Morphological characteristics of mule conceptuses during early development
Nathia Nathaly Rigoglio, Gustavo de Sá Schiavo Matias, Maria Angelica Miglino, Andrea Maria Mess, Julio Cesar Ferraz Jacob, Lawrence Charles Smith
Hybrids between species are often infertile and extremely rare among mammals. Mules, i.e. crossing between the horse and the donkey, on the other hand are very common in agricultural and leisure practices due to their enhanced post-natal physical characteristics that is believed to occur for outbreeding or hybrid vigor. Since no reports are availableon the effects of hybrid vigor during early development, this study focused on characterizing the intrauterine development of mule conceptuses during critical embryo-to-fetus transition period. Nine embryos and fetuses of early gestation, obtained after artificial insemination and transcervical flushing, were evaluated by means of gross anatomy and histology and compared to data available for the equine. We found that some events, such as C-shape turning, apearence of branchial archs, limb and tail buds, formation of primary and secondary brain vesicles, heart compartmentalization, and development of somites, occurred slightly earlier in the mule. Nonetheless, no major differences were observed in other developmental features, suggesting similarities between the mule and the horse development. In conclusion, these data suggest that the effect of hybrid vigor is present during intrauterine development in the mule, at least with regard to its maternal parent.
Allen WR, Short RV. 1997. Interspecific and extraspecific pregnancies in equids: anything goes. J Hered, 88:384-392.
Anderson GB. 1988. Interspeciﬁc pregnancy: barriers andprospects. Biol Reprod, 38:1-15.
Betteridge KJ. 2000. Comparative aspects of equine embryonic development. Anim Reprod Sci, 60-61:691-702.
Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA. 2010. Heterosis. Plant Cell, 22:2105-2112.
Birchler JA, Auger DL, Riddle NC. 2003. In search of themolecular basis of heterosis. Plant Cell, 15:2236-2239.
Blakley A. 1978. Maternal and embryonic gene effects on placental weight in mice. J Reprod Fertil, 54:301-307.
Blasco A, Ouhayoun J, Masoero G. 1983. Harmonization of criteria and terminology in rabbit meat research. World Rabbit Sci, 1:3-10.
Bradfort GE, Lahlou-Kassi A, Berger YM, Boujenane I, Derqaoui L. 1989. Performance of D’man and Sardi breeds of sheep on accelerated lambing. II. Ovulation rate and embryo survival. Small Rumin Res, 2:241-252.
Brandt H, Müllenhoff A, Lambertz C, Erhardt G, Gauly M. 2010. Estimation of genetic and crossbreeding parameters for prewearing traits in German Angus and Simmental beef cattle and the reciprocal crosses. J Anim Sci, 88:80-86.
Camillo F, Vannozi I, Rota A, Di Luzio B, Romagnoli S, Aria G, Allen WR. 2003. Successful nonsurgical transfer of horse embryos to mule recipients. Reprod Domest Anim, 38:380-385.
Chen ZJ. 2010a. Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci, 15:57-71.
Chen X. 2010b. Small RNAs - Secrets and surprises of the genome. Plant J, 61:941-958.
Cottrill CM, Ho SY, O'Connor WN. 1997. Embryological development of the equine heart. Equine Vet J Suppl, 24:14-18.
Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature, 401:157-161.
Cundiff LV, Nuñez-Domingues R, Dickerson GE, Gregory KE, Koch RM. 1992. Heterosis for lifetime production in Hereford, Angus, Shorthorn, and crossbred cows. J Anim Sci, 70:2397-2410.
Di R, Chu MX, Li YL, Zhang L, Fang L, Feng T, Cao GL, Chen HQ, Li XW. 2012. Predictive potential of microsatellite markers on heterosis of fecundity in crossbreed sheep. Mol Biol Rep, 39:2761-2766.
Ferreira VC, Rosa GJM, Berger YM, Thomas DL. 2015. Survival in crossbreed lambs: breed and heterosis effects. J Anim Sci, 93:912-919.
Franciolli ALR, Cordeiro BM, Da Fonseca ET, Rodrigues MN, Sarmento CA, Ambrósio CE, de Carvalho AF, Miglino MA, Silva LA. 2011. Characteristics of the equine embryo and fetus from days 15 to 107 of pregnancy. Theriogenology, 76:819-832.
Galvin JM, Wilmut I, Day BN, Ritchie M, Thomson M, Haley CS. 1993. Reproductive performance in relation to uterine and embryonic traits during early gestation inMeishan, large white and crossbred sows. J Reprod Fertil, 98:377-384.
Giger R, Meier HP, Küpfer U. 1997. Length of gestation of Freiberger mares with mule and horse foals, Schweiz Arch Tierheilkd, 139:303-307.
Giussani DA, Fowden AL. 2005. Development of cardiovascular function in the horse fetus.Journal of Physiol J Physiol, 565:1019-1030.
Goodwin D. 2007. Equine learning behaviour: what we know, what we don’t and future research priorities. Behav Processes, 76:17-19.
Gray AP. 1972. Mammalian hybrids.2. ed. Farnham Royal, Slough, United Kingdom: Common wealth Agricultural Bureaux, pp.125-128.
Gregory KE, Cundiff LV. 1980. Crossbreeding in beef cattle: evaluation of systems. J Anim Sci, 51:1224-1242.
Groszmann M, Greaves IK, Fujimoto R, Peacock WJ, Dennis ES. 2013. The role of epigenetics in hybrid vigour. Trends Genet, 29:684-690.
Guerrero-Bosagna C, Skinner MK. 2012. Environmentally induced epigenetic transgenerational inheritance of phenotype and disease. Mol Cell Endocrinol, 354:3-8.
He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, Qi Y, Chen R, Deng XW. 2010. Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell, 22:17-33.
Hetherington CM. 1973. The absence of any effect of maternal fetal incompatibility at the H-2 and H-3 loci on pregnancy in the mouse. J Reprod Fertil, 33:135-139.
Hochholdinger F, Hoecker N. 2007. Towards the molecularbasis of heterosis. Trends Plant Sci, 12:427-432.
Jirtle RL, Skinner MK. 2007. Environmental epigenomics and disease susceptibility. Nat Rev Genet, 8:253-262.
Kress DD, Doornbos DE, Anderson DC, Davis KC. 1995. Tarentaise and Hereford breed effects on cow and calf traits and estimates of individual heterosis. J Anim Sci, 73:2574-2578.
Land RB, Russell WS, Donald HP. 1974. The litter size and fertility of Finnish Landrace and Tasmanian Merino sheep and their reciprocal crosses. Anim Sci, 18:265-271.
Lippman ZB, Cohen O, Alvarez JP, Abu-Abied M, Pekker I, Paran I, Eshed Y, Zamir D. 2008. The making of a compound influorescence in tomato and related nightshades. PLoS Biol,18:e288.
Long CH. 1980. Crossbreeding for Beef Production: Experimental Results. J Anim Sci, 51:1197-1223.
Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ,Giovannoni JJ, Seymour GB. 2006. A naturally occurringepigenetic mutation in a gene encoding an SBP-box transcriptionfactor inhibits tomato fruit ripening. Nat Genet, 38:948-952.
Matthews J, Peel S. 1991. The uterine response in pregnant inbred and non-inbred rats. J Anat, 178:101-113.
McGovern PT. 1976. The barriers to interspeciﬁc hybridization in domestic and laboratory mammals. II. Hybrid sterility. Br Vet J, 132:68-75.
Moore KL, Persaud TVN. 2004. EmbriologiaClínica. [ClinicalEmbryology]. 7 ed. Rio de Janeiro: Elsevier. 609p.
Moore T, Haig D. 1991. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7: 45-49.
Newman S, MacNeil MD, Reynolds WL, Knapp BW, Urick JJ. 1993. Fixed effects in the formation of a composite line of beef cattle. I. Experimental design and reproductive performance. J Anim Sci, 71:2026-2032.
Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ. 2009. Altered circadian rhythms regulate growth vigour inhybrids and allopolyploids. Nature, 457:327-331.
Paolucci M, Palombi C, Sylla L, Stradaioli G, Monaci M. 2012. Ultrasonographic features of the mule embryo, fetus and fetal-placental unit. Theriogenology, 77:240-252.
Proops L, Burden F, Osthaus B. 2009. Mule cognition: a case of hybrid vigour. Anim Cogn, 12:75-84.
Retallick KM, Faulkner DB, Rodriguez-Zas SL, Nkrumah JD, Shike DW. 2013. The effect of breed and individual heterosis on the feed efficiency, performance and carcass characteristics of feed lot steers. J Anim Sci, 91:5161-5166.
Rigoglio NN, Barreto RSN, Favaron PO, Jacob JCF, Smith LC, Gastal MO, Gastal EL, Miglino MA. 2017. Central Nervous System and Vertebrae Development in Horses: A Chronological Study with Differential Temporal Expression of Nestin and GFAP. J Mol Neurosci, 61:61-78.
Rodrigues RF, Rodrigues MN, Franciolli ALR, Carvalho RC, Rigoglio NN, Jacob JCF, Gastal EL, Miglino MA. 2014. Embryonicand fetal development of the cardiorespiratory apparatus in horses (EquusCaballus) from 21 to 105 Days of Gestation. J Cytol Histol, 5:240.
Shrestha JNB, Rempel WE, Boylan WJ, Miller KP. 1983. General, specific, maternal and reciprocal effects for ewe productivity in crossing five breeds of sheep. Can J Anim Sci, 63:497-509.
Shindo C, Lister C, Crevillen P, Nordborg M, Dean C. 2006. Variation in the epigenetic silencing of FLC contributes to natural variationin Arabidopsis vernalization response. Genes Dev, 20:3079-3083.
Simmons D. 2008. The behavior of a person's genes doesn't just depend on the genes' DNA sequence - it's also affected by so-called epigenetic factors. Changes in these factors can play a critical role in disease. Epigenetic Influences and Disease NatureEducation, [serial on the Internet], 1:6pp. Available in: https://www.nature.com/scitable/topicpage/epigenetic-influences-and-disease-895. Acessed in: Aug 9th 2016.
Skinner MK, Manikkam M, Guerrero-Bosagna C. 2010. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab, 21:214-222.
Travis L. 1990. The Mule. 1. ed. London, England: J.A. Allen & Co.
Williams JL, Aguilar I, Rekaya R, Bertrand JK. 2010. Estimation of breed and heterosis effects for growth and carcass traits in cattle using published crossbreeding studies. J Anim Sci, 88:460-466.