Abstract
The development of industry and agriculture and the continuous growth of human population on Earth have dramatically increased anthropogenic pressure on natural ecosystems and wildlife. As a result, fragmentation of the natural habitats and the decrease in genetic diversity in these populations increase the probability of reproduction with genetically closely related individuals (inbreeding). However, the effect of inbreeding in felids has been studied insufficiently and data are scarce. We decided to study the effect of inbreeding on kittens’ body mass in captivity in the Eurasian lynx (Lynx lynx) colony which we keep near Moscow to study behavior and reproductive physiology of this species. This study analyzed the data on lynx kittens’ body mass in inbred and non-inbred litters. Newborn kittens’ body mass correlated negatively with the parents’ inbreeding coefficient. Inbred parents had smaller kittens at birth in comparison with non-inbred ones. These differences disappeared when kittens reached 2 months of age. It is probable that this correlates with the maternal effect (higher investment in smaller kittens) and changes in the diet of kittens.
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References
Allaine ÂD, Graziani L, Coulon J (1998) Postweaning mass gain in juvenile alpine marmots Marmota marmota. Oecologia 113:370–376. https://doi.org/10.1007/s004420050388
Ala-Honkola O, Laine L, Pekkala N, Kotiaho JS, Honkola T, Puurtinen M (2015) Males benefit from mating with outbred females in Drosophila littoralis: male choice for female genetic quality? Ethology 121:577–585. https://doi.org/10.1111/eth.12369
Alekeseeva GS, Antonevich AL, Erofeeva MN, Naidenko SV (2014) Social play in the development of sibling relations in Eurasian lynx (Lynx lynx). Biol Bull 41(4):364–371. https://doi.org/10.1134/S1062359014040025
Andersen LW, Fog K, Damgaard C (2004) Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc Biol Sci 271:1293–1302. https://doi.org/10.1098/rspb.2004.2720
Andersen IL, Nævdal E, Bøe KE (2011) Maternal investment, sibling competition, and offspring survival with increasing litter size and parity in pigs (Sus scrofa). Behavioral Ecol Sociobiol 65:1159–1167. https://doi.org/10.1007/s00265-010-1128-4
Antonevich AL, Naidenko SV (2008) Effect of sibling aggression on kittens’ behavior in Eurasian lynx Lynx lynx. Acta Zool Sin 54(1):12–19
Antonevich AL, Erofeeva MN, Naidenko CV (2012) Early sibling aggression of Eurasian lynx depends on the growth rate. Doklady Biol Scien 447:360–362. https://doi.org/10.1134/S001249661206004X
Antonevich AL, Rödel HG, Hudson R, Alekseeva GS, Erofeeva MN, Naidenko SV (2020) Predictors of individual differences in play behavior in Eurasian lynx cubs. J Zool. https://doi.org/10.1111/jzo.12761
Armbruster P, Reed DH (2005) Inbreeding in benign and stressful environments. Heredity 95:235–242. https://doi.org/10.1038/sj.hdy.6800721
Arnould JPY, Hindell MA (2002) Milk consumption, body composition and pre-weaning growth rates of Australian fur seal (Arctocephalus pusillus doriferus) pups. J Zool 256(3):351–359. https://doi.org/10.1017/S0952836902000389
Asa C, Miller P, Agnew M, Rebolledo JAR, Lindsey SL, Callahan M, Bauman K (2007) Relationship of inbreeding with sperm quality and reproductive success in Mexican gray wolves. Anim Conserv 10:326–331. https://doi.org/10.1111/j.1469-1795.2007.00116.x
Banks SC, Ward SJ, Lindenmayer DB, Finlayson GR, Lawson SJ, Taylor AC (2005) The effects of habitat fragmentation on the social kin structure and mating system of the agile antechinus, Antechinus agilis. Mol Ecol 14:1789–1801. https://doi.org/10.1111/j.1365-294X.2005.02535.x
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Barton K (2018) MuMIn: multi-model inference. R package version 1.40.4. http://CRAN.R-project.org/package=MuMIn
Beckerman AP, Benton TG, Lapsley CT, Koesters N (2006) How effective are maternal effects at having effects? Proc R Soc B Biol Sci 273:485–493. https://doi.org/10.1098/rspb.2005.3315
Beekman SPA, Kemp B, Louwmanand HCM, Colenbrander B (1999) Analyses of factors influencing the birth weight and neonatal growth rate of cheetah (Acinonyx jubatus) cubs. Zoo Biol 18:129–139. https://doi.org/10.1002/(SICI)1098-2361(1999)18:2<129::AID-ZOO4>3.0.CO;2-9
Berenos C, Ellis PA, Pilkington JG, Pemberton JM (2016) Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population. Mol Ecol 25:3152–3168. https://doi.org/10.1111/mec.13681
Berg RA, Bradley BJ, Nsubuga A, Vigilant L (2008) Effects of habitat fragmentation, population size and demographic history on genetic diversity: the Cross River gorilla in a comparative context. Am J Primatol 70(9):848–859. https://doi.org/10.1002/ajp.20559
Bowen WD, den Heyer CE, McMillan JI, Iverson SJ (2015) Offspring size at weaning affects survival to recruitment and reproductive performance of primiparous gray seals. Ecol Evol 5(7):1412–1424. https://doi.org/10.1002/ece3.1450
Breitenmoser U, Kavczensky P, Dotterer M, Breitenmoser-Wursten C, Capt S, Bernhart F, Liberek M (1993) Spatial organization and recruitment of lynx (Lynx lynx) in a rentroduced population in the Swiss Jura Mountains. J Zool 231:449–464. https://doi.org/10.1111/j.1469-7998.1993.tb01931.x
Brooker L, Brooker M, Cale P (1999) Animal dispersal in fragmented habitat: measuring habitat connectivity, corridor use, and dispersal mortality. Conserv Ecol [online] 3(1): 4. Available from the Internet. URL http://www.consecol.org/vol3/iss1/art4
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media, New York
Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. https://doi.org/10.1007/s00265-010-1029-6
Carranza J, Pérez-González J, Mateos C, Fernández-García JL (2009) Parents’ genetic dissimilarity and offspring sex in a polygynous mammal. Mol Ecol 18:4694–4973. https://doi.org/10.1111/j.1365-294X.2009.04401.x
Chen Z, Preisser EL, Xiao R, Chen J, Li D, Jiao X (2017) Inbreeding produces trade-offs between maternal fecundity and offspring survival in a monandrous spider. Animal Behav 132:253–259. https://doi.org/10.1016/j.anbehav.2017.08.020
Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270. https://doi.org/10.1046/j.1365-2540.1999.00553.x
Darwin C (1872) On the origin of species, 6th edn. New American Library Mentor, New York
Deag JM, Lawrence CE, Manning A (1987) The consequences of differences in litter size for the nursing cat and her kittens. J Zool 213:153–179. https://doi.org/10.1111/j.1469-7998.1987.tb03687.x
Dehnhard M, Fanson K, Frank A, Naidenko SV, Vargas A, Jewgenow K (2010) Comparative metabolism of gestagens and estrogens in the four lynx species, the Eurasian (Lynx lynx), the Iberian (L. pardinus), the Canada lynx (L. canadensis) and the bobcat (L. rufus). Gen compar endocr 167:287–296. https://doi.org/10.1016/j.ygcen.2010.03.023
Erofeeva MN, Naidenko SV (2012) Spatial organization of felid populations and their reproductive strategies. Biol Bull Rev 2(3):268–278. https://doi.org/10.1134/S2079086412030024
Erofeeva MN, Pavlova EV, Antonevich AL, Naidenko SV (2014) Seasonal changes in activity of males’ reproductive system in Eurasian lynx. Russ J Theriol 13(1):9–16. https://doi.org/10.15298/rusjtheriol.13.1.02
Erofeeva MN, Alekseeva GS, Sorokin PA, Naidenko SV (2018) Effect of the number of mating partners and sperm quality on reproductive success in the domestic cat (Felis catus). Biol Bull 45(7):756–765. https://doi.org/10.1134/S1062359018070063
Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258. https://doi.org/10.1111/j.1558-5646.2010.01108.x
Goritz F, Dehnhard M, Hildebrandt TB, Naidenko SV, Vargas A, Martinez F, Lopez-Bao JV, Palomares F, Jewgenow K (2009) Non cat-like ovarian cycle in the Eurasian and the Iberian lynx: ultrasonographical and endocrinological analysis. Reprod Dom Animals 44(2):87–91. https://doi.org/10.1111/j.1439-0531.2009.01380.x
Gosling LM, Baker SJ, Wright KMH (1984) Differential investment by female coypus (Myocastor coypus) during lactation. Symp Zool Soc Lond 51:273–300
Glukhov DV, Naidenko SV (2013) Seasonal variations inreproductive characteristics in teratospermic and normo-spermic male domestic cats (Felis silvestris var. catus). Zool Zh 92(10):1269–1274. https://doi.org/10.7868/S0044513413100061
Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends in Ecol Evol 31(12):940–952. https://doi.org/10.1016/j.tree
Henry P, Miquelle D, Sugimoto T, McCullough D, Caccone A, Russello MA (2009) In situ population structure and ex situ representation of the endangered Amur tiger. Mol Ecol 18:3173–3184. https://doi.org/10.1111/j.1365-294X.2009.04266.x
Heptner VG, Sludskii AA (1972) Mammals of the USSR. Carnivora, Vol. 2: hyenas and cats, Vyssh. Shk. Moscow [In Russian]
Huchard E, Knapp LA, Wang J, Raymond M, Cowlishaw G (2010) MHC, mate choice and heterozygote advantage in a wildsocial primate. Mol Ecol 19:2545–2561. https://doi.org/10.1111/j.1365-294X.2010.04644.x
Huisman J, Kruuk LEB, Ellis PA, Clutton-Brock T, Pemberton JM (2016) Inbreeding depression across the lifespan in a wild mammal population. PNAS March 29 113(13):3585–3590. https://doi.org/10.1073/pnas.1518046113
Ilmonen P, Penn DJ, Damjanovich K, Clarke J, Lamborn D, Morrison L, Ghotbi L, Potts WK (2008) Experimental infection magnifies inbreeding depression in mice. J Evol Biol 21(3):834–841. https://doi.org/10.1111/j.1420-9101.2008.01510.x
Jedrzejewski W, Jedrzejewska B, Okarma H, Schmidt K, Bunevich AN, Milkowski L (1996) Population dynamics (1869-1994), demography, and home ranges of the lynx in Bialowieza Primeval Forest (Poland and Belarus). Ecography, Copenhagen 19:122–138. https://doi.org/10.1111/j.1600-0587.1996.tb00163.x
Jewgenow K, Goritz F, Neubauer K, Fickel J, Naidenko S (2006a) Characterization of reproductive activity in captive male Eurasian lynx (Lynx lynx). J Europ Wildl Res 52(1):34–38. https://doi.org/10.1007/s10344-005-0002-6
Jewgenow K, Naidenko SV, Goeritz F, Vargas A, Dehnhard M (2006b) Monitoring testicular activity of male Eurasian (Lynx lynx) and Iberian (Lynx pardinus) lynx by fecal testosterone metabolite measurement. Gen Comp Endocrinol 149(2):151–158. https://doi.org/10.1016/j.ygcen.2006.05.015
Karlin M, Chadwick J (2012) Red wolf natal dispersal characteristics: comparing periods of population increase and stability. J Zool 286:266–276. https://doi.org/10.1111/j.1469-7998.2011.00876.x
Lacy RC, Horner BE (1997) Effects of inbreeding on reproduction and sex ratio of Rattus villosissimus. J Mammal 78(3):877–887. https://doi.org/10.2307/1382946
Laikre L, Ryman N (1991) Inbreeding depression in a captive wolf (Canis lupus). Conserv Biol 5(1):33–40. https://doi.org/10.1111/j.1523-1739.1991.tb00385.x
Lange K (1997) An approximate model of polygenic inheritance. Genetics. 147(3):1423–1430
Lariviere S, Ferguson SH (2003) Evolution of induced ovulation in North American carnivores. J Mammal 84(3):937–947. https://doi.org/10.1644/BME-003
Laws RJ, Townsend SM, Nakagawa S, Jamieson IG (2010) Limited inbreeding depression in a bottlenecked population is age but not environment dependent. J Avian Biol 41:645–652. https://doi.org/10.1111/j.1600-048X.2010.05164.x
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2019) Package “emmeans”: estimated marginal means, aka least-squares means. Compr. R Arch. Netw, 1-67
Liao W, Reed DH (2009) Inbreeding-environment interactions increase extinction risk. Anim Conserv 12:54–61. https://doi.org/10.1111/j.1365-294X.2010.04644.x
Liberg O, Andrén H, Pedersen H-C, Sand H, Sejberg D, Wabakken P, Åkesson M, Bensch S (2005) Severe inbreeding depression in a wild wolf Canis lupus. Biol Lett 1:17–20. https://doi.org/10.1098/rsbl.2004.0266
Linnell JDC, Andersen R, Kvam T, Andre H, Liberg O, Odden J, Moa PF (2001) Home range size and choice of management strategy for lynx in Scandinavia. Envir Manag 27:869–879. https://doi.org/10.1007/s002670010195
Malecot G (1969) The mathematics of heredity. Freeman, San Francisco
Margulis SW (1998) Relationships among parental inbreeding, parental behaviour and offspring viability in oldfield mice. Anim Behav 55:427–438. https://doi.org/10.1006/anbe.1997.0618
McLellan BN, Hovey FW (2001) Natal dispersal of grizzly bears. Can J Zool 79:838–844. https://doi.org/10.1139/cjz-79-5-838
Müller J, Wölfl M, Wölfl S, Dennis W, Hothorn T, Heurich M (2014) Protected areas shape the spatial distribution of a European lynx population more than 20 years after reintroduction. Biol Conserv 177:210–217. https://doi.org/10.1016/j.biocon.2014.07.007
Murphy AD, Goedert D, Morris MR (2014) Maternal effects are long-lasting and influence female offspring’s reproductive strategy in the swordtail fish Xiphophorus multilineatus. J Evol Biol. https://doi.org/10.1111/jeb.12414
Naidenko SV (1998) Interrelations of animals in family groups and possible reasons of litters dissolution in lynxes (Lynx lynx, Carnivora, Felidae). Zool Zh 77(11):1317–1320
Naidenko SV (2005) Traits of reproduction and postnatal development of Eurasian lynx. KMK Scientific Press, Moscow [in Russian]
Naidenko SV (2006) Body mass dynamic in Eurasian lynx Lynx lynx kittens during lactation. Acta Theriol 51(1):91–98. https://doi.org/10.1007/BF03192660
Naidenko S, Antonevich A, (2009) Sibling aggression in Eurasian lynx (Lynx lynx). Iberian lynx ex situ conservation: an interdisciplinary approach. A Vargas, C Breitenmoser, U Breitenmoser – Fundación Biodiversidad IUCN Cat Specialist Group: 146–155
Naidenko SV, Erofeeva MN (2004) Reproduction Eurasian Lynx Lynx lynx (Felida, carnivore) in traits of females’ reproductive strategies. Zool Zh 83(2):261–269 [in Russian]
Naidenko S, Erofeeva M, Goritz F, Neubauer K, Fickel J, Jewgenow K (2007) Eurasian lynx male reproductive success with multi-male mating in captivity. Acta Zool Sin 53(3):408–416
Neubauer K, Jewgenow K, Blottner S, Wildt DE, Pukazhenti BS (2004) Quantity rather than quality in teratospermic males: a histomorphometric and f low cytometric evaluation of spermatogenesis in the domestic cat. Biol Reprod 71(5):1524–1571
Nilsen EB, Linnell JDC, Odden J, Samelius G, Andrén H (2012) Patterns of variation in reproductive parameters in Eurasian lynx (Lynx lynx). Acta Theriol 57(3):217–223. https://doi.org/10.1007/s13364-011-0066-5
Nowell K, Jackson P (1996) Wild cats: status survey and conservation action plan. IUCN/SSC Cat Specialist Group, Gland
Oliehoek PA, Windig JJ, van Arendonk JAM, Bijma P (2006) Estimating relatedness between individuals in general populations with a focus on their use in conservation programs GENETICS May 1, vol. 173 no. 1 483–496; https://doi.org/10.1534/genetics.105.049940
Painer J, Goeritz F, Dehnhard M, Hildebrandt TB, Naidenko SV, Sánchez I, Quevedo Muñoz MA, Jewgenow K (2014) Hormone-induced luteolysis on physiologically persisting Corpora lutea in Eurasian and Iberian Lynx (Lynx lynx and L. pardinus). Theriogenology 82(4):557–562. https://doi.org/10.1016/j.theriogenology.2014.05.004
Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Amer Nat 128:573–592
Pemberton JM, Ellis PE, Pilkington JG, Bérénos C (2017) Inbreeding depression by environment interactions in a free-living mammal population. Heredity 118:64–77. https://doi.org/10.1038/hdy.2016.100
Pilorz V, Jäckel M, Knudsen K, Trillmich F (2005) The cost of a specific immune response in young guinea pigs. Physiol Behav 85:205–211. https://doi.org/10.1016/j.physbeh.2005.04.008
Pribbenow S, Jewgenow K, Vargas A, Serra R, Naidenko S, Dehnhard M (2014) Validation of an enzyme immunoassay for the measurement of faecal glucocorticoid metabolites in Eurasian (Lynx lynx) and Iberian lynx (Lynx pardinus). Gen Comp Endocrinol 206:166–177. https://doi.org/10.1016/j.ygcen.2014.07.015
Pukazhenti BS, Neubauer K, Jewgenow K, Howard JG, Wildt DE (2006) The impact and potential etiology of teratospermia in domestic cat and its wild relatives. Theriogenology 66(1):112–121. https://doi.org/10.1016/j.theriogenology.2006.03.020
Ralls K, Ballou J (1982a) Effect of inbreeding on juvenile mortality in some small mammal species. Lab Anim 16:159–166. https://doi.org/10.1258/002367782781110151
Ralls K, Ballou J (1982b) Effects of inbreeding on infant mortality in captive primates. Inter J Primat 3:491–505. https://doi.org/10.1007/BF02693747
Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol 2:185–193. https://doi.org/10.1111/j.1523-1739.1988.tb00169.x
Reed DH, Fox CW, Enders LS, Kristensen TN (2012) Inbreeding-stress interactions: evolutionary and conservation consequences. Ann N Y Acad Sci 1256:33–48. https://doi.org/10.1111/j.1749-6632.2012.06548.x
Reid JM, Arcese P, Keller LF, Elliott KH, Sampson L, Hasselquist D (2007) Inbreeding effects on immune responsein free-living song sparrows (Melospiza melodia). Proc Biol Sci 274:697–706. https://doi.org/10.1098/rspb.2006.0092
Reznick D, Callahan H, Llauredo R (1996) Maternal effects on offspring quality in poeciliid fishes. Am Zool 36:147–156
Samelius GH, Andrén O, Liberg JD, Linnell C, Odden J, Ahlqvist P, Segerström P, Sköld K (2012) Spatial and temporal variation in natal dispersal by Eurasian lynx in Scandinavia. J Zool 286:120–130. https://doi.org/10.1111/j.1469-7998.2011.00857.x
Sardell RJ, Kempenaers B, Duval EH (2014) Female mating preferences and offspring survival: testing hypotheses on the genetic basis of mate choice in a wild lekking bird. Mol Ecol 23:933–946. https://doi.org/10.1111/mec.12652
Say L, Pontier D, Natoli E (1999) High variation in multiple paternity of domestic cat (Felis catus L.) in relation to environmental conditions. Proc Biol Sci 266:2071–2074. https://doi.org/10.1098/rspb.1999.0889
Schrader M, Travis J (2012) Assessing the roles of population density and predation risk in the evolution of offspring size in populations of a placental fish. Ecol Evol 2:1480–1490. https://doi.org/10.1002/ece3.255
Shen HP, Lee LL (2000) Mother-young interactions in a maternity colony of Myotis formosus. J Mammal 81(3):726–733. https://doi.org/10.1644/1545-1542(2000)081<0726:MYIIAM>2.3.CO;2
Schmidt K (1998) Maternal behaviour and juvenile dispersal in the Eurasian lynx. Acta Theriol 43:391–408
Schmidt K, Davoli F, Kowalczyk R, Randi E (2016) Does kinship affect spatial organization in a small and isolated population of a solitary felid: the Eurasian lynx? Integr Zool 11(5):334–349. https://doi.org/10.1111/1749-4877.12182
Sikes RS (1998) Tradeoffs between quality of offspring and litter size: differences do not persist into adulthood. J Mammal 79(4):1143–1151. https://doi.org/10.2307/1383005
Sindicic M, Polanc P, Gomercic T, Jelencic M, Huber D, Trontelj P, Skrbinsek T (2013) Genetic data confirm critical status of the reintroduced Dinaric population of Eurasian lynx. Conserv Gen 14:1009–1018. https://doi.org/10.1007/s10592-013-0491-x
Sokolov VE, Naidenko SV, Serbenyuk MA (1994) Specific fights of young lynxes (Felis lynx, Carnivora, Felidae). Zool Zh 73(11):132–136 [in Russian]
Sokolov VE, Naidenko SV, Serbenyuk MA (1995) Marking bahaviour of European lynx (Felis lynx, Felidae, Carnivora) Izv RAS 3: 345–355. [in Russian]
Sokolov VE, Naidenko SV, Serbenyuk MA (1996) The recognition of species, sex and age of conspecifics, familiar and non-familiar individuals by European lynxes (Felis lynx, Felidae, Carnivora) by odor signals of urine Izv RAS 5: 487-494. [in Russian]
Sorokin PA, Rozhnov VV, Krasnenko AU, Lukarevskiy VS, Naidenko SV, Hernandez-Blanco JA (2016) Genetic structure of the Amur tiger (Panthera tigris altaica) population: are tigers in Sikhote-Alin and southwest Primorye truly isolated? Integr Zool 11:25–32. https://doi.org/10.1111/1749-4877.12175
Stehlik J (2000) Reproductive biology of the European lynx, Lynx lynx (Linnaeus, 1758) at Ostrava zoo. Zool Garten NF 70(6):351–360
Stow AJ, Sunnucks P (2004) Inbreeding avoidance in cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13:443–447. https://doi.org/10.1046/j.1365-294X.2003.02060.x
Team RDC (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Trinkel M, Cooper D, Packer C, Slotow R (2011) Inbreeding depression increases susceptibility to bovine tuberculosis in lions: an experimental test using an inbred-outbred contrast through translocation. J Wildl Dis 47(3):494–500. https://doi.org/10.7589/0090-3558-47.3.494
Uphyrkina O, Miquelle D, Quigley H, Driscoll C, O’Brien SJ (2002) Conservation genetics of the far eastern leopard (Panthera pardus orientalis). J Heredity 93(5):303–311. https://doi.org/10.1093/jhered/93.5.303
Vitikainen EIK, Haag-Liautard C, Sundström L (2015) Natal dispersal, mating patterns, and inbreeding in the ant Formica exsecta. Am Nat 186:716–727. https://doi.org/10.1086/683799
Walling CA, Nussey DH, Morris A, Clutton-Brock TH, Kruuk LEB, Pemberton JM (2011) Inbreeding depression in red deer calves. BMC Evol Biol 11:318. https://doi.org/10.1186/1471-2148-11-318
Wiegand T, Revilla E, Moloney KA (2005) Effects of habitat loss and fragmentation on population dynamics. Conserv Biol 19(1):108–121. https://doi.org/10.1111/j.1523-1739.2005.00208.x
Wildt DE, Bush M, Goodrowe KL, Packer C, Pusey AE, Brown JL, Joslin P, O’Brien SJ (1987) Reproductive and genetic consequences of founding lion populations. Nature 329:328–331. https://doi.org/10.1038/329328a0
Winternitz J, Abbate JL, Huchard E, Havl J, Cek I, Garamszegi LZ (2017) Patterns of MHC-dependent mate selection in humans and nonhuman primates: a meta-analysis. Mol Ecol 26:668–688. https://doi.org/10.1111/mec.13920
Yerga J, Calzada J, Manteca X, Vargas A, Rivas A (2014) Early development and growth in captiveborn Iberian Lynx (Lynx pardinus). Zoo Biol 33:381–387. https://doi.org/10.1002/zoo.21148
Yamane A (1998) Male reproductive tactics and reproductive success of the group living cat (Felis catus). Behav Proc 43:239–249. https://doi.org/10.1016/S0376-6357(98)00018-7
Zheltukhin AS (1984) Diurnal activity and the size of lynx habitats in the southern taiga of the upper Volga. Byul MOIP Otd Biol 89(1):54–62 [in Russian]
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We are very grateful to our colleagues A. Antonevich, E. Pavlova, G. Alekseeva, and A. Krylovich for their help in animal keeping and data collection.
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This study was supported by the Russian Science Foundation (18-14-00200).
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Erofeeva, M.N., Vasilieva, N.A. & Naidenko, S.V. Effect of inbreeding on kittens’ body mass in Eurasian lynx (Lynx lynx). Mamm Res 65, 545–554 (2020). https://doi.org/10.1007/s13364-020-00495-x
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DOI: https://doi.org/10.1007/s13364-020-00495-x