Genome-Wide Analysis Reveals Selection Signatures Involved in Meat Traits and Local Adaptation in Semi-Feral Maremmana Cattle.

Slim Ben-Jemaa,Elena Ciani,Baldassare Portolano,Gabriele Senczuk,Gennaro Catillo,Mekki Boussaha,Salvatore Mastrangelo,Roberta Ciampolini,Fabio Pilla

doi:10.3389/fgene.2021.675569

Abstract

The Maremmana cattle is an ancient Podolian-derived Italian breed raised in semi-wild conditions with distinctive morphological and adaptive traits. The aim of this study was to detect potential selection signatures in Maremmana using medium-density single nucleotide polymorphism array. Putative selection signatures were investigated combining three statistical approaches designed to quantify the excess of haplotype homozygosity either within (integrated haplotype score, iHS) or among pairs of populations (Rsb and XP-EHH), and contrasting the Maremmana with a single reference population composed of a pool of seven Podolian-derived Italian breeds. Overall, the three haplotype-based analyses revealed selection signatures distributed over 19 genomic regions. Of these, six relevant candidate regions were identified by at least two approaches. We found genomic signatures of selective sweeps spanning genes related to mitochondrial function, muscle development, growth, and meat traits (SCIN, THSD7A, ETV1, UCHL1, and MYOD1), which reflects the different breeding schemes between Maremmana (semi-wild conditions) and the other Podolian-derived Italian breeds (semi-extensive). We also identified several genes linked to Maremmana adaptation to the environment of the western-central part of Italy, known to be hyperendemic for malaria and other tick-borne diseases. These include several chemokine (C-C motif) ligand genes crucially involved in both innate and adaptive immune responses to intracellular parasite infections and other genes playing key roles in pulmonary disease (HEATR9, MMP28, and ASIC2) or strongly associated with malaria resistance/susceptibility (AP2B1). Our results provide a glimpse into diverse selection signatures in Maremmana cattle and can be used to enhance our understanding of the genomic basis of environmental adaptation in cattle.

Highlights

In livestock species, domestication followed by breed formation and the subsequent artificial selection for economic and morphological traits have shaped genomic variation, driving the formation of detectable signatures on the genome of these populations (e.g., Stella et al, 2010; Qanbari et al, 2011; Rothammer et al, 2013; Signer-Hasler et al, 2017; Mastrangelo et al, 2020a)
The present study aimed at the detection of genomic regions that had been differentially selected between Maremmana and other Podolian-derived Italian breeds, which can provide clues to potential new targets of natural and artificial selection
In addition to the aforementioned genes in the selection signature on BTA04 (ETV1, SCIN, and THSD7A), we identified other candidate genes involved in several biological processes (BP) related to muscle compartments, and many of them were previously shown to be associated with meat quality traits

Summary

Introduction

Domestication followed by breed formation and the subsequent artificial selection for economic and morphological traits have shaped genomic variation, driving the formation of detectable signatures on the genome of these populations (e.g., Stella et al, 2010; Qanbari et al, 2011; Rothammer et al, 2013; Signer-Hasler et al, 2017; Mastrangelo et al, 2020a). Several Italian breeds such as Marchigiana, Romagnola, Chianina, Calvana, Podolica, Cinisara, Modicana, and Maremmana belong to the so-called “Podolian” group (hereinafter referred to as “Podolian-derived Italian breeds”; Mastrangelo et al, 2020b) This group includes several European breeds with common phenotypic traits such as a gray coat color and long horns (Di Lorenzo et al, 2018) considered to be ancestral. The Maremmana is an ancient cattle breed that, unlike the other Podolian-derived Italian breeds, is raised in semi-feral conditions (Figure 1), whose origin can be traced back to the Etruscan era when local would have been crossed with Podolian cattle (Maretto et al, 2012) This breed has been reared for hundreds of years in the lowlands and on the hilly areas of Maremma, a territory bordering the Tyrrhenian Sea and including much of south-western Tuscany and part of northern Lazio, in western central Italy. About 11,800 animals are recorded in the herdbook in 2019, including 6,853 cows and 213 bulls reared in 250 herds for beef production.

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