Heterotic effect in two generations of experimental crossing of lines of steppe lemming, Lagurus lagurus (Rodentia, Mammalia)
Both in natural environments and during controlled breeding, animals encounter situations involving inbreeding and hybridization of inbred forms. The effects of inbreeding on individual components of fitness, such as viability and fertility, have primarily been studied in economically significant species. However, as we recognize that contrast to existing ideas about the ongoing evolution of the biosphere, degradation of the biosphere is occurring, it is essential to reevaluate the strategies for human interaction with nature. These strategies should be designed to preserve systemic organization and maintain intra- and inter-population diversity at optimal levels. When applied correctly, hybridization can serve both to establish and substantiate the species status of difficult-to-distinguish forms and to enhance valuable traits in economically important breeds while preserving the genetic diversity of domesticated animals, including rare species. To investigate the influence of intraspecific hybridization on the reproductive, behavioral, and morphological characteristics of animals, four successive cycles of inbred breeding (iF1-iF4) of the steppe lemming (Lagurus lagurus) from two distinct habitats were conducted, followed by reciprocal crossing of the resulting stocks in the hF1 and hF2 generations. Under laboratory conditions, two lines of steppe lemmings were established, bred according to a standard brother-sister scheme. The founders of these lines were descendants of animals captured in Novosibirsk Oblast: line K was sourced from the Karasuk district (forest-steppe zone of Northern Kulunda), while line CH was sourced from the Zdvinsk district (steppe areas of the Barabinskaya lowland near Lake Chany). Animals bred within each of the drains, with a random selection of pairs serving as controls, were studied. After being separated from their parents, young animals were housed in same-sex sibling groups. At the age of 1 to 1.5 months, they were individually housed. Animals that were two months old were used for breeding. The female was placed in the male's cage, and the appearance of the cubs was monitored. Each breeding pair was given the opportunity to produce up to two broods. Experimental animals were bred inbred over four successive generations. To obtain first-generation hybrids (hF1), reciprocal crossing of the descendants from two lines of the fourth generation was conducted, resulting in the formation of 32 pairs. To obtain second-generation hybrids (hF2), 20 pairs were formed among the hF1 hybrids. The weight of females, the number of live and stillborn cubs, and the growth and survival of litters until the end of the feeding period were recorded. The day after the birth of the first litter, both the female and male were assessed for parental care for 10 minutes. They were removed from the cage, and the young were relocated from the nest to the opposite corner (approximately 20 cm away). Each parent was then placed sequentially in the nest, and the time until the first pup was returned to the nest was measured. After completing double reproduction (at the age of 3 to 4 months), the animals were removed from the experiment. Body length and weight, as well as the weight of internal organs, were determined posthumously. For calculations, indices were utilized, specifically the ratio of the mass of internal organs to body weight. During inbreeding, the number of live births and the number of cubs raised to independence decreased compared to the control group, primarily due to an increase in juvenile mortality (see Fig. 1). In contrast, when two lines of steppe lemmings were hybridized, fertility increased significantly, as evidenced by a rise in both the number of live births and the number of pups raised to independence compared to those that produced inbred offspring. Body condition indicators were highest in inbred animals, which may be attributed to “favourable” housing conditions (see Fig. 5). However, reproductive rates for both males and females declined. In inbred breeding, the proportion of successfully reproducing pairs decreased significantly compared to the control group. During hybridization, this proportion returned to initial values (see Table 2). Additionally, a decrease in the relative weight of the testes in inbred males was observed, which we attribute, on one hand, to the negative effects of inbreeding and, on the other hand, to the conditions of captivity (see Fig. 4). Parental care did not diminish over four generations of inbreeding; in fact, it increased in the first two generations for both females and males when compared to the control group (see Fig. 3). This enhancement in parental care may have improved the survival chances of offspring from parents with reduced reproductive rates. The article contains 5 Figures, 2 Tables, 39 References. the authors are grateful to the teacher, Prof. Vadim Ivanovich Evsikov, who initiated this research and managed to participate in it during his lifetime, and Gulmira Tolegenovna Kokenova, with whose participation the work with animals was carried out. The Authors declare no conflict of interest.
Keywords
inbreeding,
hybridization,
heterosis,
reproductive potential,
steppe lemmingAuthors
Potapov Michael A. | Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences | vopatop@gmail.com |
Potapova Olga F. | Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences | ofpotapova@yandex.ru |
Zadubrovskiy Pavel A. | Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences; Novosibirsk State Pedagogical University | etolog@mail.com |
Zadubrovskaya Inna V. | Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences; Novosibirsk State Pedagogical University | inna_zadubrovskaya@mail.ru |
Всего: 4
References
Алтухов Ю.П. Генетика популяций и сохранение биоразнообразия // Природа. 1995. № 2. С. 27-42.
Willi Y., Kristensen T.N., Sgro C.M., Weeks A.R., 0rsted M., Hoffmann A.A. Conservation genetics as a management tool: The five best-supported paradigms to assist the management of threatened species // Proc. Natl. Acad. Sci. 2022. Vol. 119 (1). e2105076119. doi: 10.1073/pnas.2105076119.
Reed D.H., Bryant E.H. Experimental tests of minimum viable population size // Anim. Conserv. 2000. Vol. 3 (1). 7. doi: 10.1m/j.1469-r795.2000.tb00082.x.
Hedrick P.W., Kalinowski S.T. Inbreeding depression in conservation biology // Ann. Rev. of Ecol. and Systematics. 2000. Vol. 31. PP. 139-162. doi: 10.1146/annurev. ecolsys.31.1.139.
Keller L.F., Waller D.M. Inbreeding effects in wild populations // Trends Ecol Evol. 2002. Vol. 17 (5). PP. 230-241. doi: S0169-5347(02)02489-8.
Lacy R.C., Ballou J.D. Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding // Evolution. 1998. Vol. 52. PP. 900-909. doi: 10.1111/j.1558-5646.1998.tb03715.x.
Pillay N. Inbreeding in Littledale’s whistling rat Parotomys littlledalei // J. Exp. Zool. 2002. Vol. 293. PP. 171-178. doi: 10.1002/jez.10107.
Стрельцов В.В., Ильченко О.Г., Котенкова Е.В. Влияние инбридинга на репродуктивные показатели желтых пеструшек (Eolagurus luteus, Rodentia, Cricetidae) в лабораторной колонии // Зоологический журнал. 2022. Т. 101, № 9. С. 1039-1047. doi: 10.31857/S0044513422090112.
Potapov M.A., Potapova O.F., Evsikov V.I.Interstrain odor preferences and factors influencing growth rates of two strains of mice and their hybrids // Advances in Chemical Signals in Vertebrates. Boston, MA : Springer, 1999. PP. 399-406. doi: 10.1007/978-1-4615-4733-4_34.
Потапов М.А., Евсиков В.И. Генетико-физиологические взаимоотношения мать-плод и их влияние на адаптивные признаки потомков: Взгляд с третьей сторона: // Современные концепции эволюционной генетики. 2000. C. 277-293.
Потапов М.А., Потапова О.Ф., Бахвалова В.Н., Евсиков В.И. Увеличение материнского вклада как один из механизмов гетерозиса у млекопитающих // Сб. тезисов XII Международного совещания и V школы по эволюционной физиологии, Санкт-Петербург. СПб., 2001. C. 25-28.
Gerlinskaya L.A., Evsikov V.I. Influence of genetic dissimilarity of mother and fetus on progesterone concentrations in pregnant mice and adaptive features of offspring // Reproduction. 2001. Vol. 121. PP. 409-417. doi: 10.1530/rep.0.1210409.
Мейер М.Н. Метод гибридизации в систематике животных // Зоологический журнал. 1986. T. 65, № 11. C. 1605-1613.
Башенина Н.В. К вопросу о кормлении степных пеструшек при разведении их в неволе // Зоологический журнал. 1957. T. 36, № 12. C. 1882-1895.
Ченцова Н.Ю. Об адаптивном значении инбридинга для мелких грызунов // Зоологический журнал. 1969. T. 48, № 5. C. 734-745.
Литвинов Ю.Н. Элементы территориального поведения степных пеструшек, осваивающих новые стации в эксперименте // Поведение животных в сообществах: материалы Ш Всесоюзной конференции по поведению животных. М., 1983. С. 101103.
Малькова М.Г., Пальчех Н.А., Якименко В.В., Кузьмин И.В. Пространственновременная структура популяций грызунов в степной зоне Западной Сибири // Экология. 2004. № 1. С. 34-42.
Громов В.С. Взаимодействие партнеров в семейных парах и забота о потомстве у степной пеструшки (Lagurus lagurus) в лабораторных условиях // Сибирский экологический журнал. 2010. № 1. С. 181-189.
Кокенова Г.Т. Влияние брачного подбора и длительного инбредного разведения на репродуктивные характеристики степной пеструшки (Lagurus lagurus Pallas, 1773) : автореф. дис. канд. биол. наук. Новосибирск, 2007. 22 с.
Евсиков В.И., Кокенова Г.Т., Задубровский П.А., Потапова О.Ф., Потапов М.А. Моногамия как один из путей реализации адаптивного потенциала млекопитающих (на примере степной пеструшки Lagurus lagurus Pallas) // Доклады Академии наук. 2006. T. 411, № 5. C. 501-503.
Бландова З.К., Душкин В.А., Малашенко А.М., Шмидт Е.Ф. Линии лабораторных животных для медико-биологических исследований. М. : Наука, 1983. 189 c.
Назарова Г.Г., Евсиков В.И. Влияние метаболических ресурсов в период беременности у водяной полевки (Arvicola terrestris) на вторичное соотношение полов // Зоологический журнал. 2004. T. 83, № 12. C. 1488-1494.
Евсиков В.И., Потапов М.А., Потапова О.Ф. Эффекта: отбора по запаховым предпочтениям в инбредной линии могшей // Докладу: Академии наук. 2001. T. 380. C. 496-498.
Nagai J., Lee A.J., Hickman C.G. Preweaning growth of inbred, F1 hybrid, and random-bred mice as a measure of mother’s lactation // Canadian Journal of Genetics and Cytology. 1971. Vol. 13. PP. 20-28. doi: 10.1139/g71-004.
Плотников В.Г., Фирсова Н.М. Разведение, кормление и содержание кроликов. М. : Агропромиздат, 1989. 223 c.
Васеньков Д.А., Потапов М.А. Применение индекса упитанности в изучении экологии рукокрылых (Mammalia, Chiroptera) // Plecotus et al. 2007. T. 10. C. 21-31.
Стегний В.Н. Жесткий инбридинг при экстремальных режимах внешней среды-важнейший фактор микроэволюции и видообразования // Генетика. 2017. T. 53, № 7. C. 785-794.
Hedrick P.W., Garcia-Dorado A. Understanding inbreeding depression, purging, and genetic rescue // Trends Ecol. Evol. 2016. Vol. 31 (12). PP. 940-952. doi: 10.1016/ j.tree.2016.09.005.
Dorsey O.C., Rosenthal G.G. A taste for the familiar: explaining the inbreeding paradox // Trends Ecol. Evol. 2023. Vol. 38 (2). PP. 132-142. doi 10.1016/j.tree.2022.09.007.
Nagy I., Nguyen T.A. Characterizing and Eliminating the Inbreeding Load // Vet Sci. 2024. Vol. 11 (1). PP. 1-17. doi: 10.3390/vetsci11010008.
Etherington G.J., Ciezarek A., Shaw R., Michaux J., Croose E., Haerty W., Di Palma F. Extensive genome introgression between domestic ferret and European polecat during population recovery in Great Britain // J. Hered. 2022. Vol. 113 (5). PP. 500-515. doi: 10.1093/jhered/esac038.
Громов В.С. Пространственно-этологическая структура популяций грызунов. М. : Т-во научн. изданий КМК, 2008. 582 c.
Потапов М.А., Задубровская И.В., Задубровский П.А., Потапова О.Ф., Евсиков В.И. Системы брачных отношений у степной пеструшки (Lagurus lagurus) и узкочерепной полевки (Microtus gregalis) из Северной Кулунды // Экология. 2012. № 1. C. 40-44.
Терновский Д.В., Терновская Ю.Г. Экология куницеобразных. Новосибирск : Наука, 1994. 223 c.
Margulis S.W. Relationship among parental inbreeding, parental behaviour and offspring viability in old field mice // Anim. Behav. 1998. Vol. 55. PP. 427-438. doi: 10.1006/ anbe.1997.0618.
Евсиков В.И. Генетико-эволюционные аспекты проблемы гомеостаза плодовитости млекопитающих (на примере норок) // Генетика. 1987. Т. 23. C. 988-1002.
Евсиков В.И., Герлинская Л.A., Мошкин М.П., Осетрова Т.Д., Потапов М.А. Генетико-физиологические взаимоотношения мать-плод и их влияние на адаптивные признаки потомков // Онтогенез. 1998. Т. 29, № 6. C. 405-417.
Назарова Г.Г., Евсиков В.И. Влияние физического состояния матери в период беременности и лактации на постнатальный рост и репродуктивный успех потомков у водяной полевки Arvicola terrestris L // Онтогенез. 2008. Т. 39, № 2. С. 125-133.
Четвертакова Е.В. Теоретические основы селекции. Красноярск : Изд. Красноярск. гос. аграр. ун-та, 2018. 156 с.