Opera Medica et Physiologica

Prenatal Development Study on Phenomenon of Delayed Implantation

Author Affiliations

A.D. Manakhov 1, 2, A.S. Krylova 1, A.Yu. Goltsov 1, T.V. Andreeva 1,3, A.P. Grigorenko 1,4, F.E. Gusev 1, O.V. Trapezov 4, S.N. Kashtanov 1, E.I. Rogaev 1,4 

1 Vavilov Institute of General Genetics, Russian Academy of Sciences, Gubkina str. 3, 119991 Moscow, Russia

2 Lomonosov Moscow State University, GSP-1, Leninskie Gory, Moscow, 119991

3 Center of Brain Neurobiology and Neurogenetics, Institute of Cytogenetics and Genetics, Russian Academy of Sciences Prospekt Lavrentyeva 10, 630090 Novosibirsk, Russia

4 University of Massachusetts Medical School, Department of Psychiatry, BNRI Worcester, MA 01604, USA

Corresponding author: 

E.I. Rogaev (rogaev@vigg.ru)

Published ahead of print December 01, 2015; Printed December 01, 2015; OM&P 2015 Volume 1 Supplement S1, pages 14-15; doi:10.20388/omp2015.00s1.007


Delayed implantation (DI) is arrest of embryo development at the blastocyst stage, characterized by inhibition of mitotic activity and synthesis of nucleic acids in cells of the inner cell mass of embryo and temporary prevention of it implantation in uterus. The Mustelidae family seems to be the most interest for DI research because of extraordinary prevalence of this trait in this family; almost half of mammals with DI are mustelids. Delayed implantation feature is pleomorphic in mustelids. It seems to be inherited from common ancestor. In a process of evolution of this family there were multiple losses of this trait. Furthermore DI length is variable among Mustelidae family: from 50-60 days in mink (Neovison vison) to 245-275 days in marten (Martes martes) or sable (Martes zibellina). [Isakova 2004; Thom et al., 2004]. Mechanisms of transduction between active and inactive embryo stages and factors underlying the length of embryonic diapause are not clearly understood to date. It has been suggested that melatonin (pineal gland secret) is the crucial regulator of this processes. Melatonin secretion depends on photoperiod length and regulates synthesis of luteinizing hormone (LH), follicle stimulating hormone (FSH) and prolactin [Jack et al. 1996; Murphy 2012]. Nonetheless there were no any molecular-genetic studies of DI mechanisms. Research of DI is of great interest for evolutionary biology and may also be important for reproductive medicine and fur industry. Moreover studies showed that presence/absence of DI in prenatal development are correlated with longevity among mustelids [Thom et al., 2004]. We suggest that presence of DI also may have effects on animal behavior. We first made whole genome sequence of three mustelids with delayed implantation stage in prenatal development - mink (Neovison vison), marten (Martes martes) and sable (Martes zibellina). Using the data from whole genome sequencing of these animals and assembled genome of ferret (Mustela putorius furo) which is closely related specie that does not display diapause we analyzed the genes involved in melatonin pathway.


We described a set of genetic alteration in genes of melatonin pathway in mink, marten and sable. The data imply the genetic alteration may lead to changes of quantity and regulation level of melatonin in animals with DI stage in prenatal development.

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   Isakova GK. On the activity of the sable embryonic genome at the stage of delayed implantation: a cytogenetic study. Dokl Biol Sci. 2004; 397:305-306.

   Murphy BD. Embryonic diapause: advances in understanding the enigma of seasonal delayed implantation. Reprod Domest Anim. 2012;47 Suppl 6: 121-124. doi: 10.1111/rda.12046.

   Thom MD, Johnson DD, MacDonald DW, The evolution and maintenance of delayed  implantation in the mustelidae (mammalia: carnivora). Evolution, 2004; 58(1) pp 175-83.