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. 2024 Sep 12;71(3):329–337. doi: 10.1093/cz/zoae051

Long-term effect of inbreeding in the yellow steppe lemming, Eolagurus luteus, captive colony

Vladimir V Streltsov 1,✉, Olga G Ilchenko 2, Elena V Kotenkova 3
Editor: Maria Servedio
PMCID: PMC12227421  PMID: 40620595

Abstract

In the current research, we investigated the impact of gradually increasing inbreeding on the life span and reproductive rate of yellow steppe lemmings, Eolagurus luteus, that reproduced in the Moscow Zoo. The focal captive colony existed from 2017 to 2021. The studied animals belonged to the second to tenth generations. The founders of the colony were 5 females and 5 males originating from 3 females and 4 males livetrapped in the Zaisan basin (Kazakhstan). The degree of their descendant relatedness progressively increased. The animals intended to be used for reproduction were distributed to pairs with unfamiliar partners. We constructed the pedigree of 177 individuals and calculated their inbreeding coefficients. This parameter varied from 0 to 0.29, and the maximum values were registered in the lemmings of the seventh to tenth generations. We measured the life span of 61 individuals and used information about the reproduction or its absence in 45 pairs. A substantial decline in individual life span and reproductive parameters in the breeding pairs, along with a progressive increase in the inbreeding coefficients, was registered. The number of delivered litters, born pups, and young lived up to the age of puberty significantly depended on the level of mother inbreeding. The noticeable traits of inbreeding depression in the colony appeared in 2019–2020 when the offspring inbreeding coefficients reached approximately 0.2. Therefore, we assume that if the E. luteus population originates from a relatively small number of noninbred and unfamiliar individuals, then successful reproduction without significant inbreeding depression will continue for several generations of offspring.

Keywords: Arvicolinae, Eolagurus luteus, inbreeding coefficient, inbreeding depression, life span, reproductive parameters

The term “inbreeding” usually means that the breeding partners are more closely related than 2 randomly chosen mates. Inbreeding commonly results in an increased frequency of homozygotes for alleles identical by descent and a reduction in individual fitness (i.e., inbreeding depression; Crow and Kimura 1970; Keller and Waller 2002). Inbreeding depression is assumed to significantly influence the evolution of animal mating systems (Charlesworth and Charlesworth 1987; Charlesworth and Willis 2009). This is the reason why the estimation of the degree of inbreeding in the populations of mammals, including rodents, is an extremely important issue of reproductive biology. It is also necessary to investigate the negative consequences of inbreeding for the stability and productivity of animal populations. The impact of inbreeding manifests at both genetic and phenotypic levels. The high degree of inbreeding in populations of the majority of animal species results in an increase in infant mortality and decline in fecundity. Inbred individuals are more sensitive to diseases, predation, and environmental stress factors (Crnokrak and Roff 1999; DeRose and Roff 1999; Keller and Waller 2002). The immunity of inbred offspring is reduced due to the homozygotization and reduction in the variety of major histocompatibility complex (MHC) genes. Highly polymorphic MHC genes code proteins presenting pathogen-derived antigens to T-cells, that is, gene products of MHC play a crucial role in initiating the adaptive immune response (Potts and Wakeland 1993; Potts et al. 1994; Sommer 2005; Radwan et al. 2010). The depletion in variation at MHC and, consequently, less resistance of offspring to pathogens is a frequent manifestation of the population bottleneck in threatened animal species, such as cheetah, Acinonyx jubatus (O’Brien et al. 1985), giant panda, Ailuropoda melanoleuca (Zhu et al. 2007), and Galapagos penguin, Spheniscus mendiculus (Bollmer et al. 2007). At the same time, inbreeding results in increased homozygosity by loci carrying detrimental or lethal recessive alleles. These alleles are generally presented at low frequencies in population gene pools (Charlesworth and Willis 2009).

The individual degree of inbreeding is estimated by Wright’s coefficient of inbreeding calculated by the formula, which takes the amount of ancestry shared by the parents of inbred offspring, a number of generations from sire and dam, respectively, to the common ancestor and inbreeding coefficient of this ancestor into account (Wright 1922, 1950). The inbreeding coefficient measures the proportion by which the heterozygosity has been reduced. It is defined as the probability of autozygosity (presence of 2 homologous alleles identical by descent) by a certain locus. The inbreeding coefficient ranges from 0 in a randomly mating population to 1, which indicates complete homozygosity (Crow and Kimura 1970). Coefficients of inbreeding are regularly calculated for different agricultural animals, especially dairy cattle, to avoid inbreeding and adjustment for genetic variance (Wiggans et al. 1992; Panetto et al. 2010; Abanikannda and Olutogun 2019). Besides the farm animals, a huge amount of data concerning the inbreeding in the animal populations was obtained during the investigation of the laboratory (Brodkin et al. 1998; Woodworth et al. 2002) and zoo (Ralls and Ballou 1982a, b, 1983; Ralls et al. 1988; Brewer et al. 1990; Lacy 1993; Lacy et al. 1996) animals.

Apparently, the evolution of mechanisms of kin recognition and inbreeding inhibition (incest taboo) accompanies the demographic structure complication of animal social groups and populations (Pusey and Wolf 1996). In most social species, the propensity of individuals to mate with unrelated partners and assess them largely determine the level of reproductive skew in the groups (Harvey and Ralls 1986; Wolff 1992; Emlen 1995; Clarke et al. 2001; Lukas and Clutton-Brock 2012). Most animals including rodents avoid inbreeding but at varying degrees. Even closely related species may differ in their propensity to consanguineous breeding (Bollinger et al. 1991; Pillay 1998; Clarke and Faulkes 1999; Zorenko and Kaprale 2003; Nichols 2017). The differences may be determined by the reproductive strategy of certain species (Gromov 2008). The representatives of the subfamily Arvicolinae (Rodentia, Cricetidae) are among the most promising objects for the investigation of various aspects of mammal reproduction and population ecology including the long-term effect of inbreeding. This subfamily includes voles, lemmings, and muskrats. It comprises more than 150 species (Wilson and Reeder 2005) that display a wide diversity of social structures and reproductive systems. Correspondingly, their propensity to inbreeding varies (Zorenko and Kaprale 2003; Gromov 2008, 2017). According to the hypothesis valid for rodents, including voles, the incest taboo maintenance mechanisms are more developed in monogamous than in polygamous species and subspecies (Zorenko and Kaprale 2003; Kokko and Ots 2006; Smorkatcheva 2021; Zorenko and Kaija 2024). In theory, monogamy, in combination with strong pair bonds and pronounced paternal care of offspring, promotes the more intensive development of these mechanisms (Ferkin 1990; Lehmann and Perrin 2003; Parker 2006).

One of the exceedingly poorly studied species of Arvicolinae is yellow steppe lemming, Eolagurus luteus (Eversmann 1840). This is a rather large (adult body mass is on average 100–102 g) rodent inhabiting the deserts and semi-deserts of the eastern part of Kazakhstan and northwestern parts of Mongolia and China (Shubin 1978; Sokolov and Orlov 1980; Gromov and Erbaeva 1995; An et al. 2023). Field data obtained for this species in the second half of the 20th century suggest the monogamy and formation of family groups that include a pair of adults and young. Males presumably remain with the females and pups during lactation and early post-weaning period (Shubin 1978).

The range of E. luteus has been steadily reducing since the Late Pleistocene. Yellow steppe lemming inhabited the mammoth steppe-tundra of Pleistocene Eastern Europe and Siberia and later became extinct in most part of the range (Shubin 1978; Dupal 2005). The sharp decrease in the E. luteus range in the Holocene supposedly occurred for a reason of climate warming and humidity raising, which resulted in the loss of arid and periglacial landscapes. However, until the middle 19th century, yellow steppe lemming was still widespread in Kazakhstan and the Caspian region. In the second half of the 19th century, E. luteus became extinct in most of this range, presumably remaining only in the Zaisan basin (East Kazakhstan) (Shubin 1978; Gromov and Erbaeva 1995; Dupal 2005). Plague epizootics (Lobachev 1966; Dupal 2005) and significant glaciations of forage lands occurred in severe winters (Shubin 1978) were the potential reasons for this extinction. It may also have been to some degree connected with inbreeding (Dupal 2005). It should be mentioned that the suitable area for E. luteus in Xinjiang (China) has also been decreasing in recent years due to climate change and may become almost completely missing by the 2050s (An et al. 2023).

The number of yellow steppe lemmings in Kazakhstan remains low. This species is listed in the Red Data Book of the Republic of Kazakhstan (Shaimardanov 2010). The territory of the former Soviet Union inhabited by E. luteus is situated on the periphery of its range. The optimum of the range is presumably located in Mongolia (Ismagilov and Bekenov 1969; Shubin 1978). According to the hypothesis of Ismagilov and Bekenov (1969), the natural population of yellow steppe lemmings in the Zaisan basin originates from a relatively small number of animals dispersed from Dzungaria (northern part of Xinjiang). It is supposedly impossible to maintain a sustainable population in this area without mating with animals regularly dispersing from the territory of China. At least in the 60s and 70s of the 20th century, the number of lemmings in the Zaisan basin abruptly fluctuated from massive reproduction (up to 13 colonies per 1 ha) to almost complete extinction caused by adverse climatic conditions. The researchers revealed significant variations in the ecology and behavior of E. luteus depending on the population density (Ismagilov and Bekenov 1969; Shubin 1978).

The reduction in the range and fluctuations in the number supposedly put the lemmings in front of the problem of forced inbreeding. Accordingly, we assume that at least part of E. luteus individuals that inhabit the Zaisan basin are inbred to a certain extent. However, in the case that 2 partners are in a certain degree of relatedness but originate from different families, they can successfully reproduce. Therefore, the purpose of the current research is to assess the long-term increase in the degree of inbreeding in the yellow steppe lemming captive colony that originates from a few individuals and evaluate the effect of inbreeding on the animal lifespan, reproductive parameters, and offspring viability.

Materials and Methods

Animals and housing conditions

The archive data analyzed in the current research were obtained at the Experimental Department of Small Mammals of the Moscow Zoo. We used information referring to the E. luteus captive colony that existed from 2017 to 2021. The focal animals belonged to the second to tenth laboratory generations. They originated from 3 females and 4 males livetrapped in the Zaisan basin (East Kazakhstan region, Kazakhstan). These animals were captured from burrows located at a considerable distance from one another and, thus, most probably unrelated to each other. The colony founders received from nature were subsequently distributed into 4 pairs. One of the females was successively paired with 2 different males. Their descendants of the first generation were born in Saint Petersburg State University. Of these descendants, 10 animals (5 females and 5 males) born in August 2017 and originating from different family groups were later transported to the Moscow Zoo. Five of them (4 females and 1 male) were the offspring of the above-mentioned female consecutively mated with 2 males. Each of the 10 lemmings was paired with an unrelated and unfamiliar partner.

Monogamy is supposed to be a preferable mating system for yellow steppe lemmings under natural conditions (Shubin 1978). Hence, all animals intended to be used for further reproduction were distributed in pairs. For pair formation, we chose the healthy (without any visible signs of disease) and sexually mature males and females of both young and older age (age at the moment of pair establishing: females—from 25 to 701 days, males—from 34 to 691 days). Focal pairs existed until one of the partners died. The founders of each newly established pair originated from different family groups. Females were weighed weekly until pregnancy detection; after that, they were checked daily until offspring delivery. Lemmings were housed in glass chambers (100 × 50 × 35 cm size) provided with 2 wooden nest-boxes (20 × 15 × 15 cm size), according to the number of breeding animals. Wood sawdust and hay were used as bedding and material for nest building. Cages were cleaned every 3–4 weeks. Fresh carrots and grain mixture consisting of millet, rolled oats, linseed, canary, and hemp seed were provided ad libitum; the diet was seasonally supplemented with tree branches and green grass. All animals were maintained under natural lighting and at a constant temperature of 20 ± 2 °C. Young lemmings were removed from their natal groups at the age of 20–50 days. Each lemming was assigned an individual number.

Data analysis

According to the data about the focal animals’ relatedness and reproduction specified in the computer database, we constructed the pedigree of 177 individuals born in 2017–2021 and calculated their inbreeding coefficients (Fx; hereafter, IC) using Wright’s formula (Wright 1922). We performed this estimation using the GeneticsPed library (Gorjanc et al. 2022) in the R 4.3.1 environment. The inbreeding coefficients of colony founders were assumed by default as zero. We measured the life span of 61 individuals and used information about the reproduction or its absence obtained for 45 pairs (the exact number of females is 37, number of males is 34) of lemmings. Eight females and 10 males were repeatedly paired after their previous partners’ deaths (most of these animals had changed 2 partners, but one of the males was successively paired with 3 females). For each pair of successfully delivered offspring, we calculated a total number of litters, born, and survived (lived up to 30 days) pups. Given the minimum latency to the first litter in the yellow steppe lemming lasts 18 days and the minimum period of pair existence during which it is possible to raise at least 1 litter is 38 days (Streltsov et al. 2023), we excluded pairs that existed less than 40 days from the analysis.

For a precise assessment of the effect of inbreeding, the model selection, along with examining the confidential intervals (CI) for parameter estimates, was performed. We applied a linear model (LM) to examine the impact of the IC on the life span (number of days) of E. luteus individuals. Generalized linear models (GLMs) with negative binomial distribution in the MASS library (Venables and Ripley 2002) were applied to analyze the effects of IC of male and female breeders separately on the total number of litters, born and survived pups reproduced by each pair. To test the influence of multiple factors, we ranked sets of candidate models with all combinations of predictors including the interaction between parental inbreeding coefficients using Akaike’s information criterion (AIC) corrected for small samples (AICc; Burnham and Anderson 2004) in the MuMIn library (Barton 2020). The ΔAICc values and Akaike weights (wi) were calculated to infer support for each of the candidate models. The model with the lowest AICc and ΔAICc = 0 was considered to be the most parsimonious. The coefficient estimates (β-coefficients) with their errors were averaged for models within 2 units of the top model (ΔAICc ≤ 2; Burnham et al. 2011) using the AICcmodavg library (Mazerolle 2020). We used 95% confidential intervals (95% CI) to assess the significance of the effects. We based our interpretations of the relative influence of all predictors on whether or not the 95% CI spanned zero. The significance of the influence of predictors was assessed in accordance with the P-value (P ≤ 0.001—“strong effect”; 0.001 < P ≤ 0.01—“medium effect”; 0.01 < P ≤ 0.05—“weak effect”; P > 0.05—“no effect”). All statistical analyses were conducted using the R version 4.3.1.

Results

Estimation of inbreeding coefficients

The IC of yellow steppe lemming individuals in the Moscow Zoo captive colony varied from 0 to 0.29. The IC was equal to zero in all focal animals of the second and third generations. This value reached 0.2 in the offspring of the sixth generation. The maximum values of IC (0.25–0.29) were registered in the animals of seventh to tenth generations born in 2019–2021. The IC equal to 0.28–0.29 was calculated for only 3 lemmings who belonged to the eighth generation and were born in August–December 2020. The mean value of IC was the highest in the offspring of the ninth generation born in 2020–2021 (mean IC: 0.21 ± 0.004; the total number of individuals is 54). After that, in the offspring of the tenth generation born in 2021, a slight decrease in the degree of inbreeding occurred (mean IC: 0.19 ± 0.009; the total number of animals is 20) (Figure 1). The inbreeding coefficients of females kept in pairs varied from 0 to 0.29, and the IC of male partners—from 0 to 0.26.

Figure 1.

Alt text: This figure represents the variation in the inbreeding coefficients of yellow steppe lemming individuals of the Moscow Zoo captive colony depending on the generation of offspring. The investigated animals belonged to the generations from second to tenth. Boxes indicate 25% and 75% quartiles, midlines are medians, and whiskers indicate minimum and maximum values excluding any outliers. Points indicate outliers.

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Variation in the inbreeding coefficients (IC) of yellow steppe lemming, E. luteus, individuals of the Moscow Zoo captive colony depending on the generation of offspring. Number of individuals with estimated IC belonged to each generation: 2nd—10, 3rd—21, 4th—12, 5th—9, 6th—16, 7th—13, 8th—22, 9th—54, 10th—20. Boxes indicate 25% and 75% quartiles, midlines are medians, and whiskers indicate minimum and maximum values excluding any outliers. Points indicate outliers.

Life span of individuals

The life span of yellow steppe lemming individuals ranged from 30 to 1,002 days (mean: 499.4 ± 27.8 days). The maximum life span (747–1,002 days) was observed in 4 females and 5 males born in August–November 2017. Their IC was equal to zero. The minimum life span (30–194 days) was registered in 3 females and 1 male, whose IC varied from 0.17 to 0.2. Our results confirmed a strong negative correlation between the IC of individuals and their duration of life (β = –1064.93 ± 261.56; 95% CI: –1588.31 to –541.54; t = –4.07; P = 0.0001). We revealed a substantial decline in the animal life span with a progressive increase in the degree of inbreeding in the colony (Figure 2).

Figure 2.

Alt text: This figure displays the decrease in the life span of the yellow steppe lemming individuals with a progressive increase of the animal inbreeding coefficients in the Moscow Zoo captive colony from 2017 to 2021. The life span is in linear dependence on the inbreeding coefficient. Points indicate the exact values of individual life span, and a regression line displays the change in the life span depending on the individual coefficient of inbreeding. Dotted lines indicate 95% confidence intervals.

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Decrease in the life span of the yellow steppe lemming, E. luteus, individuals with a progressive increase in the animal inbreeding coefficients (IC) in the Moscow Zoo captive colony, 2017–2021. Points indicate the exact values of the individual life span, and a regression line displays the change in the life span depending on the individual IC. The dotted lines indicate 95% confidential intervals.

Reproductive parameters

In 8 of 45 pairs (18%), animals did not have offspring. In pairs successfully delivered offspring, the total number of litters reproduced by each pair ranged from 1 to 23 (mean: 7.4 ± 0.9). Two top-ranked models with a number of litters as a dependent variable included male and female IC and interaction between parental inbreeding coefficients. The total wi of the models was 0.87 (Table 1). Female IC had a negative, interaction between inbreeding coefficients of male and female had a positive, and male IC did not have a significant effect on the number of litters (Table 2). The total number of born pups in each pair varied from 1 to 70 (mean: 22.8 ± 3.08). Respectively, the total number of pups survived up to the weaning age (30 days) ranged from 0 to 61 (mean: 19.9 ± 2.8). Two top-ranked models with a number of born pups as a dependent variable also included male and female IC and interaction between parental inbreeding coefficients. The total wi of the models was 0.78 (Table 1). Female IC had a weak negative, and interaction between inbreeding coefficients of male and female had a weak positive effect, whereas male IC had no effect on the number of born pups (Table 2). The 2 most parsimonious models with a number of survived pups as a dependent variable were constructed. The total wi of these models was 0.77 (Table 1). Female IC had a negative, and interaction between male and female inbreeding coefficients had a weak positive effect, whereas the impact of male IC was insignificant (Table 2). Thus, the increase in the level of inbreeding of female breeders in the captive colony has a pronounced negative impact on the reproductive rate. The effect of this factor is enhanced if, in parallel with it, the degree of inbreeding of male breeders increases.

Table 1.

Competing top-ranked (ΔAICc ≤ 2) models of the effects of male and female inbreeding coefficients on the reproductive parameters of yellow steppe lemmings, E. luteus, in the Moscow Zoo captive colony, 2017–2021

Model AICc ΔAICc w i K Deviance
Total number of litters (mean: 7.4 ± 0.9)
FxF + FxM + FxF × FxM 210.95 0 0.57 5 –99.5
FxF 212.21 1.26 0.3 3 –102.74
Total number of born pups (mean: 22.8 ± 3.08)
F x F 301.73 0 0.39 3 –147.5
F x F + FxM + FxF × FxM 301.74 0.01 0.39 5 –144.9
Total number of survived pups (mean: 19.9 ± 2.8)
F x F 292.3 0 0.53 3 –142.79
FxF + FxM + FxF × FxM 293.9 1.6 0.24 5 –140.99
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Abbreviations: FxF: female inbreeding coefficient; FxM: male inbreeding coefficient; K: number of parameters.

Table 2.

Impact of inbreeding coefficients of male and female breeders on the reproductive parameters of yellow steppe lemmings (Eolagurus luteus) in the Moscow Zoo captive colony, 2017–2021

Covariate β ± SE 95% CI P-value Effect
Total number of litters (mean: 7.4 ± 0.9)
FxF −4.96 ± 1.75 −8.47 to −1.45 0.006 Negative
FxM −4.53 ± 2.53 −9.6 to 0.54 0.08 No effect
FxF*FxM 34.75 ± 12.73 8.86 to 60.66 0.008 Positive
Total number of born pups (mean: 22.8 ± 3.08)
FxF −4.74 ± 1.89 −8.55 to −0.93 0.015 Weak negative
FxM −4.6 ± 3.1 −10.8 to 1.59 0.1 No effect
FxF*FxM 38.2 ± 15.07 7.55 to 68.86 0.015 Weak positive
Total number of survived pups (mean: 19.9 ± 2.8)
FxF −5.2 ± 1.82 −8.87 to −1.54 0.005 Negative
FxM −3.73 ± 3.12 −9.97 to 2.51 0.24 No effect
FxF*FxM 35.21 ± 16.58 1.48 to 68.95 0.04 Weak positive
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Averaged coefficient estimates (regression coefficient β with SE) and confidence intervals (CI) are taken from the best-approximating models (Table 1) containing parameters: FxF, female inbreeding coefficient; FxM, male inbreeding coefficient.

Discussion

In the current study, the calculation of individual inbreeding coefficients provides precise information about the progressive accumulation of inbreeding in the focal zoo colony of E. luteus and the level of inbreeding, on reaching which the significant signs of inbred depression began to manifest in the colony. We revealed that the sufficient decrease in the reproductive parameters (total number of litters and born pups per 1 pair) and pup survival accompanied the abrupt increase in the offspring IC (up to approximately 0.2), which occurred in 2019–2020 (during this period, the sixth–ninth generation of offspring was obtained). In the preceding years (2017–2018), more than 90% of young successfully lived up to the age of puberty. Incidentally, the IC equal to 0.25 is equivalent to that calculated for offspring produced during father-daughter, mother-son, or full-sibling mating (Ralls and Ballou 1982a; Ralls et al. 1988). A progressive increase in the individual IC is also negatively correlated with the life span of lemmings. A certain decrease in the degree of inbreeding of individuals of the tenth generation occurred in 2021 may be explained by the minor adjustment in the process of establishing the animal pairs. Female lemmings chosen for further reproduction were slightly less inbred (mean IC of dams: 2020—0.193 ± 0.02; 2021—0.187 ± 0.04) and, whenever possible, less related to the male partners.

The results presented in this paper supplement our previously published data on the comparison of the focal E. luteus colony (data for the focal colony provided in our previous paper exclude that obtained in 2021) and a population, which was kept in the Moscow Zoo in 2008–2016 and differed from the focal colony in the degree of relatedness of breeding partners. It must be noted that the estimation of individual coefficients of inbreeding was not carried out during previous research. The comparison showed that although both zoo colonies suffered the negative impact of inbreeding the much more pronounced inbreeding depression occurred in the first colony, which originated from only 3 livetrapped animals. It manifested even in the early stages of the first population’s existence. Actually, all members of the colony were inbred. This feature resulted in much lower reproductive parameters compared with the focal (second) colony. For example, the proportion of successfully reproduced females was almost one and a half times less, and a mean number of litters per 1 pair—almost 5× less. The life span of dams was almost 1.8× shorter. Besides that, the lemmings of the first colony, especially since the 15th generation, were much less resistant to diseases. The mass mortality of infants and adults occurred in 2013–2015. By October 2016, the colony had been completely missing (Streltsov et al. 2023).

The distribution of E. luteus subfossilized remains suggests the reinforced fragmentation of its range during the Late Pleistocene–Early Holocene induced by climate changes. It presumably resulted in numerous isolations of the yellow steppe lemming small populations and population bottlenecks. It is known that lemmings from different isolated populations, which existed during the Holocene significantly differed from each other in the dimensions of the skull (Lobachev 1966). Herewith the interpopulation variability on this trait during the Pleistocene was weak, although phenotypic variability was generally higher than in the Holocene (Dupal 2005). Many isolated Holocene populations later became extinct (Lobachev 1966; Ismagilov and Bekenov 1969). Therefore, we confirm that if the yellow steppe lemming population originates from a comparatively small number of individuals, but are non-inbred and unfamiliar, then the animals can successfully reproduce without noticeable signs of inbreeding depression up to rather late stages of reproduction. Under natural conditions, this feature of breeding presumably allows the lemmings to recover the population numbers after periods of depression (Chentsova 1969). We assume that recent isolated natural populations of E. luteus are inbred to a certain extent and display a considerable resistance to inbreeding depression. According to the data obtained for other arvicoline species, such as Harting’s vole, Microtus hartingi, inhabiting fragmented natural habitats which assume lower opportunity to dispersal supposedly promotes higher inbreeding tolerance (Zorenko and Kaija 2024). Some isolated inbred populations remain stable even at a low level of genetic variability as inbreeding, in certain cases, purges deleterious alleles (Crnokrak and Barrett 2002). However, if a crucial level of inbreeding in a population is reached, it may become extinct within a certain period.

By analogy to our studies, a number of researchers registered a pronounced inbreeding depression in the captive populations of various mammal species. Consanguineous mating is almost inevitable when animals reproduce in the conditions of captivity (Ralls et al. 1988; Lacy 1993). In particular, Ralls and Ballou (1982a, b, 1983), and Ralls et al. (1988) investigated the effect of inbreeding in more than 30 mammal species belonging to the orders Didelphimorphia, Diprotodontia, Macroscelidea, Rodentia, Primates, Perissodactyla, and Artiodactyla. The investigated mammals were kept in different US zoos and research centers. Scientists revealed an increase in the mean offspring inbreeding coefficients and significantly higher inbred than noninbred infant and juvenile mortality in most of the studied populations. Other manifestations of inbreeding depression revealed in our studies, such as reduced longevity and a decrease in the number of young per 1 litter, have also been registered in captive populations of different mammalian species. For example, the decline in the life span of inbred individuals was observed in 3 gazelle species: Gazella dorcas neglecta, G. cuvieri, and G. dama mhorr (Cassinello 2005). A consistent reduction in the number of pups born per litter with the increase in offspring coefficients of inbreeding was reported for the long-haired rat, Rattus villosissimus (Lacy and Horner 1997).

Both investigated zoo populations of E. luteus originated from a relatively small number of founders. Under such conditions, the negative consequences of inbreeding are commonly more expressed. Researchers detected a significant increase in inbreeding coefficients with succeeding generations in initially small captive populations of a variety of mammal species (Ralls and Ballou 1982a, b; Lacy 1993; Lacy and Horner 1997; Cassinello 2005; Charpentier et al. 2005). Rapid loss of genetic variability and frequent fixation of deleterious alleles are quite possible under such circumstances. Less effective process of natural selection and more serious exposure to random genetic drift are the probable reasons for these traits of inbreeding depression (Lacy 1993; Keller and Waller 2002). All foregoing emphasizes the importance of developing conservation management programs allowing to avoid close inbreeding and eliminate inbreeding depression in groups of animals kept in captivity (Ballou and Lacy 1995; Laikre 1999; Lacy 2000; Boakes et al. 2007; Ivy and Lacy 2010; Caballero et al. 2017). In some instances, the estimation of the efficiency of natural selection in the purging of the deleterious alleles from the populations, which were previously exposed to long-term inbreeding is required (Lacy and Ballou 1998).

Our results confirmed a significant decline in the number of litters, born, and weaned pups in the E. luteus focal colony with the progressive increase in the degree of dam inbreeding. For instance, the IC of females that produced 10 and more (up to 23) litters varied from 0 to 0.14 (mean: 0.03 ± 0.02). This indicates that they were broadly non-inbred. Herewith, a total of females who did not deliver a single litter were inbred to a considerable extent. Their IC varied from 0.14 to 0.29 (mean: 0.21 ± 0.02). Brewer and coauthors (1990) revealed a similar negative association between dam inbreeding coefficients and such demographic values as initial litter size, number of weaned offspring, proportion of young surviving until weaning at 20 days, and litter mass at the age of weaning in captive populations of several subspecies of white-footed mouse, Peromyscus leucopus, and old-field mouse, P. polionotus. The studied subspecies differ in inhabitation and genetic diversity. The strongest association (with regression coefficients exceeding 2 standard errors) was registered in the colony of P. leucopus tornillo. The founders of the colony demonstrated considerably high genetic and allozyme variation (Brewer et al. 1990). Lacy et al. (1996) registered the analogous negative impact of the degree of dam inbreeding on the probability to deliver and litter size in P. polionotus subgriseus and P. p. rhoadsi and on the offspring body mass at weaning in the P. p. leucocephalus (Lacy et al. 1996). In both above-mentioned studies, the individual inbreeding coefficients varied in wide limits and reflected the sustained accumulation of inbreeding in the colonies (Brewer et al. 1990; Lacy et al. 1996). A significant dependence of the offspring viability on the level of the dam, not sire, inbreeding is apparently explained by the disturbances of maternal behavior of inbred females, such as maternal neglect or infanticide (Lacy et al. 1996). It also should be noted that P. leucopus is promiscuous under natural conditions (Nicholson 1941; Xia and Millar 1988, 1991; Becker et al. 2012). During the breeding season, some adult males form only temporary pairs with females, which exist for 1–2 weeks (Nicholson 1941). On the contrary, P. polionotus display long-term monogamy, family group formation, and paternal care of offspring (Foltz 1981; Margulis 1998). The mating system of P. leucopus assumes a higher propensity to inbreeding (Zorenko and Kaprale 2003; Kokko and Ots 2006), which is presumably avoided mainly through the natal dispersal of young animals (Wolff 1992).

Therefore, we conclude that the progressive accumulation of inbreeding in the yellow steppe lemming captive colony results in severe inbreeding depression manifested in the decrease in the animal life span and reproductive parameters in the breeding pairs. However, if the E. luteus population originates from a few founders, but they are non-inbred and unfamiliar, then the successful reproduction without significant traits of inbreeding depression will proceed for several generations until the mean offspring inbreeding coefficient reaches approximately 0.2. In nature, this feature of reproduction supposedly allows to recover the population numbers after periods of depression. Nevertheless, a critical level of inbreeding together with fluctuations in the number may pose a risk of the extinction of particular yellow steppe lemming populations.

Acknowledgments

We would like to express our gratitude to the staff of the Experimental Department of Small Mammals of the Moscow Zoo for responsible care of yellow steppe lemmings, establishing reproducing pairs, and timely collection of information on animal reproduction. We are also grateful to one of the lecturers of the Moscow Pedagogical State University, D.A. Shitikov, for consultation on the analysis of statistical data.

Contributor Information

Vladimir V Streltsov, Laboratory for Behaviour and Behavioural Ecology of Mammals, A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninsky Prospect, 33, Moscow 119071, Russia.

Olga G Ilchenko, Experimental Department of Small Mammals, Moscow Zoo, Bolshaya Gruzinskaya Str., 1, Moscow 123242, Russia.

Elena V Kotenkova, Laboratory for Behaviour and Behavioural Ecology of Mammals, A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninsky Prospect, 33, Moscow 119071, Russia.

Funding

The research was carried out within the framework of the theme of a State Assignment of the Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, “Ecological and Evolutionary Aspects of Animal Behavior and Communication,” project no. AAAA-A18-118042690110-1.

Authors’ Contributions

E.V.K. and V.V.S. conceived the study. O.G.I. provided animals for the study. O.G.I. and V.V.S. collected the data. V.V.S. analyzed the data and wrote the manuscript. All authors contributed critically to the final draft and gave final approval for publication.

Conflict of Interest

The authors declare no competing interests.

Ethics Statement

All experiments with lemmings were performed in accordance with the rules adopted by the European Convention for the Protection of Vertebrate Animals used for Experimental and other Scientific Purposes. The experimental protocol was approved by the Bioethical Committee of the A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences (protocol №54, 2021-22-11).

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