Molecular evolution and signatures of selective pressures on Bos, focusing on the Nelore breed (Bos indicus)

PLOS ONE RESEARCH ARTICLE Molecular evolution and signatures of selective pressures on Bos, focusing on the Nelore breed (Bos indicus) Thainá Cortez ID1*, Horácio Montenegro ID2, Luiz L. Coutinho2, Luciana C. A. Regitano3, Sónia C. S. Andrade ID1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Cortez T, Montenegro H, Coutinho LL, Regitano LCA, Andrade SCS (2022) Molecular evolution and signatures of selective pressures on Bos, focusing on the Nelore breed (Bos indicus). PLoS ONE 17(12): e0279091. https://doi.org/ 10.1371/journal.pone.0279091 Editor: Martina Zappaterra, University of Bologna, ITALY Received: February 22, 2022 Accepted: November 30, 2022 Published: December 22, 2022 Copyright: © 2022 Cortez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The raw reads from the 43 bulls used in this study are publicly available in the European Nucleotide Archive (ENA) repository (EMBL-EBI), under accession PRJEB13188. Funding: This study was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo, FAPESP (Process number 2012/23638-8, 2015/ 20139-9 and 2017/05625-0). The funders had no role in study design, data collection and analysis, 1 Departamento de Genética e Biologia Evolutiva, Universidade de São Paulo (USP), São Paulo, SP, Brazil, 2 Departamento de Zootecnia, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (ESALQ), Piracicaba, SP, Brazil, 3 Empresa Brasileira de Pesquisa Agropecuária, Embrapa Pecuária Sudeste, São Carlos, SP, Brazil * (SCSA); (TC) Abstract Evolutionary history leads to genome changes over time, especially for species that have experienced intense selective pressures over a short period. Here, we investigated the genomic evolution of Bos species by searching for potential selection signatures, focusing on Nelore, an economically relevant cattle breed in Brazil. We assessed the genomic processes determining the molecular evolution across Nelore and thirteen other related taxa by evaluating (i) amino acid sequence conservation, (ii) the dN/dS ratio, and (iii) gene families’ turnover rate (λ). Low conserved regions potentially associated with fatty acid metabolism seem to reflect differences in meat fat content in taxa with different evolutionary histories. All Bos species presented genes under positive selection, especially B. indicus and Nelore, which include transport protein cobalamin, glycolipid metabolism, and hormone signaling. These findings could be explained by constant selective pressures to obtain higher immune resistance and efficient metabolism. The gene contraction rate across the Nelore + B. indicus branch was almost nine times higher than that in other lineages (λ = 0.01043 vs. 0.00121), indicating gene losses during the domestication process. Amino acid biosynthesis, reproductive and innate immune system-related pathways were associated with genes recognized within the most frequent rapidly evolving gene families and in genes under positive selection, supporting the substantial relevance of such traits from a domestication perspective. Our data provide new insights into how the genome may respond to intense artificial selection in distinct taxa, and reinforces the presence of selective pressures on traits potentially relevant for future animal breeding investments. Introduction Domesticated species, such as sheep, horses, pigs, goats, and cattle, have been subjected to long periods of intense phenotypic selection that have resulted in dramatic genomic changes in a few generations [1]. Modern cattle, the most important domesticated group, with more than PLOS ONE | https://doi.org/10.1371/journal.pone.0279091 December 22, 2022 1 / 19 PLOS ONE decision to publish, or preparation of the manuscript." Competing interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Bos genus genomic evolution 900 million heads across the globe, can be grouped into humpless taurines (Bos taurus) and humped zebuines (Bos indicus). These species differ in many morphological and physiological aspects, but most commonly by the prominent hump and long face in the zebu. In Brazil, the humped cattle Nelore constitutes the largest part of the commercial herd, mainly because of its advantages in tropical environments, such as greater thermal tolerance, lower metabolic rate and nutrient requirement, natural resistance to ectoparasites, and higher fertility [2–4]. Previous studies [5, 6] indicated that zebu and taurine cattle lineages share the ancestor aurochs, Bos primigenius, and that the humped cattle evolution presents multiple domestication historical scenarios, where the African lineage not only seem to contain the oldest zebu lineage, but also exhibit a very particular evolutionary narrative [7]. Domestication includes artificial selection, but also the relaxation of selection pressures on several other predictors (e.g., hunting, predation, and starvation). The effects of selective breeding on economically relevant traits have been investigated by identifying footprints across the entire genomic architecture, such as high allele frequencies, increased amino acid change rates, and low genetic diversity [1, 8]. In this context, Somavilla et al. [9] studied selection signatures in Nelore cattle, which revealed several regions related to reproduction, growth, meat quality, and fatty acid content under recent selection. Evolutionary approaches have demonstrated high efficacy for the study of genomic signatures resulting from domestication, especially because recently developed methods have progressively improved accuracy. Phylogenetic analysis of homologous sequences, for example, evaluates the amount of divergence between two or more species by quantifying the substitution rate [e.g., 10–13]. Gene family’s evolution rate, based on the size of gene copies, allows us to not only infer the probability of the observed changes resulting from natural selection, but also to identify genomic changes into expansion and/or contraction rates [14–16]. Although rapid gene family expansion may indicate positive selection, the pressures underlying gene family contraction/loss are less clear and could be produced by both neutral and adaptive regimes. Despite being a useful tool to complement and benefit evolutionary studies, gene family evolution investigations remain understudied when compared to the analysis of homologous sequences [17]. In the present study, we aimed to evaluate the evolutionary history and potential signatures of selection in Nelore (B. indicus) genomic regions, as well as in four other Bos species, including B. taurus. (...truncated)