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Identification of Candidate Genes for Reactivity in Guzerat (Bos Indicus) Cattle: a Genome-Wide Association Study

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Identification of Candidate Genes for Reactivity in Guzerat (Bos Indicus) Cattle: a Genome-Wide Association Study RESEARCH ARTICLE Identification of Candidate Genes for Reactivity in Guzerat (Bos indicus) Cattle: A Genome-Wide Association Study Fernanda Caroline dos Santos1☯, Maria Gabriela Campolina Diniz Peixoto2☯, Pablo Augusto de Souza Fonseca1, Maria de FaÂtima A vila Pires2, Ricardo Vieira Ventura3,4, Izinara da Cruz. Rosse1, Frank Angelo Tomita Bruneli2, Marco Antonio Machado2, Maria Raquel Santos Carvalho1* a1111111111 1 Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil, 2 Embrapa Gado de Leite, Juiz de Fora, Brazil, 3 Center for Genetic Improvement of Livestock, University of a1111111111 Guelph, Guelph, Canada, 4 Beef Improvement Opportunities, Guelph, Canada a1111111111 a1111111111 ☯ These authors contributed equally to this work. a1111111111 * [email protected] Abstract OPEN ACCESS Temperament is fundamental to animal production due to its direct influence on the animal- Citation: dos Santos FC, Peixoto MGCD, Fonseca herdsman relationship. When compared to calm animals, the aggressive, anxious or fearful  PAdS, Pires MdFA, Ventura RV, Rosse IdC., et al. ones exhibit less weight gain, lower reproductive efficiency, decreased milk production and (2017) Identification of Candidate Genes for Reactivity in Guzerat (Bos indicus) Cattle: A higher herd maintenance costs, all of which contribute to reduced profits. However, temper- Genome-Wide Association Study. PLoS ONE 12 ament is a trait that is complex and difficult to assess. Recently, a new quantitative system, (1): e0169163. doi:10.1371/journal.pone.0169163 REATEST®, for assessing reactivity, a phenotype of temperament, was developed. Herein, Editor: Roberta Davoli, Universita degli Studi di we describe the results of a Genome-wide association study for reactivity, assessed using Bologna, ITALY REATEST® with a sample of 754 females from five dual-purpose (milk and meat production) Received: July 14, 2016 Guzerat (Bos indicus) herds. Genotyping was performed using a 50k SNP chip and a two- Accepted: December 13, 2016 step mixed model approach (Grammar-Gamma) with a one-by-one marker regression was used to identify QTLs. QTLs for reactivity were identified on chromosomes BTA1, BTA5, Published: January 26, 2017 BTA14, and BTA25. Five intronic and two intergenic markers were significantly associated Copyright: © 2017 dos Santos et al. This is an open with reactivity. POU1F1, DRD3, VWA3A, ZBTB20, EPHA6, SNRPF and NTN4 were identi- access article distributed under the terms of the Creative Commons Attribution License, which fied as candidate genes. Previous QTL reports for temperament traits, covering areas sur- permits unrestricted use, distribution, and rounding the SNPs/genes identified here, further corroborate these associations. The seven reproduction in any medium, provided the original genes identified in the present study explain 20.5% of reactivity variance and give a better author and source are credited. understanding of temperament biology. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This study was supported by FundacËão de Amparo à Pesquisa de Minas Gerais (FAPEMIG), Conselho Nacional de Introduction Desenvolvimento CientõÂfico e TecnoloÂgico (CNPq), Temperament is a complex trait comprising many phenotypes including curiosity, explora- CoordenacËão de AperfeicËoamento de Pessoal de NõÂvel Superior (CAPES) and Empresa Brasileira de tion, aggressiveness, reactivity, passivity, physical movements, persistent habits, emotions, Pesquisa AgropecuaÂria (Embrapa). Maria Gabriela alertness and response to novelty [1]. Like other behavioral traits, temperament is influenced Campolina Diniz Peixoto was supported by the by a complex network of interacting genetic components, environmental factors, genetic- PLOS ONE | DOI:10.1371/journal.pone.0169163 January 26, 2017 1 / 15 Reactivity Candidate Genes in Brazilian Guzerat Cattle Fapemig - CVZ APQ 01353 e CVZ APQ 3182-5.04/ environment interactions and life cycle events. In addition, the impact of parental experiences 07. MRSC has a fellowship from the CNPq ± is transmitted not only through shared environment but also through epigenetic mechanisms 307975/2010-0 and was supported by CNPq ± [2]. Although temperament would seem to be a brain construction, it also reflects adrenal, thy- 312068/2015-8 and 481018/2008-5 projects. MGCDP, RVV, and MAM have fellowships from roid, liver, muscle and peripheral nervous system metabolism [2±4]. FAPEMIG. PASF has CNPq fellowship. FCS and ICR Cattle temperament describes ªconsistent behavioral and physiological differences observed have CAPES fellowships. between individuals in response to human interaction or environmental challengeº [3,5]. An Competing Interests: The authors have declared observable demonstration of cattle temperament is reactivity [6]. Reactivity to humans is that no competing interests exist. mainly influenced by previous experiences of an animal with humans and depends on the con- text; for example, it can be influenced by fear [3]. Temperament is also an important compo- nent of bovine social behavior which affects animal welfare, animal-animal interactions and the animal-herdsman relationship. More excitable animals react with increased aggression and/or fear to human contact or handling. Aggressive animals present less weight gain, reduced reproductive efficiency, lower milk production, inferior meat quality and higher dis- ease susceptibility [2]. They also cause more accidents, increase herd and facility maintenance costs; and, harm themselves, other animals and even herdsmen [7±9]. Consequently, animal temperament impacts the economic efficiency of the production system. As expected, the broad and subjective definition of temperament leads to difficulties in the robust assessment of this trait [3,10]. Many different methods to evaluate different tempera- ment phenotypes have been proposed [10]. In general, tests of temperament are divided into two categories: movement restraint or movement non-restraint methods. Non-restraint meth- ods allow the animal to remain free to move around, while a technician subjectively assigns scores to the temperament or a device objectively measures traits that correlate to tempera- ment, such as heart rate. Among the restraint-based methods, the crush test and flight speed are frequently used. In the crush test, the animal is held in a crush and scores are subjectively assigned, considering the frequency and intensity of the movements, audible breathing and the frequency of bellow- ing and jumping [11]. In flight speed, the time the animal takes to travel a certain distance after being released from a balance-chute is measured using a photoelectric cell [12]. In the last decade, a new and objective method (REATEST1) was developed to evaluate animal reactivity [13]. In this test, the animal is held during the weighing and an electronic device, positioned under the chute, measures its reactivity based on the frequency and inten- sity of its movements while confined. This device contains an accelerometer which measures the frequence, intensity and temporary variation of movements for 20 seconds while the ani- mal is on the chute. The total number of pulses is automatically processed on a specific soft- ware and converted in a value in a continuous grading scale. This value is used herein as the measurement of reactivity [13±15]. Flight speed and REATEST1 were compared in the eval- uation of the Nellore breed temperament and presented high positive correlation [10]. In addition, REATEST1 results correlated better with temperament scores from crush test, than flight speed [13,15,16]. Similarly, Peixoto et al (2016) [14] found a significative correla- tion (0.89) between the crush test and REATEST1 in the Guzerat breed. REATEST1 has several advantages: 1) it does not interfere in the daily management of farms and does not increase the number of activities with the animal, thus allowing the assessment of many ani- mals in one day; 2) it eliminates the subjectivity of the evaluator; 3) it allows the detection of higher phenotypic variability, when compared to temperament scores; and, 4) the test does not expose the evaluator to additional accident risks and requires no changes in farm struc- ture [16]. REATEST1 has a main limitation, common to most phenotyping devices for behavior: lack of specificity. It has been stated that reactivity is related to aggressiveness in an animal [16]. Thinking about the reactions detected by REATEST1, it is reasonable that the device may also PLOS ONE | DOI:10.1371/journal.pone.0169163 January 26, 2017 2 / 15 Reactivity Candidate Genes in Brazilian Guzerat Cattle indirectly assess fear, panic, excitability, and anxiety. In this sense, reactivity, as a component of temperament has its own components. Temperament is a complex trait, comprising many phenotypes, probably influenced by many genes and pathways as well as environmental factors and gene-environmental interac- tions [3]. Furthermore, within a population, the same phenotype (e.g., aggressiveness) may be caused by different genetic components among different individuals/breeds. In this context, the more complex the phenotype, the harder it is to find candidate genes/regions. Despite its broad definition, several genes have already been associated with cattle tempera- ment components [17±19], such as movement on a weighing scale, habituation, disposition and docility [17,18,20]. Genes as GLRB and GRIA2 on BTA17 and QKI on BTA9
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