Evidence of early genomic selection in Holstein Friesian across African and European ecosystems

The Holstein Friesian (HF) cattle breed is the most dominant breed in commercial dairy farming worldwide and managed in more than 150 countries. These countries span diverse agro-climatic zones, ranging from tropical to cold regions. The introduction of HF animals in these regions occurred at different moments in the past which are poorly recorded and continued through importation of live animal and frozen semen. We hypothesize that the HF cattle populations in these regions underwent early forms of adaptation to these specific local environments. However, the detection of genetic variation associated with this adaptation remains poorly documented. This study investigates genetic relationship and potential early selection signatures in HF populations from three African countries (Egypt, South Africa, Uganda) and three European countries (Finland, Portugal, The Netherlands), considering five animals per country. Approximately 16.0 million single nucleotide polymorphisms (SNPs) were detected in the 30 HF animals and used for further analyses. Across all countries, we identified dispersed regions totaling 3.3 megabase of ecosystem-specific genomic regions (43 genes), indicative of early selection signatures based on fixation indices (F-statistic, Fst). Furthermore, comparing variants between tropical (Egypt and Uganda) and cold regions (Finland and The Netherlands) by Fst, nucleotide diversity (θπ ratio), and extended haplotype homozygosity (XP-EHH), we identified a total of 10 candidate regions, comprising 12 genes within a 0.57 megabase size. The regions were enriched with genes involved in signaling pathways associated directly or indirectly with adaptation, including the immune system (PGLYRP4,PGLYRP3, PAG1, CD48, SLAMF1, DYSF,and LOC615223), organ development and reproduction (LDB3, ADAMTSL4, TPRN, CCDC40, OR2AG1G, and OR8B3), thermogenic activation (TBC1D16), phospholipid metabolism (PLPPR4 and PITPNB), thermos-tolerance (ZNF423), and stimulus response (NCOA7, CYP2C85, and ARFGEF3). This study provides new insights into early forms of genetic plasticity of animals adapted to very diverse ecosystems. Our findings highlight candidate genes related to immune response, organ development, reproduction, metabolism, and thermo-tolerance, hypothesizing their role in facilitating adaptation to different environments.