Selection signatures for heat tolerance in Brazilian horse breeds.
Abstract: Since domestication, horse breeds have adapted to their environments and differentiated from one another. This paper uses two methods to detect selection signatures in 23 horse breeds, eight of which are Brazilian (610 animals), both cold-blooded and warm-blooded, from temperate and tropical regions. These animals were genotyped using the GGP Equine BeadChip and we analysed the data by Principal Component Analysis (PCA). The samples were separated into groups based on their geographical area of origin and PCA results studied. The genomic regions under selection were detected by hapFLK and PCAdapt methodologies, identifying six regions under selection with at least one Brazilian horse breed. These regions contain genes associated with heat tolerance, skin colour, body size, energy production/metabolism, genes involved in protein degradation/turnover/DNA repair, genes reducing the impact of oxidative stress/cellular repair, and transcriptional regulation. This work confirmed LCORL and NCAPG gene regions in previous studies associated with body size on Equine Chromosome Autosome 3 (ECA3). On the same ECA3, a region implicating genes linked to coat colour was identified, also previously related to heat stress. Regions with genes coding heat shock proteins were found on ECA1 and 2, and many candidate genes for oxidation-reduction which are a natural response to heat stress. However, a larger sample size and whole-genome SNPs are needed to understand better and identify new candidate regions as well as their functional relation with heat tolerance.
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Publication Date: 2022-02-12 PubMed ID: 35150300PubMed Central: 7144971DOI: 10.1007/s00438-022-01862-wGoogle Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research focuses on the genetic adaptations horses have made in response to their environment, particularly with regards to heat tolerance. Using DNA sample analysis from 23 different horse breeds, the researchers identified six regions of genetic selection linked with heat tolerance traits in Brazilian horse breeds.
Screening Methodology and Analysis
- The team obtained genetic material from 610 animals, covering 23 domesticated horse breeds which included eight Brazilian breeds.
- The horses were classified as either ‘cold-blooded’ or ‘warm-blooded’, and were derived from countries with either temperate or tropical climates.
- DNA was analysed using a GGP Equine BeadChip which allowed for in-depth genotyping.
- Data was processed via Principal Component Analysis (PCA), a statistical technique that reduces the dimensionality of the dataset while retaining most of the information in it. This allowed for differentiation and clustering of the horse breeds based on their genetic profiles and the geographical area they originated from.
Detection of Selection Signatures
- Signatures of selection were identified through two statistical methods: hapFLK and PCAdapt. These strategies permit the detection of genomic regions that have been subject to selection.
- Six selection areas were identified which showed an element of selection in at least one Brazilian horse breed.
Genes and Traits Associated with Heat Tolerance
- The six selection areas contained genes associated with various traits including heat tolerance, skin colour, body size, and energy production/metabolism. The presence of these genes suggests that these traits evolved as adaptive responses to the tropical conditions.
- Also detected were genes involved in protein degradation/turnover/DNA repair and genes that helped lessen the impact of oxidative stress/cellular repair. Both these categories of genes are involved in maintaining the health of cells under heat stress.
- The research confirmed the presence of the LCORL and NCAPG gene regions, which were linked to body size in past studies, within these sections. They also detected genes associated with coat colour on the Equine Chromosome Autosome 3 (ECA3), which was previously associated with heat stress.
- Significant findings include regions on ECA1 and 2 that code for heat shock proteins. These proteins help tolerate and protect against heat stress and many candidate genes for oxidation-reduction, which is a naturally occurring response to heat stress.
Suggestions for Future Research
- The study concluded that a larger sample size and whole-genome single-nucleotide polymorphisms (SNPs) are required for better understanding and identification of new candidate regions and their functional relation with heat tolerance. This will provide a more comprehensive understanding of the genetic diversity and adaptive capabilities of horse breeds to heat stress.
Cite This Article
APA
de Faria DA, do Prado Paim T, Dos Santos CA, Paiva SR, Nogueira MB, McManus C.
(2022).
Selection signatures for heat tolerance in Brazilian horse breeds.
Mol Genet Genomics, 297(2), 449-462.
https://doi.org/10.1007/s00438-022-01862-w Publication
Researcher Affiliations
- Faculdade de Agronomia e Veterinária, Instituto Central de Ciências, Campus Darcy Ribeiro, Universidade de Brasília, Asa Norte, Brasília, DF, 70910-900, Brazil.
- Instituto Federal de Educação, Ciência e Tecnologia Goiano, Rodovia Sul Goiana, Km 01, Zona Rural, Rio Verde, GO, 75901-970, Brazil.
- Instituto Federal de Educação, Ciência e Tecnologia Goiano, Rodovia Sul Goiana, Km 01, Zona Rural, Rio Verde, GO, 75901-970, Brazil.
- Embrapa Recursos Genéticos e Biotecnologia, Final W5 Norte, Brasília, DF, 70770-917, Brasil.
- Faculdade de Agronomia e Veterinária, Instituto Central de Ciências, Campus Darcy Ribeiro, Universidade de Brasília, Asa Norte, Brasília, DF, 70910-900, Brazil.
- Departamento de Ciências Fisiológicas, Instituto de Biologia, Campus Darcy Ribeiro, Universidade de Brasília, Asa Norte, Brasília, DF, 70910-900, Brazil. concepta@unb.br.
MeSH Terms
- Animals
- Brazil
- Genome
- Genomics / methods
- Genotype
- Horses / genetics
- Polymorphism, Single Nucleotide / genetics
- Selection, Genetic
- Thermotolerance / genetics
Grant Funding
- 001 / Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- 308929/2020-9 / Conselho Nacional de Desenvolvimento Científico e Tecnológico
- 001 / Ministério da Agricultura, Pecuária e Abastecimento
References
This article includes 86 references
- Abhijith A, Joy A, Prathap P, Vidya M, Niyas PA, Madiajagan B. Role of heat shock proteins in livestock adaptation to heat stress. J Dairy Vet Anim Res 2017;5:00127.
- Ablondi M, Viklund Å, Lindgren G, Eriksson S, Mikko S. Signatures of selection in the genome of Swedish warmblood horses selected for sport performance. BMC Genom 2019;20(1):717.
- Afsal A, Sejian V, Bagath M, Krishnan G, Devaraj C, Bhatta R. Heat stress and livestock adaptation: neuro-endocrine regulation. Int J Vet Anim Med 2018;1(2):1–8.
- Al Abri MA, Holl HM, Kalla SE, Sutter NB, Brooks SA. Whole genome detection of sequence and structural polymorphism in six diverse horses. PLoS ONE 2020;15(4):e0230899.
- Álvarez I, Fernández I, Traoré A, Pérez-Pardal L, Menéndez-Arias NA, Goyache F. Genomic scan of selective sweeps in Djallonké (West African Dwarf) sheep shed light on adaptation to harsh environments. Sci Rep 2020;10(1):2824.
- Bahbahani H, Tijjani A, Mukasa C, Wragg D, Almathen F, Nash O. Signatures of selection for environmental adaptation and zebu × taurine hybrid fitness in East African Shorthorn Zebu. Front Genet 2017;8:68.
- Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperth 2014;30(7):513–523.
- Belhadj Slimen I, Najar T, Ghram A, Abdrrabba M. Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr 2016;100(3):401–412.
- Berihulay H, Abied A, He X, Jiang L, Ma Y. Adaptation mechanisms of small ruminants to environmental heat stress. Animals .
- Bhati M, Kadri NK, Crysnanto D, Pausch H. Assessing genomic diversity and signatures of selection in Original Braunvieh cattle using whole-genome sequencing data. BMC Genom 2020;21(1):27.
- Braga RM. Cavalo Lavradeiro em Roraima: aspectos históricos, ecológicos e de conservação. 2000.
- Braga RM. Cavalo Lavradeiro: aspectos históricos, situação atual, desafios e possíveis soluções para sua conservação. 2019.
- Castanheira M, Rezende Paiva S, Louvandini H, Landim A, Fiorvanti MCS, Regina Paludo G. Multivariate analysis for characteristics of heat tolerance in horses in Brazil. Trop Anim Health Prod 2010;42(2):185–191.
- Cattell RB. The scree test for the number of factors. Multivar Behav Res 1966;1(2):245–276.
- Chedid M, Jaber L, Giger-Reverdin S, Duvaux-Ponter C, Hamadeh S. Review: water stress in sheep raised under arid conditions. Can J Anim Sci 2014;94:243–257.
- Chen Y, Arsenault R, Napper S, Griebel P. Models and methods to investigate acute stress responses in cattle. Animals .
- Chen M, Pan D, Ren H, Fu J, Li J, Su G. Identification of selective sweeps reveals divergent selection between Chinese Holstein and Simmental cattle populations. Genet Sel Evol 2016;48(1):76.
- Chen M, Wang J, Wang Y, Wu Y, Fu J, Liu J-F. Genome-wide detection of selection signatures in Chinese indigenous Laiwu pigs revealed candidate genes regulating fat deposition in muscle. BMC Genet 2018;19(1):31.
- Coenen M. Exercise and stress: impact on adaptive processes involving water and electrolytes. Livest Prod Sci 2005;92(2):131–145.
- Cortés O, Dunner S, Gama LT, Martínez AM, Delgado JV, Ginja C. The legacy of Columbus in American horse populations assessed by microsatellite markers. J Anim Breed Genet 2017;134(4):340–350.
- Costa MDR. A história dos equinos na Amazônia: ênfase ao cavalo marajoara. 2008.
- Costin G-E, Hearing VJ. Human skin pigmentation: melanocytes modulate skin color in response to stress. FASEB J 2007;21(4):976–994.
- Edea Z, Dadi H, Dessie T, Kim K-S. Genomic signatures of high-altitude adaptation in Ethiopian sheep populations. Genes Genom 2019;41(8):973–981.
- . The second report on the state of the world’s animal genetic resourses for food and agriculture. 2015.
- Fariello MI, Boitard S, Naya H, SanCristobal M, Servin B. Detecting signatures of selection through haplotype differentiation among hierarchically structured populations. Genetics 2013;193(3):929–941.
- Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 1999;61(1):243–282.
- Figueiró MR, Saraiva NZ, Sales RL, Marques LC, Costa JS, Leal RP. Características fenotípicas de mini cavalo puruca (Eqqus caballus) da Illa do Marajó, Pará, Brasil. 2016.
- Figueró MR, Saraiva NZ, Sales RL, Marques LC, Costa JS, Leal RP. Características fenotípicas de equinos (Eqqus caballus) da raça marajoara em conservação na Ilha de Marajó. 2016.
- Fleming DS, Weigend S, Simianer H, Weigend A, Rothschild M, Schmidt C. Genomic comparison of indigenous African and Northern European chickens reveals putative mechanisms of stress tolerance related to environmental selection pressure. G3 Genes Genom Genet 2017;7(5):1525.
- Gazolla AG, Lima FC, Serra OR. Condições de Manejo, Conservação, Estado Sanitário e Caracterização Fenotípica do Cavalo Baixadeiro. .
- Geibel J, Reimer C, Pook T, Weigend S, Weigend A, Simianer H. How imputation can mitigate SNP ascertainment Bias. BMC Genom 2021;22(1):340.
- Ghoreishifar SM, Eriksson S, Johansson AM, Khansefid M, Moghaddaszadeh-Ahrabi S, Parna N. Signatures of selection reveal candidate genes involved in economic traits and cold acclimation in five Swedish cattle breeds. Genet Sel Evol 2020;52(1):52.
- Grilz-Seger G, Druml T, Neuditschko M, Mesarič M, Cotman M, Brem G. Analysis of ROH patterns in the Noriker horse breed reveals signatures of selection for coat color and body size. Anim Genet 2019;50(4):334–346.
- Guo J, Tao H, Li P, Li L, Zhong T, Wang L. Whole-genome sequencing reveals selection signatures associated with important traits in six goat breeds. Sci Rep 2018;8(1):10405.
- Gurgul A, Jasielczuk I, Semik-Gurgul E, Pawlina-Tyszko K, Stefaniuk-Szmukier M, Szmatoła T. A genome-wide scan for diversifying selection signatures in selected horse breeds. PLoS ONE 2019;14(1):e0210751.
- Hao Y, Feng Y, Yang P, Cui Y, Liu J, Yang C. Transcriptome analysis reveals that constant heat stress modifies the metabolism and structure of the porcine longissimus dorsi skeletal muscle. Mol Genet Genom 2016;291(6):2101–2115.
- Ianella P, Albuquerque MDSM, Paiva SR, Egito AAD, Almeida LD, Sereno FTPS. D-loop haplotype diversity in Brazilian horse breeds. Genet Mol Biol 2017;40:604–609.
- Igoshin AV, Yurchenko AA, Belonogova NM, Petrovsky DV, Aitnazarov RB, Soloshenko VA. Genome-wide association study and scan for signatures of selection point to candidate genes for body temperature maintenance under the cold stress in Siberian cattle populations. BMC Genet 2019;20(1):26.
- Jensen P. The ethology of domestic animals: an introductory text. 2017.
- Kim ES, Elbeltagy AR, Aboul-Naga AM, Rischkowsky B, Sayre B, Mwacharo JM. Multiple genomic signatures of selection in goats and sheep indigenous to a hot arid environment. Heredity 2016;116(3):255–264.
- Kim J, Hanotte O, Mwai OA, Dessie T, Bashir S, Diallo B. The genome landscape of indigenous African cattle. Genome Biol 2017;18(1):34.
- Kim S, Cheong HS, Shin HD, Lee S-S, Roh H-J, Jeon D-Y. Genetic diversity and divergence among Korean cattle breeds assessed using a BovineHD single-nucleotide polymorphism chip. Asian Australas J Anim Sci 2018;31(11):1691–1699.
- Kurtz Filho M, Löf H. Biometria de eqüinos da raça crioula no Brasil. Arch Vet Sci 2007;12(1).
- Lachance J, Tishkoff SA. SNP ascertainment bias in population genetic analyses: why it is important, and how to correct it. BioEssays News Rev Mol Cell Dev Biol 2013;35(9):780–786.
- Lage M, Bergmann J, Procópio A, Pereira J, Biondini J. Associação entre medidas lineares e angulares de equinos da raça Mangalarga Marchador. Arquivo Brasileiro De Medicina Veterinária e Zootecnia 2009;61(4):968–979.
- Luu K, Bazin E, Blum MGB. pcadapt: an R package to perform genome scans for selection based on principal component analysis. Mol Ecol Resour 2017;17(1):67–77.
- Maciel FC, Bertoli CD, Braccini Neto J, Cobuci JA, Paiva SR, McManus CM. Population structure and genealogical analysis of the Brazilian Crioula Horse. Anim Genet Resour 2014;54:115–125.
- Maruch S. Estudo de características morfométricas em equinos Mangalarga Marchador por meio de modelo animal e componentes principais. 2018.
- Mastrangelo S, Tolone M, Sardina MT, Sottile G, Sutera AM, Di Gerlando R. Genome-wide scan for runs of homozygosity identifies potential candidate genes associated with local adaptation in Valle del Belice sheep. Genet Sel Evol 2017;49(1):84.
- Mcmanus C, Falcão R, Spritze A, Costa D, Louvandini H, Dias L. Variação genética, fenotípica e caracterização do cavalo Campeiro. Revista Brasileira De Zootecnia 2005;34(5):1553–1562.
- McManus C, Santos SA, Dallago BSL, Paiva SR, Martins RFS, Braccini Neto J. Evaluation of conservation program for the Pantaneiro horse in Brazil. Revista Brasileira De Zootecnia 2013;42:404–413.
- McManus CM, Faria DA, Lucci CM, Louvandini H, Pereira SA, Paiva SR. Heat stress effects on sheep: are hair sheep more heat resistant?. Theriogenology 2020;155:157–167.
- Metzger J, Philipp U, Lopes MS, da Camara Machado A, Felicetti M, Silvestrelli M. Analysis of copy number variants by three detection algorithms and their association with body size in horses. BMC Genom 2013;14(1):487.
- Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988;16(3):1215–1215.
- Mirol PM, García PP, Vega-Pla JL, Dulout FN. Phylogenetic relationships of Argentinean Creole horses and other South American and Spanish breeds inferred from mitochondrial DNA sequences. Anim Genet 2002;33(5):356–363.
- Miserani MG, McManus C, Santos SA, Silva JAD, Mariante ADS, Abreu UGPD. Avaliação dos fatores que influem nas medidas lineares do cavalo Pantaneiro. Revista Brasileira De Zootecnia 2002;31:335–341.
- Mitchell D, Snelling EP, Hetem RS, Maloney SK, Strauss WM, Fuller A. Revisiting concepts of thermal physiology: predicting responses of mammals to climate change. J Anim Ecol 2018;87(4):956–973.
- Mwacharo JM, Okeyo AM, Kamande GK, Rege JEO. The small East African shorthorn zebu cows in Kenya. I: Linear body measurements. Trop Anim Health Prod 2006;38(1):65–74.
- Nolte W, Thaller G, Kuehn C. Selection signatures in four German warmblood horse breeds: tracing breeding history in the modern sport horse. PLoS ONE 2019;14(4):e0215913.
- Pamplona R, Costantini D. Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol 2011;301(4):R843–R863.
- Patterson L, Staiger EA, Brooks SA. DMRT3 is associated with gait type in Mangalarga Marchador horses, but does not control gait ability. Anim Genet 2015;46(2):213–215.
- Petersen JL, Mickelson JR, Cothran EG, Andersson LS, Axelsson J, Bailey E. Genetic diversity in the modern horse illustrated from genome-wide SNP data. PLoS ONE 2013;8(1):e54997.
- Petersen JL, Mickelson JR, Rendahl AK, Valberg SJ, Andersson LS, Axelsson J. Genome-wide analysis reveals selection for important traits in domestic horse breeds. PLoS Genet 2013;9(1):e1003211.
- Pimentel AMH, Souza JRMD, Boligon AA, Moreira HLM, Pimentel CA, Martins CF. Biometric evaluation of Criollo horses participating in the Freio de Ouro competition, Brazil. Revista Brasileira de Zootecnia 2018;47.
- Privé F, Luu K, Vilhjálmsson BJ, Blum MGB. Performing highly efficient genome scans for local adaptation with R package pcadapt version 4. Mol Biol Evol 2020;37(7):2153–2154.
- Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007;81(3):559–575.
- Qiu XB, Shao YM, Miao S, Wang L. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci CMLS 2006;63(22):2560–2570.
- Quinton J, Tracy SV, Gefeng L, Yu C, Currie RW. Heat shock proteins protect against ischemia and inflammation through multiple mechanisms. Inflamm Allergy Drug Targ (discontinued) 2011;10(4):247–259.
- Reis SP, Gonçalves EC, Silva A, Schneider MP. Genetic variability and efficiency of DNA microsatellite markers for paternity testing in horse breeds from the Brazilian Marajó archipelago. Genet Mol Biol 2008;31:68–72.
- Saadeldin IM, Swelum AA-A, Elsafadi M, Mahmood A, Osama A, Shikshaky H. Thermotolerance and plasticity of camel somatic cells exposed to acute and chronic heat stress. J Adv Res 2020;22:105–118.
- Saravanan KA, Panigrahi M, Kumar H, Bhushan B, Dutt T, Mishra BP. Selection signatures in livestock genome: a review of concepts, approaches and applications. Livest Sci 2020;241:104257.
- Scheet P, Stephens M. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 2006;78(4):629–644.
- Schreck R, Rieber P, Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 1991;10(8):2247–2258.
- Sejian V, Gaughan J, Baumgard L, Prasad CS. Climate change impact on livestock: adaptation and mitigation. 2015.
- Sharma A, Lee JS, Dang CG, Sudrajad P, Kim HC, Yeon SH. Stories and challenges of genome wide association studies in livestock—a review. Asian Australas J Anim Sci 2015;28(10):1371–1379.
- Shields A, Panayi G, Corrigall V. A new-age for biologic therapies: long-term drug-free therapy with BiP?. Front Immunol 2012;3:17.
- Silva R, La Scala Jr N, Tonhati H. Radiative properties of the skin and haircoat of cattle and other animals. Trans ASAE .
- Silva ACM, Paiva S, Albuquerque M, Egito A, Santos S, Lima FC. Genetic variability in local Brazilian horse lines using microsatellite markers. GMR 2012;11:881–890.
- Souza AFD, Fonteque JH, Costa D. Campeiro horse: past, present and future of the Araucarias Gaited horse. Revista Acadêmica Ciência Animal 2018;16(Special edition), e162102.
- Srikanth K, Kim N-Y, Park W, Kim J-M, Kim K-D, Lee K-T. Comprehensive genome and transcriptome analyses reveal genetic relationship, selection signature, and transcriptome landscape of small-sized Korean native Jeju horse. Sci Rep 2019;9(1):16672.
- Srikanth K, Kim N-Y, Park W, Kim J-M, Kim K-D, Lee K-T. Author Correction: Comprehensive genome and transcriptome analyses reveal genetic relationship, selection signature, and transcriptome landscape of small-sized Korean native Jeju horse. Sci Rep 2020;10(1):18383.
- Staiger EA, Abri MA, Silva CAS, Brooks SA. Loci impacting polymorphic gait in the Tennessee Walking Horse1. J Anim Sci 2016;94(4):1377–1386.
- Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci 2003;100(16):9440.
- Wickham H. ggplot2: elegant graphics for data analysis. 2016.
- Yurchenko AA, Daetwyler HD, Yudin N, Schnabel RD, Vander Jagt CJ, Soloshenko V. Scans for signatures of selection in Russian cattle breed genomes reveal new candidate genes for environmental adaptation and acclimation. Sci Rep 2018;8(1):12984.
- Zhang H, Wang Z, Wang S, Li H. Progress of genome wide association study in domestic animals. J Anim Sci Biotechnol 2012;3(1):26.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists