Research Article

Multiple paternity in American mink: using males of different color lines allows mating efficiency evaluation

Beata Seremak 1 , Lidia Felska-Błaszczyk 2, Marta Dworecka-Borczyk1

1*Department of Animal Reproduction Biotechnology and Environmental Hygiene, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology, Klemensa Janickiego 29, 71-270 Szczecin, Poland

2Laboratory of Animal Anatomy, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology, Doktora Judyma 14,71-466 Szczecin, Poland

Abstract. The study aimed at developing an optimal mink (Neovison vison) mating system by examining the effectiveness of multiple paternity, which was achieved by mating a female to two males of contrastingly different color lines over an interval of time within the same estrus. The hypothesis tested was that embryos generated from the first mating survived and developed despite subsequent matings. The experiment was carried out in two consecutive breeding seasons on a mink farm. We used pure genetic lines of the coat-color varieties. In order to find the most effective system of mating, we counted the offspring sired by each male. Mating to two males of different coat colors on two, time-separated dates produced litters consisting of two distinctly marked groups of kits, easily recognizable as to which kit had been sired by which male. This suggests that blastocysts generated from the first mating do survive until parturition and, what is more, develop normally. Despite prior mating to another male, kits derived from the subsequent mating were more numerous in the litter.

Keywords: American mink, breeding, multiple mating

INTRODUCTION

The life history of the American mink (Neovison vison) is characteristic for the complexity of the reproductive process. This may be a challenge for the farmer; if the breeding performance of a given season is not satisfying, the complexity of the mink reproductive biology does not facilitate diagnosis of the problem. The physiological specificity is marked by monoestrous character, delayed blastocyst implantation, and—in consequence—a varying length of gestation [Yamaguchi et al. 2004Yamaguchi, N., Sarno, R.J., Johnson, W.E., O'Brien, S.J., Macdonald, D.W. (2004). Multiple paternity and reproductive tactics of free-ranging American minks, Mustela vison., J. Mammal., 85, 432–439. https://doi.org/10.1644/1545-1542(2004)0852.0.CO;2, Thom et al. 2004Thom, M., Johnson, D.D.P., Macdonald, D.W. (2004). The evolution and maintenance of delayed implantation in the Mustelidae. Evolution, 58, 175–183. https://doi.org/10.1111/j.0014-3820.2004.tb01584.x].

Diapause, which is followed by photoperiod-triggered resumption of embryonic development and implantation, allows the embryos derived from several joinings which occur on different days to level their development before birth. As a result, total gestation length may vary greatly, from 36 to 85 days; however, most often gestation remains in the range 45 to 55 days [Tauson et al. 2000Tauson, A.H., Fink, R., Chwalibob, A. (2000). The female mink (Mustela vison) as a model for studies on nutrition: reproduction interactions. Rec. Res. Dev. Nutr., 3, 239–263. Google Scholar, Persson 2007Persson, S. (2007). The Mink (Mustela vison) as an indicator of environmental reproductive toxicity. Swed. Univ. Agric. Sci., 50, 1–23. Google Scholar, Seremak et al. 2009Seremak., B., Lasota, B., Masłowska, A., Dziadosz, M., Mieleńczuk, G. (2009). Analysis of relation between the date of first mating to the date of implantation and gestation length in wild and standard color american mink (Neovison vison). Acta. Sci. Pol. Zootechnica, 8(4), 41–48 [in Polish]. Google Scholar, Felska-Błaszczyk et al. 2010Felska-Błaszczyk, L., Sulik, M., Dobosz, M. (2010). Effect of mink (Neovison vison) reproduction in relation to age and colour variety. Acta. Sci. Pol. Zootechnica, 9(3), 19–30. Google Scholar]. During diapause, the development of the embryo is reversibly restrained at the stage of blastocyst and the process of its implantation in the uterus is delayed [Desmarais et al. 2004Desmarais, J.A., Bordignon, V., Lopes, F.L., Smith, L.C., Murphy, B. (2004). The escape of the mink embryo from obligate diapause. Biol. Reprod., 70, 662–670. https://doi.org/10.1095/biolreprod.103.023572, Lopes et al. 2003Lopes, F.L., Desmarais, J.A., Gévry, N.Y., Ledoux, S., Murphy, B.D. (2003). Expression of vascular endothelial growth factor isoforms and receptors Flt-1 and KDR during the pre-implantation period in the mink, Mustela vison. Biol. Reprod., 68, 1926–1933. https://doi.org/10.1095/biolreprod.102.013441, Lefèvre et al. 2011Lefèvre, P.L., Palin, M.F., Chen, G., Turecki, G., Murphy, B.D., (2011). Polyamines are implicated in the emergence of the embryo from obligate diapause. Endocrinology, 152(4), 1627–1639. https://doi.org/10.1210/en.2010-0955]. Diapause in mink also varies in length, depending on the moment of implantation [Wehrenberg et al. 1992Wehrenberg, W.B., Kurt, K.J., Hutz, R.J. (1992). Effects of equine chorionic gonadotropin on reproductive performance in anestrous mink., J. Anim. Sci., 70, 499–502. https://doi.org/10.2527/1992.702499x, Polejaeva et al. 1997Polejaeva, I.A., Reed, W.A., Bunch, T.D., Ellis, L.C., White, K.L. (1997). Prolactin – inducted termination of obligate diapause of mink (Mustela vison) blastocystys in vitro and subsequent establishment of embryonic stem-like cells., J. Reprod. Fert., 109, 229–236. https://doi.org/10.1530/jrf.0.1090229, Lopes et al. 2003Lopes, F.L., Desmarais, J.A., Gévry, N.Y., Ledoux, S., Murphy, B.D. (2003). Expression of vascular endothelial growth factor isoforms and receptors Flt-1 and KDR during the pre-implantation period in the mink, Mustela vison. Biol. Reprod., 68, 1926–1933. https://doi.org/10.1095/biolreprod.102.013441]. According to Lefèvre et al. [2011]Lefèvre, P.L., Palin, M.F., Chen, G., Turecki, G., Murphy, B.D., (2011). Polyamines are implicated in the emergence of the embryo from obligate diapause. Endocrinology, 152(4), 1627–1639. https://doi.org/10.1210/en.2010-0955, diapause lasts 2–3 weeks on average, although it is possible to extend to more than three months [Rose et al. 1986Rose, J., Oldfield, J.E., Stormshak, F. (1986). Changes in serum prolactin concentrations and ovarian prolactin receptors during embryonic diapause in mink. Biol. Reprod., 34, 101–106. https://doi.org/10.1095/biolreprod34.1.101, Martinet et al. 1981Martinet, L., Allais, C., Allain, D. (1981). Role of prolactin and LH in luteal function and blastocyst growth in mink (Mustela vison). J. Reprod. Fert., 29, 119–130. Google Scholar]. Reactivation from diapause is triggered by the increasing photoperiod following the vernal equinox, which results in an increase in circulating prolactin and a subsequent increase in ovarian progesterone synthesis [Renfree and Fenelon 2017Renfree, M.B., Fenelon, J.C. (2017). The enigma of embryonic diapause. Development, 144, 3199–3210. https://doi.org/10.1242/dev.148213, Tauson et al. 2000Tauson, A.H., Fink, R., Chwalibob, A. (2000). The female mink (Mustela vison) as a model for studies on nutrition: reproduction interactions. Rec. Res. Dev. Nutr., 3, 239–263. Google Scholar, Lopes et al. 2004Lopes, F.L., Desmarais, J.A., Murphy, B.D. (2004). Embryonic diapause and its regulation. Reproduction, 128, 669–678. https://doi.org/10.1530/rep.1.00444]. According to Murphy and James [1974]Murphy, B.D., James, D.A. (1974). The effects of light and sympathetic innervation to the head on nidation in mink., J. Exp. Zoo., 187(2), 267–276. https://doi.org/10.1002/jez.1401870210, the daylight phase of 12 to 16 hours is an optional signal to induce implantation. Estrus is initiated when the daylight phase reaches 10 hours, i.e. when the day becomes about two hours longer than the eight-hour winter day [Klotchkov et al. 1998Klotchkov, D.V., Trapezov, O.V., Kharlamova, A.V. (1998). Folliculogenesis, onset of puberty and fecundity of mink (Mustela vison Scherb) selectively bred for docility or aggressiveness. Theriogenology, 49, 1545–1553. https://doi.org/10.1016/S0093-691X(98)00100-9, Felska-Błaszczyk et al. 2010Felska-Błaszczyk, L., Sulik, M., Dobosz, M. (2010). Effect of mink (Neovison vison) reproduction in relation to age and colour variety. Acta. Sci. Pol. Zootechnica, 9(3), 19–30. Google Scholar]. The period between implantation and birth, 30–31 days, is rather constant [Song et al. 1998Song, J.H., Sirois, J., Houde, A., Murphy, B. (1998). Cloning, developmental expression, and immunohistochemistry of cyclooxygenase 2 in the endometrium during embryo implantation and gestation in the mink (Mustela vison). Endocrinology, 139(8), 3629–3636. https://doi.org/10.1210/endo.139.8.6142, Gulevich et al. 1995Gulevich, R.G., Klotchkov, D.V., Ivanova, L.N., Osadchuk, L.V. (1995). Gonadal function in mink under artificial photoperiods. J. Reprod. Fert., 103, 147–152. https://doi.org/10.1530/jrf.0.1030147, Polejaeva et al. 1997Polejaeva, I.A., Reed, W.A., Bunch, T.D., Ellis, L.C., White, K.L. (1997). Prolactin – inducted termination of obligate diapause of mink (Mustela vison) blastocystys in vitro and subsequent establishment of embryonic stem-like cells., J. Reprod. Fert., 109, 229–236. https://doi.org/10.1530/jrf.0.1090229, Tauson et al. 2000Tauson, A.H., Fink, R., Chwalibob, A. (2000). The female mink (Mustela vison) as a model for studies on nutrition: reproduction interactions. Rec. Res. Dev. Nutr., 3, 239–263. Google Scholar, Klotchkov and Eryuchenkov 2003Klotchkov, D.V., Eryuchenkov, P.A. (2003). Effects of hCG on folliculogenesis and fecundity in mink (Mustela vison Scherb). Theriogenology, 60, 1583–1593. https://doi.org/10.1016/S0093-691X(03)00093-1].

Sexual maturity is attained at age 8–12 months and is characterized by recurring morphological and hormonal changes in the reproductive system linked with the estrus, i.e. folliculogenesis, ovulation, luteinization and luteolysis of the corpus luteum. Cyclic maturation of oocytes over time allows multiple matings without breaking the estrus, which is a characteristic of the species [Persson 2007Persson, S. (2007). The Mink (Mustela vison) as an indicator of environmental reproductive toxicity. Swed. Univ. Agric. Sci., 50, 1–23. Google Scholar].

Typically, the mink sustain sexual activity for a relatively short period of time [Travis and Pilbeam 1980Travis, H.F., Pilbeam, T.E. (1980). Use of artificial light and day length to alter the life cycles of mink., J. Anim. Sci., 50, 1108–1112. https://doi.org/10.2527/jas1980.5061108x] and a breeding season lasts 2–3 weeks [Trani et al. 2007Trani, M.K., Ford, W.M., Chapman, B.R. (2007). The land manager's guide to mammals of the South. Durham, NC: The Nature Conservancy; Atlanta, GA, U.S. Forest Service. Google Scholar, Seremak et al. 2009Seremak., B., Lasota, B., Masłowska, A., Dziadosz, M., Mieleńczuk, G. (2009). Analysis of relation between the date of first mating to the date of implantation and gestation length in wild and standard color american mink (Neovison vison). Acta. Sci. Pol. Zootechnica, 8(4), 41–48 [in Polish]. Google Scholar] or 1 month at most [Klotchkov and Eryuchenkov 2003Klotchkov, D.V., Eryuchenkov, P.A. (2003). Effects of hCG on folliculogenesis and fecundity in mink (Mustela vison Scherb). Theriogenology, 60, 1583–1593. https://doi.org/10.1016/S0093-691X(03)00093-1]. Follicles continuously mature on the ovaries during the season of sexual activity, with their greatest numbers appearing – in the moderate climate of Poland – between March 10 and 20. The continuous maturation of ova during the estrus period is addressed with a system of mating a single female to one or more males at several times [Seremak et al. 2009Seremak., B., Lasota, B., Masłowska, A., Dziadosz, M., Mieleńczuk, G. (2009). Analysis of relation between the date of first mating to the date of implantation and gestation length in wild and standard color american mink (Neovison vison). Acta. Sci. Pol. Zootechnica, 8(4), 41–48 [in Polish]. Google Scholar]. Copulation, ovulation or conception do not shorten the period of estrus [Persson 2007Persson, S. (2007). The Mink (Mustela vison) as an indicator of environmental reproductive toxicity. Swed. Univ. Agric. Sci., 50, 1–23. Google Scholar], and blastocysts resulting from the initial mating develop, despite any subsequent copulations [Murphy 1983Murphy, B.D. (1983). Precocious induction of luteal activation and termination of delayed implantation in mink with the dopamine antagonist pimozide. Biol. Reprod., 29, 658–662. https://doi.org/10.1095/biolreprod29.3.658, Polejaeva et al. 1997Polejaeva, I.A., Reed, W.A., Bunch, T.D., Ellis, L.C., White, K.L. (1997). Prolactin – inducted termination of obligate diapause of mink (Mustela vison) blastocystys in vitro and subsequent establishment of embryonic stem-like cells., J. Reprod. Fert., 109, 229–236. https://doi.org/10.1530/jrf.0.1090229, Klotchkov and Eryuchenkov 2003Klotchkov, D.V., Eryuchenkov, P.A. (2003). Effects of hCG on folliculogenesis and fecundity in mink (Mustela vison Scherb). Theriogenology, 60, 1583–1593. https://doi.org/10.1016/S0093-691X(03)00093-1].

Many farms apply a group system of breeding in which a group of closely related females is joined with an unrelated pool of males which are also related to each other. Such a mating system allows changing the sires while maintaining genetic improvement of the herd [Seremak et al. 2011Seremak, B., Dziadosz, M., Felska-Błaszczyk, L., Lasota, B., Pławski, K., Masłowska, A., Mieleńczuk, G. (2011). A novel arrangement of breeding sets has a positive effect on some reproductive parameters in females of the american mink (Neovison vison). Acta. Sci. Pol. Zootechnica 10(4), 105–114 [in Polish]. Google Scholar]. Many farmers are concerned with selecting the most suitable date to start breeding in order to obtain the greatest conception rates and largest litters. Long-established on-farm practice and observations have allowed the farmers to develop mating systems that are appropriate for this particular species. Farm practices include double mating, according to the formula 1 + 8 or 1 + 9 (numbers represent subsequent days on which mating takes place), triple mating, 1 + 2 + 8, 1 + 2 + 9 or 1 + 8 + 9, and quadruple mating, according to the formula 1 + 2 + 8 + 9 [Ślaska and Rozempolska-Rucińska 2011Ślaska, B., Rozempolska-Rucińska, I. (2011). Mating system and level of reproductive performance in mink (Neovison vison). Ann. Anim. Sci., 11(1), 105–113. Google Scholar]. However, on some farms females are still mated only once during the entire reproductive season.

The decision to choose the best mating system is crucial to obtaining large litters. Hence, this study was conducted to check the effectiveness of multiple paternity by joining females with males so that the offspring of each mating would differ in coat color. The hypothesis tested assumed that the embryos generated from the first mating survived and developed despite the subsequent mating.

MATERIAL AND METHODS

This study was carried out in strict accordance with the recommendations of the Polish Act dated 21 January 2005 on Animal Experiments (Journal of Laws 2005, no. 33, pos. 289). The protocol was approved by the Local Ethical Committee for Experiments on Animals at the West Pomeranian University of Technology, Szczecin, Poland (permit number: 3/2013, dated 7 March 2013).

The experiment was carried out during two consecutive years (breeding seasons) on a farm located in northern Poland. The mink were managed in an open-shed system, fed a standard semiliquid chicken- and fish-based feed, according to the standards for the species [PAN 2011PAN (2011). Zalecenia żywieniowe i wartość pokarmowa pasz – zwierzęta futerkowe. Praca zbiorowa, A. Gugołek (red.) [Nutritional recommendations and nutritional value of feed – fur animals. Collective work, A. Gugołek (ed.)], Wydaw. Inst. Fizjol. Żyw. Zwierz. PAN, Jabłonna [in Polish]. Google Scholar]. During the breeding season, the mink were arranged in 70 breeding sets. Each breeding set consisted of a group of 40 females, divided into 5 sections of 8 females each, and 8 males in a sixth section. On the selected day, in the morning, females of a section were monogamously mated to one of the males. Another section of females was similarly mated that evening. Thus, each male had potentially served two females daily. On the following day, another section of females was mated to the males, and so forth.

The studied heard consisted of 2738 females (1791 Pearl, P, and 947 White Hedlund, WH) and 548 males (178 Pearl, 94 White Hedlund, 180 White Regal, WR, and 96 Black Cross, BC), all the animals at age 1 year. Pure genetic lines of color variants were used in order to find the proportion of offspring sired by each male in the litter of a multiple-mated female. Table 1 presents coat colors of the progeny obtained from crossing breeders of each color variant.

Table 1. Coat colors of the kits born from crossing applied color lines
Tabela 1. Kolory urodzonych młodych z poszczególnych krzyżowań odmian barwnych rodziców

Male color
Odmiana barwna samca

Female color
Odmiana barwna samicy

Pearl
Perła

White Hedlund
Biała Hedlunda

Pearl
Perła

Pearl
Perła

Pastel
Pastel

White Hedlund
Biała Hedlunda

Pastel
Pastel

White Hedlund
Biała Hedlunda

White Regal
Biała Regal

Pastel
Pastel

Black Cross
Czarny Krzyżak

Black Cross
Czarny Kryżak

Table 2 presents the scheme of matings in both years of the experiment. The first mating date was assumed as the day the female was bred for the first time in the season (not later than March 7) with a repetition the next day (if any). The second mating took place after seven days and was also possibly repeated the next day, as well as a single mating (with or without repetition the next day) performed later than March 7. All the data were obtained through non-invasive observation which did not require contact with the mink and were carried out during normal farm operations.

Table 2. Mating scheme by year of experiment; color variants of females and of males on the first and second date
Tabela 2. Krycia w kolejnych latach badań; odmiany barwne samic i samców dopuszczonych do kryć w pierwszym i drugim terminie kojarzeń


Female color variant
Odmiana barwna samicy

Male color variant
Odmiana barwna samca

First mating date, I
Krycie w pierwszym terminie, I

Second mating date, II
Krycie w drugim terminie, II

First year
Pierwszy rok

P

P or WR

WR or P

P

WR

P

Second year
Drugi rok

WH

WH

BC

WH

BC

WH

The following mating patterns were designed in relation to multiplicity and dates of matings (Arabic digits, 1 or 2, denote the number of matings, whereas Roman numerals, I or II, denote the date of mating):

  • 1-I – single mating on the first date
  • 1-II – single mating on the second date
  • 2-I – double mating on the first date
  • 2-II – double mating on the second date
  • 1-I 1-II – single mating on the first date and single mating on the second date
  • 1-I 2-II – single mating on the first date and double mating on the second date
  • 2-I 1-II – double mating on the first date and single mating on the second date
  • 2-I 2-II – double mating on the first date and double mating on the second date

The mating process was supervised by designated farm workers, each copulation was duly registered in the female’s records.

Statistical analyses

Data on the number of kits born from each mating were analyzed statistically using the Statistica 12PL package. Descriptive statistics included the arithmetic mean, m, and standard error, SE. HSD Tukey test and two-way ANOVA were performed to test the significance of differences between the values. For fertility, we used the non-parametric Kruskal-Wallis test to compare many samples of independent groups.

RESULTS

The results presented in Tables 3 and 4 are not broken by the color variants of males and females, since we did not analyze the information on the reproduction performance of particular variants. Using pure genetic lines of each color variant was aimed entirely to mark the offspring produced in the given mating scheme.

Table 3. Fertility of mink as the average litter size obtained from mating dates I and II, by date and the number of matings in the first year
Tabela 3. Plenność samic norek z uwzględnieniem średniej liczby norcząt uzyskanych z I oraz II terminu kojarzenia w zależ­ności od zastosowanych terminów i krotności kryć w pierwszym roku badań

Pattern of mating
Krotność oraz termin kryć

Number of matings
Liczba kryć

N

Litter size overall
Liczba urodzonych młodych w miocie

No. of kits derived from each mating (mean)
Liczba młodych z poszczegółnych kryć (średnia)

No. of live-born kits per litter
Liczba żywo urodzonych w miocie

m

SE

I date
I termin

II date
II termin

m

SE

1-I

1

57

5.07AEFG

0.38

5.07

4.56 Aa

0.38

1-II

1

37

6.11B

0.44

6.11

5.43

0.41

2-I

2

228

6.18C

0.20

6.18

5.14BC

0.19

2-II

2

127

6.14D

0.24

6.14

5.70

0.24

1-I 1-II

2

81

6.70E

0.26

2.80**

3.90**

6.01

0.25

1-I 2-II

3

172

6.90F

0.19

1.21**

5.69**

6.29 AB

0.19

2-I 1-II

3

135

6.77G

0.23

1.63**

5.14**

5.95 a

0.23

2-I 2-II

4

628

7.27ABCD

0.08

1.48**

5.79**

6.58AC

0.09

A, B, C… means in columns marked with the same letters differ significantly at P ≤ 0.01 (upper case) and at P ≤ 0.05 (lower case letters); **means in rows differ significantly at P ≤ 0.01.
A, B, C… średnie w kolumnach oznaczone tymi samymi literami różnią się istotnie przy P ≤ 0,01, a małymi literami przy P ≤ 0,05; **średnie w wierszach różnią się statystycznie przy P ≤ 0,01.

Table 4. Fertility of mink as the average litter size obtained from mating dates I and II, by date and the number of matings in the second year
Tabela 4. Plenność samic norek z uwzględnieniem średniej liczby norcząt uzyskanych z I oraz II terminu kojarzenia w zależ­ności od zastosowanych terminów i krotności kryć w drugim roku badań

Pattern of mating
Krotność oraz termin kryć

Number of matings
Liczba kryć

N

Litter size overall
Liczba urodzonych młodych w miocie

No. of kits derived from each mating
(mean)
Liczba młodych z poszczególnych kryć (średnia)



No. of live-born kits per litter
Liczba żywo urodzonych w miocie

m

SE

I date
I termin

II date
II termin

m

SE

1-I

1

39

5.44ACDEFa

0.44

5.44

5.05 ABCDH

0.46

1-II

1

122

7.16 C

0.21

7.16

6.18

0.23

2-I

2

88

6.11 B

0.28

6.11

5.58 EFG

0.27

2-II

2

164

7.18 D

0.18

7.18

6.57D

0.19

1-I 1-II

2

38

7.00E

0.44

1.67**

5.33**

6.71CG

0.41

1-I 2-II

3

77

7.25 F

0.24

0.83**

6.42**

6.88BF

0.24

2-I 1-II

3

109

6.89a

0.23

0.49**

6.40**

6.44H

0.23

2-I 2-II

4

175

7.36AB

0.14

2.10**

5.26**

6.98AE

0.15

A, B, C… means in columns marked with the same letters differ significantly at P ≤ 0.01 (upper case) and at P ≤ 0.05 (lower case letters); **means in rows differ significantly at P ≤ 0.01.
A, B, C… średnie w kolumnach oznaczone tymi samymi literami różnią się istotnie przy P ≤ 0,01, a małymi literami przy P ≤ 0,05; **średnie w wierszach różnią się statystycznie przy P ≤ 0,01.

Fertility of Pearl dams the first year of the study are presented in Table 3. The most numerous litters, 7.27 born and 6.58 live-born kits, were attained by females mated four times (2-I 2-II) during the breeding season. These differed significantly (at P ≤ 0.01) from the litter sizes produced by dams mated once, i.e. on the first date (1-I, 5.07 kits), or on the second date (1-II, 6.11 kits), or mated twice on the first date (2-I, 6.18 kits, and 2-II, 6.14 kits). The lowest average litter of live-born kits, 4.56 individuals, was observed in the group of females mated once on the first date (1-I). If we look at the litter size sired by the first and the second male with the same number of matings (two mating schemes, 1-I 1-II, and 2-I 2-II), more kits may be born if either a single or double mating be repeated using another male. The mean litter sizes obtained from these schemes were, respectively, 3.9 and 5.79, while for the same matings with the first male, 2.80 and 1.48 kits were born only, respectively.

A similar relationship was observed comparing two systems of triple mating according to the scheme 1-I 2-II (single mating in the first and double in the second term) and 2-I 1-II (double mating in the first and single one in the second term), for which the average litter size was 1.21 and 1.63, on the first date, and 5.69 and 5.14 kits, on the second date. It is worth noting that in the 2-I 1-II system a higher average, 5.14 kits, was obtained from the single mating in the second term, compared to the average, 1.63, obtained from the double mating on the first date.

Analysis of White Hedlund females breeding in year 2 (Table 4) reveals that the largest litters were produced by dams mated four times, i.e. twice on the first and twice on the second date (scheme 2-I 2-II) with 7.36 kits per litter on average, significantly (P ≤ 0.01) higher in relation to those mated once or twice on the first date, which produced 6.11 and 5.44 kits per litter, respectively (Table 4). Those dams also produced the largest live-born litters, 6.98 kits on average. By far the lowest litter sizes of born (5.44) and live-born kits (5.05) were obtained from females mated once on the first date of the breeding season. These data differed significantly (P ≤ 0.01) between litters produced by dams mated in 1-II and 2-II schemes, i.e. 7.46 and 7.18, respectively, born and live-born kits per litter, and those obtained from females mated in systems 2-I and 2–1 2-II, which averaged 5.58 and 6.98 kits per litter, respectively. The average live-born litter size (5.05 kits) in the dams mated 1-I differed significantly (P ≤ 0.05) from that obtained from dams mated three times 1-I 2-II.

DISCUSSION

The American mink breeding physiology is characteristic for superfetation, or fertilization of oocytes ovulating in subsequent cycles, which leads to implantation of another ovum without shortening the oestrus cycle [Persson 2007Persson, S. (2007). The Mink (Mustela vison) as an indicator of environmental reproductive toxicity. Swed. Univ. Agric. Sci., 50, 1–23. Google Scholar]. Another specificity is superfecundation, i.e. fertilization of the egg cells generated within a single ovulation cycle by sperm coming from different, time-separated sexual acts [Lefèvre and Murphy 2008Lefèvre, P., Murphy, B.D. (2008). Physiological constrains on litter size in mink. Scientifur, 32(4), 13–14. Google Scholar]. Thus, the cyclic maturation of oocytes per heat allowed the development of a multiple-mating system using the same or different males [Seremak et al. 2009Seremak., B., Lasota, B., Masłowska, A., Dziadosz, M., Mieleńczuk, G. (2009). Analysis of relation between the date of first mating to the date of implantation and gestation length in wild and standard color american mink (Neovison vison). Acta. Sci. Pol. Zootechnica, 8(4), 41–48 [in Polish]. Google Scholar]. Both our results and those reported by Ślaska et al. [2009]Ślaska, B., Rozempolska-Rucińska, I., Jeżewska-Witkowska, G. (2009). Variation in some reproductive traits of mink (Neovison vison) according to their coat colour. Ann. Anim. Sci., 9(3), 287–297. Google Scholar confirm that the litter sizes in farmed mink are larger if more matings are applied.

Besides the outcomes of multiple matings, our study shows that the date of mating is important for the quality of reproduction parameters. Although the latter proves crucial in terms of breeding performance, it is often neglected in the subject literature or discussed only in general. The impact of the date of mating was evaluated by means of the mean size of the litter sired by males of different coat colors (light or dark). This was possible since we applied crossing males and females of pure genetic lines of contrasting color variants.

The positive effect of multiple mating for litter size has also been reported by Møller [1974]Møller, O.M. (1974). The Fine Structure of the Lutein Cells in the Blue Fox (Alopex lagopus) with Special Reference to the Secretory Activity during Pregnancy. Cell Tiss. Res., 149, 61–79. https://doi.org/10.1007/BF00209050, who assessed this gain at a level of 0.2–0.3 kits per litter. Likewise, Ślaska et al. [2009]Ślaska, B., Rozempolska-Rucińska, I., Jeżewska-Witkowska, G. (2009). Variation in some reproductive traits of mink (Neovison vison) according to their coat colour. Ann. Anim. Sci., 9(3), 287–297. Google Scholar attained a higher level of fertility in mink females mated repeatedly as compared to those mated only once or twice. The multiple matings should not be, however, considerably extended in time, as this makes the diapause longer, which is adverse in relation to embryonic survival rates [Rozempolska-Rucińska et al. 2004Rozempolska-Rucińska, I., Jeżewska, G., Zięba, G. (2004). Influence of whelping date on reproduction traits in minks. Acta Sci. Pol. Zootechnica, 3(1), 67–76 [in Polish]. Google Scholar]. This is linked with the fact of ovulation recurring several times during a breeding season and the possibility to produce offspring from time-separated ovulations [Sundqvist et al. 1989Sundqvist, C., Amador, A.G., Bartke, A. (1989). Reproduction and fertility in the mink (Mustela vision)., J. Reprod. Fertil., 85, 413–441. https://doi.org/10.1530/jrf.0.0850413].

The fertilization of an already pregnant female in subsequent ovulations is possible due to delayed implantation and embryonic diapause [Yamaguchi et al. 2006Yamaguchi, N., Dugdale, H.L., Macdonald, D.W. (2006). Female receptiveity, embryonic diapause, and superfetation in the European badger (Meles meles): implications for the reproductive tactics of males and females., Q. Rev. Biol., 81, 33–48. https://doi.org/10.1086/503923], which in turn is associated with a low level of progesterone produced by corpora lutea, insufficient to prevent subsequent ovulations. Applying a 7-day break and mating on day 8 is reasonable, as supported by Elofson et al. [1989]Elofson, L., Lagerkvist, G., Gustafsson, H., Einarsson, S. (1989). Mating systems and reproduction in mink. Acta Agric. Scand., 39, 23–41. https://doi.org/10.1080/00015128909438496, and allows another ovulation to come forth. From the perspective of the species reproduction physiology, such a system of mating is indeed fully justified.

Our results confirm the findings reported by Polejaeva et al. [1997]Polejaeva, I.A., Reed, W.A., Bunch, T.D., Ellis, L.C., White, K.L. (1997). Prolactin – inducted termination of obligate diapause of mink (Mustela vison) blastocystys in vitro and subsequent establishment of embryonic stem-like cells., J. Reprod. Fert., 109, 229–236. https://doi.org/10.1530/jrf.0.1090229 and Klotchkov and Eryuchenkov [2003]Klotchkov, D.V., Eryuchenkov, P.A. (2003). Effects of hCG on folliculogenesis and fecundity in mink (Mustela vison Scherb). Theriogenology, 60, 1583–1593. https://doi.org/10.1016/S0093-691X(03)00093-1, who claim that blastocysts from the first mating develop despite other subsequent matings. The results presented in this study show, however, that the largest number of kits in a litter originate from the second mating, which implies that many embryos from the first mating probably die during the diapause. Some portion of them, however, do survive until birth, positively contributing to the resulting litter size. Delayed implantation in mink probably plays the key role in the litter size regulation. Extended period of diapause increases embryonic mortality, and in extreme may lead to complete die out of all the embryos, which may be mistakenly taken as female barrenness. Multiple paternity in mink is not an isolated phenomenon among animals, similar effect has been observed in raccoon dogs [Ślaska and Jeżewska 2008Ślaska, B., Jeżewska, G. (2008). Bi-paternal litter in Finn raccoon (Nyctereutes procyonoides Gray 1834) detected by polymorphic DNA markers. Folia Biol. (Kraków), 56(3–4), 193–195. https://doi.org/10.3409/fb.56\_3-4.193-195] and badgers [Dugdale et al. 2007Dugdale, H.L., Macdonald, D.W., Pope, L.C., Burke, T. (2007). Polygynandry, extra-group paternity and multiple-paternity litters in European badger (Meles meles) social groups. Mol. Ecol., 16(24), 5294–5306. https://doi.org/10.1111/j.1365-294X.2007.03571.x].

Ślaska et al. [2009]Ślaska, B., Rozempolska-Rucińska, I., Jeżewska-Witkowska, G. (2009). Variation in some reproductive traits of mink (Neovison vison) according to their coat colour. Ann. Anim. Sci., 9(3), 287–297. Google Scholar confirm the observation that the number of matings is positively correlated with litter size in mink. We found that, besides the multiplicity of mating, the breeding outcomes also depend on the date of mating. The latter proved to be very significant in terms of reproduction parameters, yet the literature seems to avoid this topic or treats it without a deeper reflection. Its efficiency was tested on the average number of kits derived from different sires of contrasting (light or dark) coat colors. This was possible by using pure genetic lines of various color varieties of males and females. The results confirm data reported by Polejaeva et al. [1997]Polejaeva, I.A., Reed, W.A., Bunch, T.D., Ellis, L.C., White, K.L. (1997). Prolactin – inducted termination of obligate diapause of mink (Mustela vison) blastocystys in vitro and subsequent establishment of embryonic stem-like cells., J. Reprod. Fert., 109, 229–236. https://doi.org/10.1530/jrf.0.1090229 and Klotchkov and Eryuchenkov [2003]Klotchkov, D.V., Eryuchenkov, P.A. (2003). Effects of hCG on folliculogenesis and fecundity in mink (Mustela vison Scherb). Theriogenology, 60, 1583–1593. https://doi.org/10.1016/S0093-691X(03)00093-1, who claim that blastocysts originating from the first mating do develop despite subsequent multiple copulations. Our studies show, however, a dominance of the kits derived from the second mating, which may imply that a number of embryos from the previous conception probably die during the diapause. Some of them, though, survive and enlarge the total size of the litter. The phenomenon of delayed implantation in mink is likely to play a key role in the sizes of litters. An extended period of diapause promotes the mortality of embryos; should all of them die, this may be mistakenly taken as female sterility.

CONCLUSION

The results obtained in both the first and the second year of the experiment confirm the significance of timing and multiplicity of mating during the breeding period and confirm the desirability of mating American mink females in two dates (breeding both in the first and second date) of the breeding season. Breeding females to males of two different colour varieties on two time-separated dates produced litters consisting of two groups of kits, light and dark in color. This suggests that blastocysts derived from the first mating survive and develop, despite subsequent multiple matings to other males; kits derived from the second breeding, however, predominate in the litter.

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This Article

Received: 1 Jul 2020

Accepted: 15 Aug 2020

Published online: 2 Sep 2020

Accesses: 128

How to cite

Seremak, B., Felska-Błaszczyk, L., Dworecka-Borczyk, M., (2020). Multiple paternity in American mink: using males of different color lines allows mating efficiency evaluation. Acta Sci. Pol. Zootechnica, 19(2), 55–62. DOI: 10.21005/asp.2020.19.2.07.