Assessment of between-founder heterogeneity in inbreeding depression for reproductive traits in Baluchi sheep.

Magnitude of inbreeding depression could be different among descendants of various founder animals, when recessive genetic composition of a population is unevenly distributed among founder animal genomes. Reproductive records of Baluchi sheep for the litter variables size at birth (LSB), size at weaning (LSW), mean weight/lamb born (LMWLB), mean weight/lamb weaned (LMWLW), total weight at birth/ewe lambing (TLWB) and total weight at weaning/ewe lambing (TLWW) were used to examine heterogeneity in inbreeding depression between founder animals. Pedigree-based inbreeding coefficients were proportioned into components coming from founder animals and Mendellian contribution from non-founder animals. Two approaches were used to assess effects of inbreeding: overall inbreeding coefficients or partial inbreeding of the four main founder animals as possible covariates included in statistical models. Among the traits evaluated, there were effects on LMWLB, LMWLW and TLWW of inbreeding with there being a -8, -48, and -95 g decrease per 1% increase in inbreeding, respectively. Linear regressions of traits on partial inbreeding coefficients due to founder animals were of different magnitudes and ranged between -0.12 and +0.128. Heterogeneous contribution of founder animals to inbreeding depression occurred for LSB, LMWLB, and TLWW. These results indicate there was uneven distribution of recessive genetic composition among genomes of founder animals or differences in selection pressures on unfavorable alleles between different founder lines. The observed variation in founder-specific inbreeding depression indicates a small number of alleles with major effects are contributing to inbreeding depression.

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation.

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

Inbreeding depression in sperm quality in a critically endangered amphibian.

Small, isolated populations often experience increased inbreeding and decreased heterozygosity, which increases the potential risk of inbreeding depression. The relationship between inbreeding and sperm health is well-documented in a variety of taxa, but has yet to be explored in amphibians. The dusky gopher frog, Lithobates sevosus, is a critically endangered species with years of documented inbreeding and low genetic variability as a consequence of isolation and population size reduction. This study investigated the effects of inbreeding on sperm quality in captive L. sevosus using an outbred, sister species (Lithobates pipiens) as a standard for comparison. We found L. sevosus to have severely reduced sperm quality in terms of total motility, forward progressive motility, concentration, and viability. Additionally, we observed a significant, negative relationship between total sperm motility and mean kinship within captive-bred individuals. These data serve to enhance our understanding of the role inbreeding plays in amphibians, and to provide valuable insight into new risk factors declining amphibian populations may face.

Little to no inbreeding depression in a tapeworm with mixed mating.

Meta-studies on hermaphrodites have found a negative relationship between primary selfing rates and levels of inbreeding depression (ID) and, thus, generally support purging in inbred systems. However, in plants, high among-taxa variance in ID results in no difference in the mean ID between outcrossing and mixed-mating taxa. Selective interference likely explains high ID among mixed-mating taxa, whereas low levels of ID among mixed-mating taxa are not as stressed. Among animal hermaphrodites, primarily molluscs, there are little data on mixed-mating systems. To fill a taxonomic and mating system gap, we tested for ID in a mixed-mating tapeworm, Oochoristica javaensis. We provide a direct estimate of ID across infection of an intermediate host by comparing selfing rates at two life history stages. We found little to no evidence for ID, and the level of ID falls in line with what is reported for highly selfing species even though O. javaensis has mixed mating. We discuss this result within the context of kin mating in O. javaensis. Our results emphasize that primary selfing rates alone may be insufficient to classify the inbreeding history in all species when testing for a relationship to ID. Mixed-mating taxa, and possibly some outcrossing taxa, may exhibit low levels of ID if biparental inbreeding is also driving purging. We advocate that ID studies report estimates of inbreeding history (e.g. FIS or identity disequilibrium) from nature-derived adult samples to provide context rather than relying on primary selfing rates alone.

Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population.

The fitness consequences of inbreeding and the individual behaviors that prevent its detrimental effects can be challenging to document in wild populations. Here, we use field and molecular data from a 17-year study of banner-tailed kangaroo rats (Dipodomys spectabilis) to quantify the relationship between inbreeding, mate kinship, and lifetime reproductive success. Using a pedigree that was reconstructed using genetic and field data within a Bayesian framework (median probability of parental assignment = 0.92, mean pedigree depth = 6 generations), we estimated both inbreeding coefficients and kinship between individuals that produced offspring (mean inbreeding coefficient = 0.07, mean mate kinship = 0.08). We also used the pedigree, in combination with census data, to generate a series of fitness estimates, ranging from survival to reproductive maturity to lifetime reproductive success. We found that the population's inbreeding load was low to moderate (0.98-4.66 haploid lethal equivalents) and increased with the time frame over which fitness was estimated (lowest for survival to maturity, highest for adult-to-adult reproductive success). Fitness decreased with increasing inbreeding coefficients. For example, lifetime reproductive success was reduced by 24% for individuals with inbreeding coefficients greater than twice the population mean. Within full sibling pairs, the sibling with less-related mates produced an average of 30% more offspring over its lifetime. These data further illustrate that inbreeding can have a negative effect on lifetime reproductive success.

Interplay between age-based competitive asymmetries within the brood and direct competition between inbred and outbred offspring in a burying beetle.

Theory suggests that intraspecific competition associated with direct competition between inbred and outbred individuals should be an important determinant of the severity of inbreeding depression. The reason is that, if outbred individuals are stronger competitors than inbred ones, direct competition should have a disproportionate effect on the fitness of inbred individuals. However, an individual's competitive ability is not only determined by its inbreeding status but also by competitive asymmetries that are independent of an individual's inbreeding status. When this is the case, such competitive asymmetries may shape the outcome of direct competition between inbred and outbred individuals. Here, we investigate the interface between age-based competitive asymmetries within broods and direct competition between inbred and outbred offspring in the burying beetle Nicrophorus vespilloides. We found that inbred offspring had lower survival than outbred ones confirming that there was inbreeding depression. Furthermore, seniors (older larvae) grew to a larger size and had higher survival than juniors (younger larvae), confirming that there were age-based competitive asymmetries. Nevertheless, there was no evidence that direct competition between inbred and outbred larvae exacerbated inbreeding depression, no evidence that inbreeding depression was more severe in juniors and no evidence that inbred juniors suffered disproportionately due to competition from outbred seniors. Our results suggest that direct competition between inbred and outbred individuals does not necessarily exacerbate inbreeding depression and that inbred individuals are not always more sensitive to poor and stressful conditions than outbred ones.

Sex-specific effects of inbreeding on reproductive senescence.

Inbreeding depression plays a significant role in evolutionary biology and ecology. However, we lack a clear understanding of the fitness consequences of inbreeding depression. Studies often focus on short-term effects of inbreeding in juvenile offspring, whereas inbreeding depression in adult traits and the interplay between inbreeding depression and age are rarely addressed. Inbreeding depression may increase with age and accelerate the decline in reproductive output in ageing individuals (reproductive senescence), which could be subject to sex-specific dynamics. We test this hypothesis with a longitudinal experimental study in a short-lived songbird. Adult inbred and outbred male and female canaries were paired in a 2 × 2 factorial design, and survival and annual reproductive performance were studied for 3 years. We found inbreeding depression in female egg-laying ability, male fertilization success and survival of both sexes. Annual reproductive success of both males and females declined when paired with an inbred partner independent of their own inbreeding status. This shows that inbreeding can have fitness costs in outbred individuals when they mate with an inbred individual. Further, inbred females showed faster reproductive senescence than outbred females, confirming that inbreeding depression and age can interact to affect fitness. By contrast, there was no evidence for an interaction between inbreeding depression and reproductive senescence in male fertilization success. Our findings highlight the importance of considering sex-specific effects and age to determine the full range of fitness consequences of inbreeding and demonstrate that inbreeding depression can accelerate reproductive senescence.

Changes in floral biology and inbreeding depression in native and invaded regions of Datura stramonium.

Plant populations invading new environments might compromise their fitness contribution to the next generation, because of the lack of native specialist pollinators and/or potential mates. Thus, changes in plant mating system and traits linked to it are expected in populations colonising new environments where selection would favour selfing and floral traits that maximise reproductive output. To test this, we studied native (Mexico) and non-native (Spain) populations of the obligate sexual reproducing annual weed Datura stramonium. Flower size, herkogamy, total number of seeds per plant, number of visits by and type of pollinators, and inbreeding depression were assessed in native and non-native populations. Finally, we measured phenotypic selection on corolla size and herkogamy in each population. Flower size and herkogamy showed wide and similar variation in both ranges. However, the largest average flower size was found in one non-native population whereas the highest average positive herkogamy was detected in one native population. On average, flowers in the native range received more visits by pollinators. Hawkmoths were the main visitors in the native populations while only bees were observed visiting flowers in Spain's populations. Only in the native range was inbreeding depression detected. Selection to reduce herkogamy was found only in one native population. Absence of both inbreeding depression and selection on floral traits suggest a change in mating system of D. stramonium in a new range where generalist pollinators may be promoting high reproductive success. Selection against deleterious alleles might explain the reduction of inbreeding depression, promoting the evolution of selfing.

Genome-wide autozygosity is associated with lower general cognitive ability.

Inbreeding depression refers to lower fitness among offspring of genetic relatives. This reduced fitness is caused by the inheritance of two identical chromosomal segments (autozygosity) across the genome, which may expose the effects of (partially) recessive deleterious mutations. Even among outbred populations, autozygosity can occur to varying degrees due to cryptic relatedness between parents. Using dense genome-wide single-nucleotide polymorphism (SNP) data, we examined the degree to which autozygosity associated with measured cognitive ability in an unselected sample of 4854 participants of European ancestry. We used runs of homozygosity-multiple homozygous SNPs in a row-to estimate autozygous tracts across the genome. We found that increased levels of autozygosity predicted lower general cognitive ability, and estimate a drop of 0.6 s.d. among the offspring of first cousins (P=0.003-0.02 depending on the model). This effect came predominantly from long and rare autozygous tracts, which theory predicts as more likely to be deleterious than short and common tracts. Association mapping of autozygous tracts did not reveal any specific regions that were predictive beyond chance after correcting for multiple testing genome wide. The observed effect size is consistent with studies of cognitive decline among offspring of known consanguineous relationships. These findings suggest a role for multiple recessive or partially recessive alleles in general cognitive ability, and that alleles decreasing general cognitive ability have been selected against over evolutionary time.