Interspecific and extraspecific pregnancies in equids: anything goes.
Abstract: Equids possess the unusual ability to interbreed freely among the phenotypically and karyotypically diverse member species of the genus to produce viable, but usually infertile, offspring. The mule (female horse x male donkey) was humanity's first successful attempt at genetic engineering and its clear expression of both parental phenotypes has contributed much to our understanding of genetic inheritance over the centuries. Even more surprising, mares and donkeys have been shown to be capable of carrying to term a range of true, xenogeneic extraspecies pregnancies created by embryo transfer, including Przewalski's horse (Equus prezwalskii; 2n = 66)-in-horse, (E. caballus; 2n = 64), and Grant's zebra (E. burchelli; 2n = 44)-in-horse pregnancies. Fetal genotypes has a marked influence on placental development in equids, especially on the width and general development of the annulate chorionic girdle, progenitor tissue of the gonadotrophin (eCG)-secreting endometrial cups. However, transfer of intact and bisected demi-mule embryos (E. mulus; 2n = 63) to Jenny donkeys (E. asinus; 2n = 62) showed convincingly that maternal uterine environment, probably mediated by intrauterine growth factor production, can exert an overriding influence on chorionic girdle development and its invasion of the maternal endometrium. Transfer of donkey embryos (2n = 62) to horse mares (2n = 64) results in the development of an exceptionally small chorionic girdle that completely fails to invade the endometrium to form endometrial cups. Around 70% of these donkey-in-horse pregnancies are aborted between days 80 and 85 of gestation in conjunction with delayed and abnormal placental attachment combined with a vigorous maternal cell-mediated reaction against the xenogeneic donkey trophoblast. This model of pregnancy loss shows strong evidence of immune memory and the rate of fetal death is reduced by immunization of the surrogate mare against donkey lymphocytes. The findings suggest an important role for the invasive trophoblast cells of the equine placenta in initiating and driving attachment and interdigitation of the non-invasive placenta for fetal sustenance, and in modulating materno-fetal immunological interaction to enable survival of the antigenetically foreign fetus in the uterus.
Publication Date: 1997-11-05 PubMed ID: 9378914DOI: 10.1093/oxfordjournals.jhered.a023123Google Scholar: Lookup
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- Journal Article
Summary
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The research is an extensive investigation into the unusual capability of equid species (like horses and donkeys) to interbreed and carry extraspecies pregnancies to term. It analyzes the genetic implications of such mixed breeding and how the genetic makeup of the fetus influences placental development. Additionally, the study looks into the role of maternal environment and immune responses in determining the success or failure of these interspecific pregnancies.
Understanding Interspecific and Extraspecific Pregnancies
- Researchers found that equids, member species of the horse family genus, are able to interbreed regardless of their phenotypical and karyotypical diversity, often resulting in viable but usually infertile offspring. An example of this kind of breeding is the mule, the product of a female horse and male donkey.
- This kind of genetic crossover has been of great significance in broadening our understanding of genetic inheritance.
- In certain comparable instances, mares and donkeys have successfully carried xenogeneic extraspecies pregnancies to term through embryo transfer; embryos from different equid species, such as Prezewalski’s horse and Grant’s zebra, were transferred to these species and brought to term.
The Influence of Fetal Genotypes
- The genotype of the fetus significantly influences how the placenta develops in equids. This is most evidently seen in the development of the annulate chorionic girdle, a tissue associated with the production of equine chorionic gonadotropin (eCG), a key hormone in equine pregnancies.
- However, when intact embryos or half embryos of mules were transferred to Jenny donkeys, it showed that the maternal uterine environment can also significantly influence the development of the chorionic girdle, especially in terms of its invasion of the maternal endometrium.
The Role of Maternal Factors
- When donkey embryos were transferred to horses, an exceptionally small chorionic girdle was observed that utterly failed to invade the endometrium which usually results in the formation of endometrial cups. This indicated the presence of maternal factors in determining the nature of the pregnancy.
- About 70% of these donkey-in-horse pregnancies were aborted between the 80th and 85th days of gestation due to abnormal placental attachment and a strong maternal immune reaction against the foreign donkey trophoblast (part of the placenta).
- In such cases of pregnancy loss, there were strong indications of immune memory, and the rate of fetal death was reduced by immunizing the surrogate mare against donkey lymphocytes. This pointed to the role of maternal immunity in interspecific pregnancies.
Conclusion
- These findings emphasize the crucial role of the invasive trophoblast cells of the equine placenta in ensuring proper attachment and fetal sustenance.
- These cells also play a role in moderating maternal immunity to allow the survival of the foreign fetus in the uterus, shedding light on the complex interplay of genetics, environment, and immunity in interspecific equine pregnancies.
Cite This Article
APA
Allen WR, Short RV.
(1997).
Interspecific and extraspecific pregnancies in equids: anything goes.
J Hered, 88(5), 384-392.
https://doi.org/10.1093/oxfordjournals.jhered.a023123 Publication
Researcher Affiliations
- University of Cambridge, Department of Clinical Veterinary Medicine, Cambridge, England.
MeSH Terms
- Animals
- Chorion / physiology
- Crosses, Genetic
- Embryo Transfer
- Endometrium / physiology
- Equidae / genetics
- Female
- Fetus / physiology
- Genetic Engineering / methods
- Gonadotropins / metabolism
- Horses / genetics
- Hybridization, Genetic
- Male
- Pregnancy
- Pregnancy Outcome / veterinary
- Pregnancy, Animal / genetics
- Stem Cells / physiology
Citations
This article has been cited 13 times.- Gambini A, Smith JM, Gurkin RJ, Palacios PD. Current and Emerging Advanced Techniques for Breeding Donkeys and Mules. Animals (Basel) 2025 Mar 29;15(7).
- Martini M, Degl'Innocenti A, Altomonte I, Sodi I, Bocci C, Fanelli D, Moroni R, Panzani D, Camillo F, Salari F. Report on a Milking Mule: Milk Qualitative Characteristics during Lactation. Animals (Basel) 2024 May 27;14(11).
- Fanelli D, Moroni R, Bocci C, Camillo F, Rota A, Panzani D. Interspecific and Intraspecific Artificial Insemination in Domestic Equids. Animals (Basel) 2023 Feb 7;13(4).
- Antczak DF, Allen WRT. Placentation in Equids. Adv Anat Embryol Cell Biol 2021;234:91-128.
- Rigoglio NN, Matias GSS, Miglino MA, Mess AM, Jacob JCF, Smith LC. Morphological characteristics of mule conceptuses during early development. Anim Reprod 2018 Dec 5;15(4):1214-1222.
- Dini P, Kalbfleisch T, Uribe-Salazar JM, Carossino M, Ali HE, Loux SC, Esteller-Vico A, Norris JK, Anand L, Scoggin KE, Rodriguez Lopez CM, Breen J, Bailey E, Daels P, Ball BA. Parental bias in expression and interaction of genes in the equine placenta. Proc Natl Acad Sci U S A 2021 Apr 20;118(16).
- Gambini A, Duque Rodríguez M, Rodríguez MB, Briski O, Flores Bragulat AP, Demergassi N, Losinno L, Salamone DF. Horse ooplasm supports in vitro preimplantation development of zebra ICSI and SCNT embryos without compromising YAP1 and SOX2 expression pattern. PLoS One 2020;15(9):e0238948.
- Heintzman PD, Zazula GD, MacPhee R, Scott E, Cahill JA, McHorse BK, Kapp JD, Stiller M, Wooller MJ, Orlando L, Southon J, Froese DG, Shapiro B. A new genus of horse from Pleistocene North America. Elife 2017 Nov 28;6.
- Steiner CC, Ryder OA. Characterization of Prdm9 in equids and sterility in mules. PLoS One 2013;8(4):e61746.
- de Mestre AM, Hanlon D, Adams AP, Runcan E, Leadbeater JC, Erb HN, Costa CC, Miller D, Allen WR, Antczak DF. Functions of ectopically transplanted invasive horse trophoblast. Reproduction 2011 Jun;141(6):849-56.
- Santani A, Raudsepp T, Chowdhary BP. Interstitial telomeric sites and NORs in Hartmann's zebra (Equus zebra hartmannae) chromosomes. Chromosome Res 2002;10(7):527-34.
- Skidmore JA, Billah M, Binns M, Short RV, Allen WR. Hybridizing Old and New World camelids: Camelus dromedarius x Lama guanicoe. Proc Biol Sci 1999 Apr 7;266(1420):649-56.
- Raudsepp T, Chowdhary BP. Construction of chromosome-specific paints for meta- and submetacentric autosomes and the sex chromosomes in the horse and their use to detect homologous chromosomal segments in the donkey. Chromosome Res 1999;7(2):103-14.
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