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PubMed2005

Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini.

Sperm competition is a potent evolutionary force shaping the reproductive biology of most animal species. Here, we estimated the heritability of sperm competition success in the promiscuous bulb mite Rhizoglyphus robini. Sperm competition success was measured with the sterile male technique as the proportion of eggs fertilised by the second of three males mated with a single female. Sperm competition success responded significantly to selection. The heritability estimated from the response to five generations of selection was 0.13. We also estimated the effect of inbreeding on sperm competition success. Males produced by sib-mating (F=0.25) had a significantly lower sperm competition success than outbred males. The estimated coefficient of inbreeding depression was 0.53. Such high inbreeding depression together with moderately low heritability is consistent with the view that sperm competitive ability is under strong directional selection and strongly influences the reproductive success of males.

Acaridae↗

PubMed2006

Among- and within-population variation in outcrossing rate of a mixed-mating freshwater snail.

Mixed-mating animals self-fertilize a proportion of their offspring. Outcrossing rate may covary with the ecological and historical factors affecting the population. Theory predicts that outcrossing is favored when inbreeding depression is high and when individual heterozygosity is important. Self-fertilization is predicted to be favored when costs of male function, or mate finding are high, for example, when empty patches are colonized by few individuals. In this study, we assessed primary (after hatching) and secondary (after juvenile mortality) outcrossing rates of two mixed-mating snail populations. Our purpose was to assess the variation in mating-system parameters and estimate significance of inbreeding depression for secondary outcrossing rate (the realized outcrossing rate of parents that produce the next generation). Secondary outcrossing rate was higher than the primary outcrossing rate in one of the two populations, suggesting considerable inbreeding depression. In the other study population, secondary outcrossing rates were found to increase when initially low, or decrease when initially high, depending on the family. Moderate outcrossing rates were found to be more stable. Parental inbreeding coefficients were close to zero in both populations. Outcrossing rate was much more variable among families in the population with the lower average outcrossing rate, suggesting that individuals differed considerably in their mating system. Our results add to recent studies suggesting that populations of mixed-mating animals may differ in their mating system parameters and expression of inbreeding depression.

Animals↗

PubMed2003

A test for a metastable epigenetic component of heterosis using haploid induction in maize.

We conducted a test to detect if there is a heritable epigenetic component to hybrid vigor and/or inbreeding depression. The impetus for this work was a classical study of the effect of homozygosis on the expression of the maize red color ( r1) locus. It had been shown that maintaining R1 mottling alleles in the homozygous state over several generations produces a progressive decrease of their paternally imprinted expression. This effect is reversed by R1/r1 allele heterozygosity. If this behavior were characteristic of many regulatory genes, then such a phenomenon could contribute to inbreeding depression and heterosis. To examine this question, inbreds of Mo17 and B73 and the two reciprocally produced hybrids were crossed by Stock 6 to generate four classes of maternal haploids. The mature haploid plants were measured for several quantitative traits. If inbreeding depression results from an accumulating heritable effect that is reversed by the hybrid state, one would expect the haploids derived from the hybrids to perform better than those derived from the inbred lines. The hybrid-derived haploids did not exhibit greater average performance than the inbred-derived haploids. These data fail to support the hypothesis that inbreeding depression and heterosis have a metastable epigenetic component.

Epigenesis, Genetic↗

PubMed2006

Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus.

When close relatives are forced to reproduce, the resulting offspring inherit above average homozygosity and reduced fitness. Biologists now recognize inbreeding depression in the wild, a phenomenon that will probably increase as natural populations become depleted and fragmented. Inbreeding depression is most commonly expressed as compromised fertility and embryogenesis, but actual mechanisms remain poorly understood, especially for wild populations. Here, we examine how reduced heterozygosity influences spermatozoal and gonadal traits in wild rabbits (Oryctolagus cuniculus) sampled across the United Kingdom. By using a suite of 29 microsatellite markers (analyzed to confirm representation of individual heterozygosity across our sample), we found a significant negative relationship between heterozygosity and the production of normal sperm; the relationship was significant both between (n = 12) and within (n = 91 [total males], 42 [island], 49 [mainland]) populations. Reduced heterozygosity was also associated with decreased testis size across males (n = 112), but no relationship was seen at the population level, suggesting environmental confounds. Our results show, for a wild mammal, that inbreeding is associated with decreased sperm quality, confirming suggestions of links between inbreeding and elevated sperm abnormalities in rare felids . These findings could explain why inbreeding depression so frequently arises via compromised fertility and embryogenesis .

Animals↗

PubMed2026

Ex situ reared black-footed ferrets exhibit altered sperm DNA methylation.

Many endangered species rely on ex situ management for survival when external threats exist on the landscape. Yet, ex situ settings pose challenges through space limitation, altered environment, and diet. This can lead to environmentally determined inbreeding depression, where ex situ animals exhibit reduced reproductive fitness compared with their in situ counterparts, despite originating from the same genetic stock. We investigated epigenetic differences as a potential mechanism underlying environmentally determined inbreeding depression in black-footed ferrets (Mustela nigripes), a North American endemic species reliant on ex situ conservation. More specifically, we explored how environmental context may influence sperm DNA methylation in samples collected from 12 ex situ and 5 in situ males. Average sperm DNA methylation was significantly higher in ex situ individuals. We additionally identified more than 500 differentially methylated regions between ex situ and in situ sperm samples that were enriched for gene ontology terms pertaining to reproduction and development. Putative genes of interest included NPR2, WEE2, SLC15A1, PDE10A, PIP5K1B, CACNA1E, and CACNA1A, all of which have previously been linked to spermatogenesis, sperm motility, or fertilization in mammals. Results suggest that environmental conditions may alter sperm DNA methylation in black-footed ferrets, with possible links to decreased reproductive success in ex situ settings. These findings provide valuable insights into the molecular mechanisms underlying environmentally determined inbreeding depression in black-footed ferrets and other conservation-reliant species, and can serve as a foundation for future research on improving reproductive health in endangered wildlife.

Animals↗

PubMed1998

Relationships among parental inbreeding, parental behaviour and offspring viability in oldfield mice

Studies of inbreeding depression have traditionally suffered from two weaknesses. First, they usually confound offspring deficiencies with parental ones; second, they neglect the possible role of behaviour in inbreeding depression. In the present study, I examined the relationship among parental inbreeding, offspring viability and parental behaviour in two subspecies of the monogamous oldfield mouse, Peromyscus polionotus. Parental inbreeding was separated from any offspring inbreeding effects through both experimental design and analysis. Dams performed more parental behaviour than did sires, and maternal behaviour had a stronger effect on offspring survival than did paternal behaviour. Maternal behaviour was more buffered to the effects of inbreeding than was paternal behaviour; that is, parental behaviour of inbred females was not compromised. In contrast, inbred males showed substantial deficits in parental behaviour, but this did not put their offspring at risk. Although inbred females had lower reproductive success than outbred females, this effect was not manifest in terms of lower offspring viability. Therefore, inbreeding depression manifests itself through deficits on traits of adult females other than maternal care. A possible physiological basis for these findings is hypothesized.Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article↗

PubMed2001

Self-pollination and its costs in a monoecious fig (Ficus aurea, Moraceae) in a highly seasonal subtropical environment.

The unusual floral phenology of most monoecious figs, related to their highly specialized pollination mutualism with agaonid wasps, combines pronounced dichogamy at the level of inflorescences and individuals with population-level asynchrony in flowering. This floral phenology ensures that outcrossing strongly predominates. Fig populations may thus be expected to possess deleterious recessive alleles that lead to inbreeding depression when selfing does occur. However, whether monoecious figs are self-compatible and whether selfing results in inbreeding depression have never been investigated. Using wasps as "pollination tools" and exploiting infrequent overlap in male and female phases on the same tree, we conducted controlled selfed and outcrossed pollination experiments in Ficus aurea. Our results show that this species is totally self-compatible. No negative effects of selfing could be demonstrated on syconium retention, number of vacant ovaries, seed set, or seed germination. However, wasp production had a tendency to be higher after self-pollination. While it is possible that inbreeding depression is expressed at later developmental stages, its absence at the early stages we examined is nonetheless surprising for a plant expected to be highly outcrossed. It is likely that selection pressures other than avoidance of inbreeding are responsible for the evolution and maintenance of the unusual floral phenology of figs.

Journal Article↗

PubMed2026

REVIEW: CAUSES AND CONSEQUENCES OF DOING IT WITH ONESELF-SYNTHESIS AND META-ANALYSIS OF NEODERMATAN HERMAPHRODITIC MATING SYSTEMS.

Hermaphroditic mating systems profoundly influence evolution, yet in parasitic flatworms (Neodermata) they remain strikingly understudied. For decades, sweeping claims have oscillated between pervasive selfing and near-universal outcrossing, reflecting a lack of comprehensive synthesis. This review, the first in more than 40 yr, integrates nearly a century of research, from early observational studies to modern genetic analyses, to reveal a far more nuanced picture. Our meta-analysis of population-genetic data shows a sharp departure from the bimodal selfing patterns typical of plants and other hermaphroditic animals: neodermatan parasites are strongly skewed toward outcrossing. We link variation in mating systems to parasite demography and life-history traits, especially in species exhibiting mixed mating or elevated selfing. Current evidence suggests outcrossing is common, but taxonomic and life-history gaps preclude definitive conclusions. Beyond patterns and causes, we explore evolutionary consequences ranging from fitness costs such as inbreeding depression to trait evolution, including delayed selfing, sex allocation, and complex life cycles. Evidence for inbreeding depression is mixed and limited, yet emerging approaches using selfing-rate comparisons offer promising avenues for future research. Notably, demographic constraints, such as infection intensity and life-cycle architecture, often explain mixed mating without invoking selection, challenging classical models. Similarly limited in number, studies on sex allocation indicate that hermaphroditic mating systems can shape reproductive investment, with patterns consistent with local sperm competition in some taxa. By consolidating historical observations with modern genetic insights, this review provides the most comprehensive synthesis of hermaphroditic mating systems in the Neodermata to date. We highlight critical gaps in taxonomic coverage and experimental data and point to future opportunities for integrating genomic approaches with ecological and demographic frameworks. Such integration will be essential to illuminate how mating systems shape parasite evolution and to resolve long-standing questions about the persistence of mixed mating despite theoretical expectations.

Animals↗

PubMed2002

Lethals in finite populations.

It has been assumed, based on theoretical studies, that lethals with the level of dominance estimated from experimental studies would have an allele frequency that is virtually independent of effective population size. However, here it is shown numerically that the expected frequency of lethals with low levels of dominance is also dependent on finite population size, although not as much as completely recessive lethals. This finding is significant in determining the standing level of inbreeding depression and the consequent potential for the evolution of self-fertilization. In addition, the architecture of genetic variation influencing inbreeding depression in populations with a history of small size may be of important consequence in endangered species. Finally, it is shown that the loss of lethal genetic variation often occurs much more quickly than the regeneration of lethal variation by mutation. This asymmetry may result in a lower standing genetic variation for inbreeding depression than expected from mutation rates and contemporary population size data.

Animals↗

PubMed2006

When not to avoid inbreeding.

Avoidance of incestuous matings is widely reported across many animal taxa, and the adaptive value of such behavior is explained through inbreeding depression. However, an old and somewhat neglected theoretical result predicts that inbred matings offer another, positive effect on the inclusive fitness of parents: an individual who mates with a relative will help that relative to spread genes identical by descent. This benefit can be substantial, if the additional mating achieved by the relative does not harm his mating success otherwise, and in the context of selfing in plants the phenomenon is well known. Here, we develop a model that derives expected values of inbreeding tolerance, that is, the magnitude of inbreeding depression that is required to make individuals avoid inbreeding, for different animal life histories and parental investment patterns. We also distinguish between simultaneous and sequential mate choice, and show that inbreeding tolerance should often be remarkably high in the latter scenario in particular, although egalitarian parental care will lead to lower tolerance. There is a mismatch between theory and data: the almost complete lack of cases where individuals prefer to mate incestuously is at odds with a large overlap between the predicted range of inbreeding tolerance and estimates of inbreeding depression found in nature. We discuss four different solutions to this enigma, and suggest that inbreeding tolerance, where it is found, should not always be attributed to a simple constraint that has prevented finding any other mate.

Animals↗

PubMed2000

Exploring the genetic basis and proximate causes of female fertility advantage in gynodioecious Thymus vulgaris.

In many gynodioecous species, females produce more viable seeds than hermaphrodites. Knowledge of the relative contribution of inbreeding depression in hermaphrodites and maternal sex effects to the female fertility advantage and the genetic basis of variation in female fertility advantage is central to our understanding of the evolution of gender specialization. In this study we examine the relative contribution of inbreeding and maternal sex to the female fertility advantage in gynodioecious Thymus vulgaris and quantify whether there is genetically based variation in female fertility advantage for plants from four populations. Following controlled self and outcross (sib, within-population, and between-population) pollination, females had a more than twofold fertility advantage (based on the number of germinating seeds per fruit), regardless of the population of origin and the type of pollination. Inbreeding depression on viable seed production by hermaphrodites occurred in two populations, where inbreeding had been previously detected. Biparental inbreeding depression on viable seed production occurred in three of four populations for females, but in only one population for hermaphrodites. Whereas the maternal sex effect may consistently enhance female fertility advantage, inbreeding effects may be limited to particular population contexts where inbreeding may occur. A significant family x maternal sex interaction effect on viable seed production was observed, illustrating that the extent of female fertility advantage varies significantly among families. This result is due to greater variation in hermaphrodite (relative to female) seed fertility between families. Despite this genetic variation in female fertility advantage and the highly female biased sex ratios in populations of T. vulgaris, gynodioecy is a stable polymorphism, suggesting that strong genetic and/or ecological constraints influence the stability of this polymorphism.

Analysis of Variance↗

PubMed1999

Conservation genetics of Nordic carnivores: lessons from zoos.

This paper summarizes results from genetic studies of Nordic carnivore populations bred in captivity. The conservation genetic implications of those results for the management of wild populations of the same species are discussed. Inbreeding depression has been documented in the brown bear (Ursus arctos), wolf (Canis lupus), and lynx (Lynx lynx) populations held in Nordic zoos. The characters negatively affected by inbreeding include litter size (brown bear and wolf), longevity (lynx and wolf), female reproduction, and weight (wolf). In addition, hereditary defects caused by single autosomal alleles occur in the wolf and brown bear populations. These deleterious alleles cause blindness (wolf) and albinism (brown bear) in the homozygous state. The amount of inbreeding depression observed in Nordic carnivores are similar to that documented in other species. The captive populations have the same genetic background as the current wild ones and inbreeding depression is therefore a potential threat to wild carnivore populations in Sweden. This threat is presently not being adequately recognized in the management of these species. Frequently occurring misunderstandings regarding the kind of conclusions that can be drawn from the presented genetic observations are also discussed.

Animal Husbandry↗

PubMed2001

Effects of population size and metapopulation dynamics on a mating-system polymorphism.

The evolutionary dynamics of neutral alleles under the Wright-Fisher model are well understood. Similarly, the effect of population turnover on neutral genetic diversity in a metapopulation has attracted recent attention in theoretical studies. Here we present the results of computer simulations of a simple model that considers the effects of finite population size and metapopulation dynamics on a mating-system polymorphism involving selfing and outcrossing morphs. The details of the model are based on empirical data from dimorphic populations of the annual plant Eichhornia paniculata, but the results are also of relevance to species with density-dependent selfing rates in general. In our model, the prior selfing rate is determined by two alleles segregating at a single diploid locus. After prior selfing occurs, some remaining ovules are selfed through competing self-fertilisation in finite populations as a result of random mating among gametes. Fitness differences between the mating-system morphs were determined by inbreeding depression and pollen discounting in a context-dependent manner. Simulation results showed evidence of frequency dependence in the action of pollen discounting and inbreeding depression in finite populations. In particular, as a result of selfing in outcrossers through random mating among gametes, selfers experienced a "fixation bias" through drift, even when the mating-system locus was selectively neutral. In a metapopulation, high colony turnover generally favoured the fixation of the outcrossing morph, because inbreeding depression reduced opportunities for colony establishment by selfers through seed dispersal. Our results thus demonstrate that population size and metapopulation processes can lead to evolutionary dynamics involving pollen and seed dispersal that are not predicted for large populations with stable demography.

Alleles↗

PubMed2001

Neither vegetative nor reproductive advantages account for high frequency of male-steriles in southern Spanish gynodioecious Daphne laureola (Thymelaeaceae).

In gynodioecious species, male-steriles (termed "females" hereafter) usually exhibit some reproductive advantage over hermaphrodites that allow them to compensate for the loss of male reproductive function. This compensation can result from higher fecundity, vegetative outperformance, and/or lower inbreeding depression. In this study we compared vegetative and reproductive parameters of female and hermaphrodite Daphne laureola individuals in two southeastern Spanish populations and estimated the magnitude of inbreeding depression up to the seedling emergence stage by conducting controlled pollinations and experimental sowings of seed progenies in the field. Reproductive shrubs of both sexes did not differ significantly in size, leaf production, leaf size, leaf growth, nutrient allocation to leaves, and production of flowers and fruits. Seed set and seed size of cross- and self-pollinated flowers of hermaphrodites and cross-pollinated females were also similar. Seedling emergence rates of self- and cross-pollinated seeds from hermaphrodites under natural field conditions were similar, suggesting a minor role of inbreeding depression up to that reproductive stage. Seeds from females produced more seedlings than selfed seeds from hermaphrodites. In 21 populations surveyed in the study region over a broad geographical and elevational gradient, the proportion of females ranged between 20.6 and 56.1% and was inversely related to elevation. The establishment and maintenance of females in southeastern Spanish populations of D. laureola seem to be mainly mediated by ecological factors.

Journal Article↗

PubMed2003

Effects of inbreeding on coastal Douglas fir growth and yield in operational plantations: a model-based approach.

In advanced generation seed orchards, tradeoffs exist between genetic gain obtained by selecting the best related individuals for seed orchard populations, and potential losses due to subsequent inbreeding between these individuals. Although inbreeding depression for growth rate is strong in most forest tree species at the individual tree level, the effect of a small proportion of inbreds in seed lots on final stand yield may be less important. The effects of inbreeding on wood production of mature stands cannot be assessed empirically in the short term, thus such effects were simulated for coastal Douglas fir [ Pseudotsuga menziesii var. menziesii (Mirb.) Franco] using an individual-tree growth and yield model TASS (Tree and Stand Simulator). The simulations were based on seed set, nursery culling rates, and 10-year-old field test performance for trees resulting from crosses between unrelated individuals and for inbred trees produced through mating between half-sibs, full-sibs, parents and offspring and self-pollination. Results indicate that inclusion of a small proportion of related clones in seed orchards will have relatively low impacts on stand yields due to low probability of related individuals mating, lower probability of producing acceptable seedlings from related matings than from unrelated matings, and a greater probability of competition-induced mortality for slower growing inbred individuals than for outcrossed trees. Thus, competition reduces the losses expected due to inbreeding depression at harvest, particularly on better sites with higher planting densities and longer rotations. Slightly higher breeding values for related clones than unrelated clones would offset or exceed the effects of inbreeding resulting from related matings. Concerns regarding the maintenance of genetic diversity are more likely to limit inclusion of related clones in orchards than inbreeding depression for final stand yield.

Analysis of Variance↗

PubMed2003

Microsatellite measures of inbreeding: a meta-analysis.

Meta-analyses of published and unpublished correlations between phenotypic variation and two measures of genetic variation at microsatellite loci, multilocus heterozygosity (MLH) and mean d2, revealed that the strength of these associations are generally weak (mean r < 0.10). Effects on life-history trait variation were significantly greater than zero for both measures over all reported effect sizes (r = 0.0856 and 0.0479 for MLH and mean d2, respectively), whereas effects on morphometric traits were not (r = 0.0052 and r = 0.0038), which is consistent with the prediction that life-history traits exhibit greater inbreeding depression than morphometric traits. Effect sizes reported using mean d2 were smaller and more variable than those reported using MLH, suggesting that MLH may be a better metric for capturing inbreeding depression most of the time. However, analyses of paired effect sizes reported using both measures from the same data did not differ significantly. Several lines of evidence suggest that published effects sizes are upwardly biased. First, effect sizes from published studies were significantly higher than those reported in unpublished studies. Second, fail-safe numbers for reported effect sizes were generally quite low, with the exception of correlations between MLH and life-history traits. Finally, the slope of the regression of effect size on sample size was negative for most sets of traits. Taken together, these results suggest that studies designed to detect inbreeding depression on a life-history trait using microsatellites will need to sample in excess of 600 individuals to detect an average effect size (r = 0.10) with reasonable statistical power (0.80). Very few published studies have used samples sizes approaching this value.

Body Weights and Measures↗

PubMed2000

Predicting response to selection on a quantitative trait: a comparison between models for mixed-mating populations.

Two different theoretical frameworks have been developed to predict response to selection in a mixed mating population (in which reproduction occurs by a mixture of outcrossing and self-fertilization). The genotypic covariance model (GCM) and the structured linear model (SLM) rely on the same assumptions regarding quantitative trait inheritance, but use different genetic summary statistics. Here, we demonstrate the algebraic relationships between the various genetic metrics used in each theory. This is accomplished by reformulating the GCM in terms of the Wright-Kempthorne equation. We use stochastic simulations to investigate the relative accuracy of each theory for a range of selfing rates. The SLM is generally more accurate than the GCM, the most pronounced differences emerging in simulations with inbreeding depression for fitness. In fact, with strong inbreeding depression and high selfing rates, evolution can occur opposite the direction predicted by the GCM. The simulations also indicate that direct application of random mating models to partially selfing populations can produce very inaccurate predictions if quantitative trait loci exhibit dominance.

Animals↗

PubMed2005

Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly.

Inbreeding depression is most pronounced for traits closely associated with fitness. The traditional explanation is that natural selection eliminates deleterious mutations with additive or dominant effects more effectively than recessive mutations, leading to directional dominance for traits subject to strong directional selection. Here we report the unexpected finding that, in the butterfly Bicyclus anynana, male sterility contributes disproportionately to inbreeding depression for fitness (complete sterility in about half the sons from brother-sister matings), while female fertility is insensitive to inbreeding. The contrast between the sexes for functionally equivalent traits is inconsistent with standard selection arguments, and suggests that trait-specific developmental properties and cryptic selection play crucial roles in shaping genetic architecture. There is evidence that spermatogenesis is less developmentally stable than oogenesis, though the unusually high male fertility load in B. anynana additionally suggests the operation of complex selection maintaining male sterility recessives. Analysis of the precise causes of inbreeding depression will be needed to generate a model that reliably explains variation in directional dominance and reconciles the gap between observed and expected genetic loads carried by populations. This challenging evolutionary puzzle should stimulate work on the occurrence and causes of sex differences in fertility load.

Animals↗