Inbreeding Avoidance Mechanisms Research Articles

Early-acting inbreeding depression can evolve as an inbreeding avoidance mechanism.

Despite the potential for mechanical, developmental and/or chemical mechanisms to prevent self-fertilization, incidental self-fertilization is inevitable in many predominantly outcrossing species. In such cases, inbreeding can compromise individual fitness. Unquestionably, much of this inbreeding depression is maladaptive. However, we show that when reproductive compensation allows for the replacement of inviable embryos lost early in development, selection can favour deleterious recessive variants that induce 'self-sacrificial' death of inbred embryos. Our theoretical results provide numerous testable predictions which could challenge the assumption that inbreeding depression is always maladaptive. Our work is applicable any species that cannot fully avoid inbreeding, exhibits substantial inbreeding depression, and has the potential to compensate embryos lost early in development. In addition to its general applicability, our theory suggests that self-sacrificial variants might be responsible for the remarkably low realized selfing rates of gymnosperms with high primary selfing rates, as gymnosperms exhibit strong inbreeding depression, have effective reproductive compensation mechanisms, and cannot evolve chemical self-incompatibility.

Multiple mechanisms for inbreeding avoidance used simultaneously in a wild ape.

Mating with close kin can have considerable negative fitness consequences, which are expected to result in selective pressure for inbreeding avoidance mechanisms, such as dispersal, mate choice and post-copulatory biases. Captive studies have suggested that inbreeding avoidance through mate choice is far less widespread than expected and may be absent where other mechanisms already limit inbreeding. However, few studies have examined multiple mechanisms of inbreeding avoidance simultaneously, particularly in the wild. We use 13 years of detailed dispersal, copulation and paternity data from mountain gorillas to examine inbreeding avoidance. We find that partial dispersal of both sexes results in high kinship in multimale groups, but that copulations between close kin occur 40% less than expected. We find strong kin discrimination in mate choice, with significant avoidance of maternal kin but more limited avoidance of paternal kin. We find no evidence for post-copulatory inbreeding avoidance. Our analyses support familiarity-based mechanisms of kin identification and age-based avoidance that limits mating between fathers and daughters in their natal group. Our findings demonstrate that multiple complementary mechanisms for inbreeding avoidance can evolve in a single species and suggest that inbreeding avoidance through mate choice may enable more flexible dispersal systems to evolve.

Relatedness dynamics and sex-biased dispersal in a seasonal cycle of corn mice from intensively managed agroecosystems.

The sex-biased dispersal and kinship dynamics are important factors shaping the spatial distribution of individuals and are key parameters affecting a variety of ecological and evolutionary processes. Here, we studied the spatial distribution of related individuals within a population of corn mice Calomys musculinus in a seasonal cycle to infer dispersal patterns. The sampling was carried out from spring 2005 to winter 2006 in field borders of intensively managed agroecosystems. Genotyping data from 346 individuals with 9 microsatellites showed spatial genetic structure was weak for males, but not for females. The results indicate a complex spatial kinship dynamic of related females across all seasons. Which, contrary to our expectations, dispersal distances decrease with the increase of the population abundance. Meanwhile, male dispersal distances were greater when population abundance increased and thus the availability of active females. Males disperse greater distances to mate and sire offspring with distant females as a possible inbreeding avoidance mechanism. This study shows that C. musculinus is capable of much greater scattering distances than previously reported and that dispersal occurs fluidly and without barriers across the agroecosystem. The indirect benefit of dispersal on individual fitness could be related to relaxing the competition in the natal area and increasing the mating rate. Our study highlights the value of combining genetic relatedness, fieldwork observations, and behavioral data to estimate dispersal at a fine geographical scale.

Evidence of low within-pair genetic relatedness in a relict population of Thorn-tailed Rayadito despite long-term isolation.

Investigating whether mating patterns are biased in relation to kinship in isolated populations can provide a better understanding of the occurrence of inbreeding avoidance mechanisms in wild populations. Here, we report on the genetic relatedness (r) among breeding pairs in a relict population of Thorn‐tailed Rayadito (Aphrastura spinicauda) in north‐central Chile that has experienced a long‐term history of isolation. We used simulations based on 8 years of data to assess whether mating is random with respect to relatedness. We found that mean and median population values of pair relatedness tended to be lower than randomly generated values, suggesting that mating is not random with respect to kinship. We hypothesize that female‐biased dispersal is the main mechanism reducing the likelihood of mating among kin, and that the proportion of related pairs (i.e., r > 0.125) in the study population (25%) would presumably be higher in the absence of sex‐biased dispersal. The occurrence of other mechanisms such as extra‐pair copulations, delayed breeding, and active inbreeding avoidance through kin discrimination cannot be dismissed and require further study.

Human-controlled reproductive experience may contribute to incestuous behavior observed in reintroduced semi-feral stallions (Equuscaballus)

Equine reproductive behavior is affected by many factors, some remaining poorly understood. This study tested the hypothesis that a period of captivity during the juvenile period and human-controlled reproduction may potentially be involved in the disruption of the development of incestuous mating avoidance behavior in sanctuary-reintroduced male Konik polski horses. Between 1986 and 2000, cases of incestuous behavior in harem stallions born and reared until weaning in the sanctuary were studied. Eight males lived in the sanctuary's feral herd for the rest of their lives (the non-captive group; nC). They gained their own harem of mares without human intervention (no human-controlled reproductive activity, nHC). Another five stallions were removed as weanlings, reared in captivity and then reintroduced as adults (captive, C). Three of these C stallions were used as in-hand breeding stallions, one as a “teaser” (human-controlled reproductive activity, HC) and one was not used for reproduction in captivity (nHC). Reproductive records for 46 mares, daughters of all 13 harem stallions, were scrutinized and cases of incestuous breeding were recorded by interrogation of foal parentage records. C stallions failed to expel more daughters than nC stallions (33% vs. 18%, P = 0.045), and mated with significantly more of them (28% vs. 11%, P = 0.025). Interestingly, HC stallions expelled fewer (60%) and successfully mated with more (33%) daughters that nHC stallions (84% expelled, P = 0.013, and 10% successful mating with daughters, P = 0.010). All HC stallions bred incestuously at least once.We propose that human intervention during a critical period of development of social and reproductive behavior in young stallions, by enforced separation from their natal herd and in-hand breeding, may contribute to their later aberrant behavior and disruption of inbreeding avoidance mechanisms in these stallions. The previous occurrence of human-controlled breeding may be one of the factors promoting incestuous behavior of stallions in natural conditions. The uninterrupted presence of stallions in their harems and herd member recognition may also play important roles in inbreeding avoidance in horses.

Cooperatively breeding banded mongooses do not avoid inbreeding through familiarity-based kin recognition

In species that live in family groups, such as cooperative breeders, inbreeding is usually avoided through the recognition of familiar kin. For example, individuals may avoid mating with conspecifics encountered regularly in infancy, as these likely include parents, siblings, and closely related alloparents. Other mechanisms have also been reported, albeit rarely; for example, individuals may compare their own phenotype to that of others, with close matches representing likely relatives (“phenotype matching”). However, determinants of the primary inbreeding avoidance mechanisms used by a given species remain poorly understood. We use 24 years of life history and genetic data to investigate inbreeding avoidance in wild cooperatively breeding banded mongooses (Mungos mungo). We find that inbreeding avoidance occurs within social groups but is far from maximised (mean pedigree relatedness between 351 breeding pairs = 0.144). Unusually for a group-living vertebrate, we find no evidence that females avoid breeding with males with which they are familiar in early life. This is probably explained by communal breeding; females give birth in tight synchrony and pups are cared for communally, thus reducing the reliability of familiarity-based proxies of relatedness. We also found little evidence that inbreeding is avoided by preferentially breeding with males of specific age classes. Instead, females may exploit as-yet unknown proxies of relatedness, for example, through phenotype matching, or may employ postcopulatory inbreeding avoidance mechanisms. Investigation of species with unusual breeding systems helps to identify constraints against inbreeding avoidance and contributes to our understanding of the distribution of inbreeding across species.Significance statementChoosing the right mate is never easy, but it may be particularly difficult for banded mongooses. In most social animals, individuals avoid mating with those that were familiar to them as infants, as these are likely to be relatives. However, we show that this rule does not work in banded mongooses. Here, the offspring of several mothers are raised in large communal litters by their social group, and parents seem unable to identify or direct care towards their own pups. This may make it difficult to recognise relatives based on their level of familiarity and is likely to explain why banded mongooses frequently inbreed. Nevertheless, inbreeding is lower than expected if mates are chosen at random, suggesting that alternative pre- or post-copulatory inbreeding avoidance mechanisms are used.

Genetic diversity and population structure of six South African Acacia mearnsii breeding populations based on SSR markers.

Black wattle (Acacia mearnsii) has great economic value as a commercial source of tannins, timber and a source of firewood for local and international markets. It has been suggested that to maximize the genetic gain of A. mearnsii plantations in South Africa, the gene pool that exist within ICFR needs to be broadened via introduction of new genotypes with diverse traits. In this work, 282 A. mearnsii samples sourced from the ICFR breeding program were genotyped using 11 cross-species SSR markers. Our results showed low to moderate genetic differentiation (FST) among the six breeding subpopulations, with positive inbreeding (FIS) values that could be attributed to an historical inbreeding event. Low levels of relatedness could however indicate some mechanism of inbreeding avoidance. The effects from a recent supplementation of genetic material from two native Australian populations were observed through genetic structuring analyses. Analysis of molecular variance (AMOVA) revealed that significant genetic variation was mainly distributed within populations (75%) and among individuals (23%). The results provide significant information on A. mearnsii population genetic diversity and structure, which can be used for conservation of the current subpopulations and future tree improvement programs.

Mechanisms of Inbreeding Avoidance in a Wild Primate

The deleterious effects of inbreeding have been well-documented in both captive and wild populations. Hence, animals are expected to engage in inbreeding avoidance. However, one recent meta-analysis of mate-choice experiments indicates that animals of many species do not avoid mating with kin in experimental settings, and another reports that behavioral inbreeding avoidance is likely to evolve only when kin encounter each other regularly and inbreeding costs are high. These important results call for more detailed data on the patterns and processes of encounter frequency and mating behavior between kin within natural animal populations. Here, we present the first detailed assessment of encounter frequency and behavioral inbreeding avoidance in multiple kin classes in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes coreside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥ 0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to the problem of kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10x higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.

Genetic consequences of social structure in the golden-crowned sifaka

Many species are structured in social groups (SGs) where individuals exhibit complex mating strategies. Yet, most population genetic studies ignore SGs either treating them as small random-mating units or focusing on a higher hierarchical level (the population). Empirical studies acknowledging SGs have found an overall excess of heterozygotes within SGs and usually invoke inbreeding avoidance strategies to explain this finding. However, there is a lack of null models against which ecological theories can be tested and inbreeding avoidance quantified. Here, we investigate inbreeding (deviation from random mating) in an endangered forest-dwelling pair-living lemur species (Propithecus tattersalli). In particular, we measure the inbreeding coefficient (FIS) in empirical data at different scales: SGs, sampling sites and forest patches. We observe high excess of heterozygotes within SGs. The magnitude of this excess is highly dependent on the sampling scheme: while offspring are characterised by a high excess of heterozygotes (FIS < 0), the reproductive pair does not show dramatic departures from Hardy–Weinberg expectations. Moreover, the heterozygosity excess disappears at larger geographic scales (sites and forests). We use a modelling framework that incorporates details of the sifaka mating system but does not include active inbreeding avoidance mechanisms. The simulated data show that, although apparent “random mating” or even inbreeding may occur at the “population” level, outbreeding is maintained within SGs. Altogether our results suggest that social structure leads to high levels of outbreeding without the need for active inbreeding avoidance mechanisms. Thus, demonstrating and measuring the existence of active inbreeding avoidance mechanisms may be more difficult than usually assumed.

Inbreeding and disease avoidance in a free-ranging koala population.

Habitat destruction and fragmentation are increasing globally, forcing surviving species into small, isolated populations. Isolated populations typically experience heightened inbreeding risk and associated inbreeding depression and population decline; although individuals in these populations may mitigate these risks through inbreeding avoidance strategies. For koalas, as dietary specialists already under threat in the northern parts of their range, increased habitat fragmentation and associated inbreeding costs are of great conservation concern. Koalas are known to display passive inbreeding avoidance through sex-biased dispersal, although population isolation will reduce dispersal pathways. We tested whether free-ranging koalas display active inbreeding avoidance behaviours. We used VHF tracking data, parentage reconstruction, and veterinary examination results to test whether free-ranging female koalas avoid mating with (a) more closely related males; and (b) males infected with sexually transmitted Chlamydia pecorum. We found no evidence that female koalas avoid mating with relatively more related available mates. In fact, as the relatedness of potential mates increases, so did inbreeding events. We also found no evidence that female koalas can avoid mating with males infected with C.pecorum. The absence of active inbreeding avoidance mechanisms in koalas is concerning from a conservation perspective, as small, isolated populations may be at even higher risk of inbreeding depression than expected. At risk koala populations may require urgent conservation interventions to augment gene flow and reduce inbreeding risks. Similarly, if koalas are not avoiding mating with individuals with chlamydial disease, populations may be at higher risk from disease than anticipated, further impacting population viability.

Female guppies increase their propensity for polyandry as an inbreeding avoidance strategy

Mating with close relatives often causes a decline in offspring fitness, termed inbreeding depression. Consequently, pre- and postcopulatory inbreeding avoidance mechanisms are likely to evolve, especially in females due to their relatively high levels of reproductive investment. If precopulatory inbreeding avoidance mechanisms are absent or unreliable, females may exploit postcopulatory sexually selected inbreeding avoidance mechanisms by mating with multiple males (polyandry). Despite this expectation, few studies have tested whether females alter their propensity to mate multiply in an inbreeding avoidance context. Here, we tested whether the perceived risk of inbreeding promotes polyandrous behaviour in guppies, Poecilia reticulata, a species susceptible to inbreeding depression. Virgin females were assigned to either a sibling or nonsibling mating and subsequently presented with three unrelated males simultaneously. Consistent with previous studies, we found that females did not discriminate between initially encountered males based on relatedness. However, females increased their propensity to mate multiply after mating with a brother. Subsequent paternity tests were performed to determine whether polyandry minimizes inbreeding through a dilution effect (i.e. greater number of sires in the related treatment) or through postcopulatory biasing mechanisms (i.e. greater paternity skew towards unrelated males). Surprisingly, our results supported neither scenario; we detected no significant difference in paternity skew or the number of sires between treatments. Overall, our study provides a rare example of females responding to an increased risk of inbreeding by increasing their propensity to remate, but the postcopulatory processes arising from this behaviour, along with the mechanisms underlying kin recognition, await further investigation.

Close‐kin mating, but not inbred parents, reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long-lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long-lived species is limited. In this study, we leverage a well-studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long-lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex-specific evolutionary trade-offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long-lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.

Opposition to Inbreeding Between Close Kin Reflects Inclusive Fitness Costs.

Due to the intense selection pressure against inbreeding, humans are expected to possess psychological adaptations that regulate mate choice and avoid inbreeding. From a gene’s-eye perspective, there is little difference in the evolutionary costs between situations where an individual him/herself is participating in inbreeding and inbreeding among other close relatives. The difference is merely quantitative, as fitness can be compromised via both routes. The question is whether humans are sensitive to the direct as well as indirect costs of inbreeding. Using responses from a large population-based sample (27,364 responses from 2,353 participants), we found that human motivations to avoid inbreeding closely track the theoretical costs of inbreeding as predicted by inclusive fitness theory. Participants were asked to select in a forced choice paradigm, which of two acts of inbreeding with actual family members they would want to avoid most. We found that the estimated fitness costs explained 83.6% of participant choices. Importantly, fitness costs explained choices also when the self was not involved. We conclude that humans intuit the indirect fitness costs of mating decisions made by close family members and that psychological inbreeding avoidance mechanisms extend beyond self-regulation.

Close inbreeding and low genetic diversity in Inner Asian human populations despite geographical exogamy

When closely related individuals mate, they produce inbred offspring, which often have lower fitness than outbred ones. Geographical exogamy, by favouring matings between distant individuals, is thought to be an inbreeding avoidance mechanism; however, no data has clearly tested this prediction. Here, we took advantage of the diversity of matrimonial systems in humans to explore the impact of geographical exogamy on genetic diversity and inbreeding. We collected ethno-demographic data for 1,344 individuals in 16 populations from two Inner Asian cultural groups with contrasting dispersal behaviours (Turko-Mongols and Indo-Iranians) and genotyped genome-wide single nucleotide polymorphisms in 503 individuals. We estimated the population exogamy rate and confirmed the expected dispersal differences: Turko-Mongols are geographically more exogamous than Indo-Iranians. Unexpectedly, across populations, exogamy patterns correlated neither with the proportion of inbred individuals nor with their genetic diversity. Even more surprisingly, among Turko-Mongols, descendants from exogamous couples were significantly more inbred than descendants from endogamous couples, except for large distances (>40 km). Overall, 37% of the descendants from exogamous couples were closely inbred. This suggests that in Inner Asia, geographical exogamy is neither efficient in increasing genetic diversity nor in avoiding inbreeding, which might be due to kinship endogamy despite the occurrence of dispersal.

No evidence for an inbreeding avoidance system in the bumble bee Bombus terrestris

Inbreeding is caused by the mating of closely related individuals and may produce a decrease in the fitness of offspring and have deleterious consequences for adults. In haplodiploid social Hymenoptera inbreeding has a further negative effect due to the production of unviable or sterile diploid males. As a consequence, mechanisms of inbreeding avoidance would be expected to evolve. In this study, we investigated the mating choice between related (inbred) or unrelated (outbred) gynes and males of Bombus terrestris reared in laboratory conditions by performing cage and tunnel experiments. Not only did we find no mating preference for related or unrelated partners (mating success 41.55 ± 3.7 and 39.69 ± 4.4%, respectively), but the mating latency was even shorter in inbred (6.97 ± 0.6 min) than in outbred matings (8.74 ± 0.8 min). We hypothesize that in wild populations of B. terrestris, the lack of incest avoidance could be compensated by tolerance of high levels of inbreeding.

Producing offspring in Armadillidium vulgare: Effects of genetic diversity and inbreeding.

Genetic diversity is known to be correlated to fitness traits, and inbred individuals often display lower values for life history traits. In this study, we attempt to quantify how inbreeding affects such traits in the terrestrial isopod Armadillidium vulgare by performing inbred and non-inbred crosses under laboratory conditions. We estimated genetic characteristics of parents and offspring, and related them to fecundity and fertility measures, as well as offspring growth and survival. Our study shows that a decrease in offspring number might result from mortality around birth, but not to changes in fecundity, fertilization rate, or developmental failure between inbred and non-inbred crosses. More heterozygous females tended to be bigger and had a higher fecundity, which could have implications in mate choice. No effect of inbreeding was detected on offspring growth and survival. These results can be related to previously observed effects of genetic characteristics on mating strategies in A. vulgare, and could shed light on mechanisms of inbreeding avoidance in this species.

Different reproductive strategies and their possible relation to inbreeding risk in the bumble bee Bombus terrestris

In many species, inbreeding avoidance mechanisms prevent mating between close relatives, but these mechanisms are poorly studied in bumble bees. The probability of inbred matings within a colony in eusocial insects may depend on the timing of gyne and male emergence and on their sex ratio. In this study, we compared the development of 35 colonies of the bumble bee Bombus terrestris from founding to the emergence of the last gyne, and we investigated the probability of inbred mating in colonies with fertile newborn gynes and males. We calculated a novel colony inbreeding risk index (IRI), which considers the overlap period between fertile gynes and males, their numbers, and the colony sex ratio. We found that the IRI values were strictly correlated with the time elapsed between the gyne point and the switch point (i.e., from the moment of deposition of the first diploid egg that produces a gyne to the first haploid egg). We separated the colonies into two groups based on the mean value of the IRI: colonies with low IRI produced more gynes (93.8 ± 9.4), for a longer period (32.1 ± 1.8 days) and with a lower percentage of overlapped gynes (69 ± 5%) than colonies with high IRI (57.1 ± 21 gynes, 23.3 ± 2.9 days, and 100% overlapped gynes, respectively). A low IRI is connected to a reduced risk of inbred mating, while colonies with a high IRI may be advantaged in conditions of isolation, in case of the absence of non-related reproducers. Inbreeding risk index proved to be a good indicator of the colony reproductive strategy.

Evolution of precopulatory and post-copulatory strategies of inbreeding avoidance and associated polyandry.

Inbreeding depression is widely hypothesized to drive adaptive evolution of precopulatory and post‐copulatory mechanisms of inbreeding avoidance, which in turn are hypothesized to affect evolution of polyandry (i.e. female multiple mating). However, surprisingly little theory or modelling critically examines selection for precopulatory or post‐copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post‐copulatory inbreeding avoidance, but not for precopulatory inbreeding avoidance, requires polyandry, whereas interactions between precopulatory and post‐copulatory inbreeding avoidance might cause functional redundancy (i.e. ‘degeneracy’) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual‐based modelling to quantify evolution of interacting precopulatory and post‐copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post‐copulatory inbreeding avoidance increased selection for initially rare polyandry and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower‐cost alternative strategy. Further, fixed precopulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post‐copulatory inbreeding avoidance, but fixed post‐copulatory inbreeding avoidance did not preclude evolution of precopulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry is therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of precopulatory inbreeding avoidance and resulting low polyandry is more likely when post‐copulatory inbreeding avoidance is precluded or costly, and evolution of post‐copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.

The effects of familiarity and reproductive status on olfactory discrimination by female Cape ground squirrels (Xerus inauris)

The ability to differentiate among conspecifics on the basis of genetic relatedness can be advantageous in kin and mate selection. Selection of mates that are of an intermediate degree of relatedness maximizes the propagation of shared genes to offspring, while minimizing the accumulation of deleterious recessive alleles that can result from close inbreeding. Odors produced from various glandular surfaces of the body have been shown to influence discrimination of conspecifics in numerous taxa, including the order Rodentia. We investigated whether female Cape ground squirrels (Xerus inauris) discriminate between the odors of familiar and foreign males by conducting scent experiments. We simultaneously presented odors that had been collected on acrylic cubes from the anal gland of a familiar (non-dispersed) and a foreign male as well as an unscented control, and recorded the response of focal pregnant and non-pregnant females (n = 19). Non-pregnant females responded differently to the odors of the scent cubes, sniffing the scent collected from the foreign male significantly longer than either the familiar male or control odor, whereas there was no difference in the response of pregnant females. We conclude that male familiarity may influence female mate choice, as familiarity is reliably correlated with relatedness in this population. Based on prior knowledge about the social behavior of Cape ground squirrels, the ability to discriminate between familiar and foreign males may be used by females as an inbreeding avoidance mechanism, as close inbreeding can be avoided by mating with foreign males. Olfactory cues are one method of social communication among conspecifics, and can play an important role in nepotism, territory defense, and mate choice. We studied olfactory discrimination in the Cape ground squirrel, a highly social, semi-fossorial mammal that occurs in South Africa. We assessed the response of pregnant and non-pregnant females to the odors of familiar and unfamiliar males. We found that non-pregnant females displayed a preference for unfamiliar males, whereas pregnant females displayed no preference. Cape ground squirrels are non-territorial and exhibit low levels of intraspecific aggression; therefore, our results indicate that odor may be involved in mate selection by females, rather than territoriality, as relatively low levels of inbreeding are maintained in this population.

Inbreeding and inbreeding avoidance in wild giant pandas

Inbreeding can have negative consequences on population and individual fitness, which could be counteracted by inbreeding avoidance mechanisms. However, the inbreeding risk and inbreeding avoidance mechanisms in endangered species are less studied. The giant panda, a solitary and threatened species, lives in many small populations and suffers from habitat fragmentation, which may aggravate the risk of inbreeding. Here, we performed long-term observations of reproductive behaviour, sampling of mother-cub pairs and large-scale genetic analyses on wild giant pandas. Moderate levels of inbreeding were found in 21.1% of mating pairs, 9.1% of parent pairs and 7.7% of panda cubs, but no high-level inbreeding occurred. More significant levels of inbreeding may be avoided passively by female-biased natal dispersal rather than by breeding dispersal or active relatedness-based mate choice mechanisms. The level of inbreeding in giant pandas is greater than expected for a solitary mammal and thus warrants concern for potential inbreeding depression, particularly in small populations isolated by continuing habitat fragmentation, which will reduce female dispersal and increase the risk of inbreeding.