in Holstein indicate aptitude for milk protein synthesis and feed efficiency. Additionally, reproductive genes (RGS3, GSE1, MARCH10) showed distinct selection pressures between Dual-purpose and Holstein breeds, reflecting adaptation to different production systems.

Keywords: Aosta breed; Copy number variant (CNV); Dual-purpose breed; Environmental adaptation; Holstein.

Fig. 1

Relationship between count and total length (bp) of CNVs identified in each sample according to state (gain vs. loss).

Fig. 2

Physical distribution of copy number variant regions (CNVRs) identified in each breed (present in at least 2% of samples), categorized by state (gain, loss, and complex), with corresponding average frequencies provided.

Fig. 3

CNVRs diversity among breeds. Venn Diagram built using CNVRs of all the 4 breeds (identified in at least 2% of cows) (A); PCA results obtained using CNVRs of all the 4 breeds (B).

Fig. 4

Venn Diagram of number of genes annotated within the Aosta and dual-purpose common CNVRs and the ones shared with HOL breeds (A). Number of QTL terms –Type Trait and proportion of QTL terms –Trait Class already associated with genes annotated in the same CNVRs (according with the CattleQTLdb: https://www.animalgenome.org/cgi-bin/QTLdb/BT/index) (B).

Fig. 5

Genome wide V_ST value plots obtained for the following combinations: (A) Aosta (ARP + ABCH) vs. HOL; (B) Aosta (ARP + ABCH) vs. ORO; (C) Dual-purpose (ARP + ABCH + ORO) vs. HOL. Thresholds set to top 5% V_ST values.