Inbreeding depression of sperm traits in the zebra finch Taeniopygia guttata

Inbreeding depression, or the reduction in fitness due to mating between close relatives, is a key issue in biology today. Inbreeding negatively affects many fitness‐related traits, including survival and reproductive success. Despite this, very few studies have quantified the effects of inbreeding on vertebrate gamete traits under controlled breeding conditions using a full‐sib mating approach. Here, we provide comprehensive evidence for the negative effect of inbreeding on sperm traits in a bird, the zebra finch Taeniopygia guttata. We compared sperm characteristics of both inbred (pedigree F = 0.25) and outbred (pedigree F = 0) individuals from two captive populations, one domesticated and one recently wild‐derived, raised under standardized conditions. As normal spermatozoa morphology did not differ consistently between inbred and outbred individuals, our study confirms the hypothesis that sperm morphology is not particularly susceptible to inbreeding depression. Inbreeding did, however, lead to significantly lower sperm motility and a substantially higher percentage of abnormal spermatozoa in ejaculate. These results were consistent across both study populations, confirming the generality and reliability of our findings.     

FITNESS CONSEQUENCES OF OUTCROSSING IN A SOCIAL SPIDER WITH AN INBREEDING MATING SYSTEM

Inbreeding mating systems are uncommon because of inbreeding depression. Mating among close relatives can evolve, however, when outcrossing is constrained. Social spiders show obligatory mating among siblings. In combination with a female‐biased sex ratio, sib‐mating results in small effective populations. In such a system, high genetic homozygosity is expected, and drift may cause population divergence. We tested the effect of outcrossing in the social spider Stegodyphus dumicola. Females were mated to sib‐males, to a non‐nestmate within the population, or to a male from a distant population, and fitness traits of F1s were compared. We found reduced hatching success of broods from between‐population crosses, suggesting the presence of population divergence at a large geographical scale that may result in population incompatibility. However, a lack of a difference in offspring performance between inbred and outbred crosses indicates little genetic variation between populations, and could suggest recent colonization by a common ancestor. This is consistent with population dynamics of frequent colonizations by single sib‐mated females of common origin, and extinctions of populations after few generations. Although drift or single mutations can lead to population divergence at a relatively short time scale, it is possible that dynamic population processes homogenize these effects at longer time scales.     

Scope for genetic enhancement of the parasitisation potential of four native strains of Trichogrammatoidea sp. nr. lutea Girault (Hymenoptera: Trichogrammatidae) in Kenya

In response to emerging interest in commercial mass production of Trichogramma for Helicoverpa armigera biocontrol in eastern Africa, laboratory experiments were undertaken to assess the scope for genetic enhancement of the parasitisation potential of native strains of the local common trichogrammatid species, Trichogrammatoidea sp. nr. lutea. Four promising strains (ex-Kilifi – Kilifi District, ex-Kwa Chai – Kibwezi District, ex-Rarieda – Bondo District and ex-Ebuhayi, Kakamega District) were tested for cross-mating in reciprocal combinations with focus on fecundity and progeny female ratio. While all the crosses resulted in F1 progeny of both sexes, significant differences were observed between homogamic and reciprocal heterogamic crosses in fecundity, progeny production, proportion of female progeny and adult longevity. Among all the crosses, the cross between ex-Rarieda strain females and ex-Kilifi strain males resulted in progeny that was significantly superior in fecundity and progeny female ratio. Conversely, Kilifi strain females crossed to males from ex-Rarieda strain gave rise to progeny with relatively low fecundity and female ratio. There were significant differences between homogamic crosses and most reciprocal heterogamic crosses in the major biological attributes. Genotypic and phenotypic variance-covariance matrices generated for six life-history traits showed high positive correlations for most traits in both inbred (P<0.05) and reciprocal heterogamic crosses (P<0.05 and P<0.001). Fecundity and number of female offspring were the most important factors in the heterogamic crosses. The results confirmed the scope for genetic enhancement through inter-strain crossing for improving the field impact potential of T. sp. nr. lutea being targeted for commercial mass production.     

Intergenerational effects of inbreeding in Nicrophorus vespilloides: offspring suffer fitness costs when either they or their parents are inbred

Inbreeding depression is the reduction in fitness caused by mating between related individuals. Inbreeding is expected to cause a reduction in offspring fitness when the offspring themselves are inbred, but outbred individuals may also suffer a reduction in fitness when they depend on care from inbred parents. At present, little is known about the significance of such intergenerational effects of inbreeding. Here, we report two experiments on the burying beetle Nicrophorus vespilloides, an insect with elaborate parental care, in which we investigated inbreeding depression in offspring when either the offspring themselves or their parents were inbred. We found substantial inbreeding depression when offspring were inbred, including reductions in hatching success of inbred eggs and survival of inbred offspring. We also found substantial inbreeding depression when parents were inbred, including reductions in hatching success of eggs produced by inbred parents and survival of outbred offspring that received care from inbred parents. Our results suggest that intergenerational effects of inbreeding can have substantial fitness costs to offspring, and that future studies need to incorporate such costs to obtain accurate estimates of inbreeding depression.     

Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster

Summary This experiment was designed to study the relationship between rate of inbreeding and observed inbreeding depression of larval viability, adult fecundity and cold shock mortality in Drosophila melanogaster. Rates of inbreeding used were full-sib mating and closed lines of N=4 and N=20. Eight generations of mating in the N=20 lines, three generations in the N=4 lines and one generation of full-sib mating were synchronised to simultaneously produce individuals with an expected level of inbreeding coefficient (F) of approximately 0.25. Inbreeding depression for the three traits was significant at F=0.25. N=20 lines showed significantly less inbreeding depression than full-sib mated lines for larval viability at approximately the same level of F. A similar trend was observed for fecundity. No effect of rate of inbreeding depression was found for cold shock mortality, but this trait was measured with less precision than the other two. Natural selection acting on loci influencing larval viability and fecundity during the process of inbreeding could explain these results. Selection is expected to be more effective with slow rates of inbreeding because there are more generations and greater opportunity for selection to act before F=0.25 is reached. Selection intensities seem to have been different in the three traits measured. Selection was most intense for larval viability, less intense for fecundity and, perhaps, negligible at loci influencing cold shock mortality.     

Strong inbreeding depression in male mating behaviour in a poeciliid fish

The magnitude of inbreeding depression is often larger in traits closely related to fitness, such as survival and fecundity, compared to morphological traits. Reproductive behaviour is also closely associated with fitness, and therefore expected to show strong inbreeding depression. Despite this, little is known about how reproductive behaviour is affected by inbreeding. Here we show that one generation of full‐sib mating results in a decrease in male reproductive performance in the least killifish (Heterandria formosa). Inbred males performed less gonopodial thrusts and thrust attempts than outbred males (δ = 0.38). We show that this behaviour is closely linked with fitness as gonopodial performance correlates with paternity success. Other traits that show inbreeding depression are offspring viability (δ = 0.06) and maturation time of males (δ = 0.19) and females (δ = 0.14). Outbred matings produced a female biased sex ratio whereas inbred matings produced an even sex ratio.     

Life-history plasticity and inbreeding depression under mate limitation and predation risk: cumulative lifetime fitness dissected with a life table response experiment

Environmental effects on the evolution of mating systems are increasingly discussed, but we lack many examples of how environmental conditions affect the expression and consequences of alternative mating systems. Variation in mate availability sets up a trade-off between reproductive assurance and inbreeding depression, but the consequences of both mate limitation and inbreeding may depend on other environmental conditions. Predation risk is common under natural conditions, and known to affect allocation to reproduction, but we know little about the effects of isolation and inbreeding under predation risk. We reared selfed and outcrossed hermaphroditic freshwater snails (Physa acuta) in four environments (predator cues present or absent crossed with mating partners available or not) and quantified life-history traits and cumulative lifetime fitness. Our results confirm that isolation from mates can increase longevity and growth, resulting in higher lifetime fecundity. Thus, we observed no evidence for mate limitation of reproduction. However, reproduction under isolation (i.e., selfing) resulted in inbreeding depression, which should counteract the benefits of selfing. Inbreeding depression in fitness occurred in both predator and no-predator environments, but there was no overall change in inbreeding depression with predator cues. This represents, to our knowledge, the first empirical estimate of the effect of predation risk on inbreeding depression in an animal. Cumulative fitness was most influenced by early survival and especially early fecundity. As predation risk and inbreeding (both ancestral and due to a lack of mates) reduced early fecundity, these effect are predicted to have important contributions to population growth under natural conditions. Therefore life-history plasticity (e.g., delayed reproduction) is likely to be very important to overall fitness.     

The effect of inbreeding on natural selection in a seed‐feeding beetle

Little is known about how inbreeding alters selection on ecologically relevant traits. Inbreeding could affect selection by changing the distribution of traits and/or fitness, or by changing the causal effect of traits on fitness. Here, I test whether selection on egg size varies with the degree of inbreeding in the seed‐feeding beetle, Stator limbatus. There was strong directional selection favoring large eggs for both inbred and outbred beetles; offspring from smaller eggs had lower survivorship on a resistant host. Inbreeding treatment had no effect on the magnitude of selection on egg size; all selection coefficients were between ~0.078 and 0.096, regardless of treatment. However, inbreeding depression declined with egg size; this is because the difference in fitness between inbreds and outbreds did not change, but average fitness increased, with egg size. A consequence of this is that populations that differ in mean egg size should experience different magnitudes of inbreeding depression (all else being equal) and thus should differ in the magnitude of selection on traits that affect mating, simply as a consequence of variation in egg size. Also, maternal traits (such as egg size) that mediate stressfulness of the environment for offspring can mediate the severity of inbreeding depression.     

Inbreeding,inbreeding depression and extinction

Inbreeding is unavoidable in small, isolated populations and can cause substantial fitness reductions compared to outbred populations. This loss of fitness has been predicted to elevate extinction risk giving it substantial conservation significance. Inbreeding may result in reduced fitness for two reasons: an increased expression of deleterious recessive alleles (partial dominance hypothesis) or the loss of favourable heterozygote combinations (overdominance hypothesis). Because both these sources of inbreeding depression are dependent upon dominance variance, inbreeding depression is predicted to be greater in life history traits than in morphological traits. In this study we used replicate inbred and control lines of Drosophila simulans to address three questions:1) is inbreeding depression greater in life history than morphological traits? 2) which of the two hypotheses is the major underlying cause of inbreeding depression? 3) does inbreeding elevate population extinction risk? We found that inbreeding depression was significantly greater in life history traits compared to morphological traits, but were unable to find unequivocal support for either the overdominance or partial dominance hypotheses as the genetic basis of inbreeding depression. As predicted, inbred lines had a significantly greater extinction risk.     

Inbreeding and courtship calling in the cricket Teleogryllus commodus

Male field crickets produce two acoustic signals for mating: advertisement calls and courtship calls. While the importance of advertisement calling in mate attraction is well understood, the function of courtship calling is less clear. Here, we tested if the courtship call of male crickets Teleogryllus commodus signals aspects of male quality by comparing the calls of inbred and outbred males. We examined the effect of one generation of full sibling mating on fine‐scale call structure, along with several life history traits. Inbreeding reduced nymph survival but had no significant effect on weight or development time. Inbreeding resulted in a small but significant change in two of the six call parameters measured. We then tested if inbreeding affects call trait combinations that are important to females by using the results of a previous selection analysis to compare the multivariate attractiveness of the calls of inbred and outbred males. There was no difference. We conclude that the courtship call of T. commodus is not a reliable signal of aspects of male quality that are affected by inbreeding (which generally reduces fitness‐enhancing traits). It might, however, signal components of male fitness that are not affected by changes in heterozygosity.     

Outbreeding effects in an inbreeding insect,Cimex lectularius

In some species, populations with few founding individuals can be resilient to extreme inbreeding. Inbreeding seems to be the norm in the common bed bug, Cimex lectularius, a flightless insect that, nevertheless, can reach large deme sizes and persist successfully. However, bed bugs can also be dispersed passively by humans, exposing inbred populations to gene flow from genetically distant populations. The introduction of genetic variation through this outbreeding could lead to increased fitness (heterosis) or be costly by causing a loss of local adaptation or exposing genetic incompatibility between populations (outbreeding depression). Here, we addressed how inbreeding within demes and outbreeding between distant populations impact fitness over two generations in this re‐emerging public health pest. We compared fitness traits of families that were inbred (mimicking reproduction following a founder event) or outbred (mimicking reproduction following a gene flow event). We found that outbreeding led to increased starvation resistance compared to inbred families, but this benefit was lost after two generations of outbreeding. No other fitness benefits of outbreeding were observed in either generation, including no differences in fecundity between the two treatments. Resilience to inbreeding is likely to result from the history of small founder events in the bed bug. Outbreeding benefits may only be detectable under stress and when heterozygosity is maximized without disruption of coadaptation. We discuss the consequences of these results both in terms of inbreeding and outbreeding in populations with genetic and spatial structuring, as well as for the recent resurgence of bed bug populations.     

Plant chemistry underlies herbivore‐mediated inbreeding depression in nature

The cost of inbreeding (inbreeding depression, ID) is an important variable in the maintenance of reproductive variation. Ecological interactions such as herbivory could modulate this cost, provided that defence traits harbour deleterious mutations and herbivores are responsible for differences in fitness. In the field, we manipulated the presence of herbivores on experimentally inbred and outcrossed plants of Solanum carolinense (horsenettle) for three years. Damage was greater on inbred plants, and ID for growth and fitness was significantly greater under herbivory. Inbreeding reduced phenolic expression both qualitatively (phytochemical diversity) and quantitatively, indicating deleterious load at loci related to the biosynthesis of defence compounds. Our results indicate that inbreeding effects on plant–herbivore interactions are mediated by changes to functional plant metabolites, suggesting that variation in inbreeding could be a predictor of defence trait variation. The magnitude of herbivore‐mediated, ecological ID indicates that herbivores could maintain outcrossing mating systems in nature.     

FITNESS CONSEQUENCES OF MATERNAL AND NONMATERNAL COMPONENTS OF INBREEDING IN THE GYNODIOECIOUS PHACELIA DUBIA

I assessed the relationship between the level of inbreeding, F, and fitness, and the effects of nonmaternal and maternal components of inbreeding on fitness in Phacelia dubia. I conducted two generations of controlled crosses and tested the performance of the F₂ progeny in field and artificial conditions covering the whole life cycle. Inbreeding significantly decreased the individual contribution of seeds to the next generation in the field, but this decrease apparently is not enough to explain the maintenance of gynodioecy. The inbred progeny contributes significantly to the population genetic structure of P. dubia. Fitness estimates and fitness components tended to decrease, usually monotonically, with F. However, nonmonotonic relationships were found in male fitness components and, in some families, in fitness estimates, seed production per fruit, and establishment. Most of the inbreeding depression takes place at the level of seed establishment in the field, but, in artificial conditions the effects of inbreeding were similar at fecundity and establishment. I studied maternal and nonmaternal components of inbreeding by testing the effects of the relatedness of maternal grandparents and parents on the performance of the progeny. Both components affected fitness. Inbreeding depression was conditioned by the level of inbreeding of the maternal plant, but this interaction varied at different fitness components. Also, the magnitude and even the direction of the relationship between fitness and F changed as a result of the combined effects of maternal and nonmaternal components of inbreeding. Such interactions can render convex or concave fitness functions, giving in the latter case the appearance of a false purging. Maternal effects of inbreeding can result from several processes: maternal investment perhaps with serial adjustments during seed development, purging of recessive deleterious genes, and nucleocytoplasmic interactions. These results illustrate the importance of maternal effects of inbreeding, and the complex effects of inbreeding on fitness. A full understanding of the fitness consequences of inbreeding and, therefore, their potential implications in the evolution of breeding systems, should take into account male and female components as well as transgenerational effects in the context of the particular environment in which fitness is evaluated.     

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

Inbreeding is widely hypothesized to shape mating systems and population persistence, but such effects will depend on which traits show inbreeding depression. Population and evolutionary consequences could be substantial if inbreeding decreases sperm performance and hence decreases male fertilization success and female fertility. However, the magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding. Further, the hypothesis that inbreeding could increase within‐ejaculate variation in sperm traits and thereby further affect male fertilization success has not been explicitly tested. We used a wild pedigreed song sparrow (Melospiza melodia) population, where frequent extrapair copulations likely create strong postcopulatory competition for fertilization success, to quantify effects of male coefficient of inbreeding (f) on key sperm performance traits. We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within‐ejaculate variance in sperm velocity did not increase with male f. Contrary to inferences from highly inbred captive and experimental populations, our results imply that moderate inbreeding will not necessarily constrain sperm performance in wild populations. Consequently, the widely observed individual‐level and population‐level inbreeding depression in male and female fitness may not stem from reduced sperm performance in inbred males.     

SEX RATIO VARIATION IN A PARASITIC WASP II. DIALLEL CROSS

Sex ratio has been studied from many theoretical and empirical perspectives, but a general assumption in sex ratio research is that changes in sex ratio occur because of selection on sex ratio itself. I carried out a quantitative genetic experiment—a diallel cross among three strains—on a parasitic wasp, Muscidifurax raptor (Hymenoptera: Pteromalidae), to measure genetic variation for sex ratio. I also tested whether sex ratio may change as a consequence of selection on other life-history traits by estimating genetic covariances between sex ratio, fecundity, longevity, and development time. Most of the variation among strains could be accounted for by a maternal effect, likely caused by a microsporidian parasite that was transmitted through the West Germany (WG) strain. Genetic variation was small by comparison, but almost all traits were affected by dominance. The only significant additive genetic effect was for fecundity early in life. Upon crossing, all traits displayed heterosis: more female-biased sex ratio, greater fecundity, longer life, and faster development time. All life-history traits were correlated phenotypically, but the correlations were mainly the result of decreased performance in crosses with the WG strain that carried the microsporidian parasite. Dominance genetic correlations were also found between sex ratio, fecundity, and longevity. How the correlation between sex ratio and other life-history traits would affect sex ratio evolution depends upon the frequencies of sex-ratio genotypes within a population as well as the signs of the correlations, because sex ratio is under frequency-dependent selection whereas other traits are generally under directional selection. Although the results from crosses among laboratory populations should be approached with caution, the inbreeding depression (the difference between inbred and outcrossed progeny) found in M. raptor implies that the evolution of a female-biased sex ratio could be affected by selection for inbreeding avoidance.     

Effects of inbreeding on aversive learning in Drosophila

Inbreeding adversely affects life history traits as well as various other fitness‐related traits, but its effect on cognitive traits remains largely unexplored, despite their importance to fitness of many animals under natural conditions. We studied the effects of inbreeding on aversive learning (avoidance of an odour previously associated with mechanical shock) in multiple inbred lines of Drosophila melanogaster derived from a natural population through up to 12 generations of sib mating. Whereas the strongly inbred lines after 12 generations of inbreeding (0.75 < F < 0.93) consistently showed reduced egg‐to‐adult viability (on average by 28%), the reduction in learning performance varied among assays (average = 18% reduction), being most pronounced for intermediate conditioning intensity. Furthermore, moderately inbred lines (F = 0.38) showed no detectable decline in learning performance, but still had reduced egg‐to‐adult viability, which indicates that overall inbreeding effects on learning are mild. Learning performance varied among strongly inbred lines, indicating the presence of segregating variance for learning in the base population. However, the learning performance of some inbred lines matched that of outbred flies, supporting the dominance rather than the overdominance model of inbreeding depression for this trait. Across the inbred lines, learning performance was positively correlated with the egg‐to‐adult viability. This positive genetic correlation contradicts a trade‐off observed in previous selection experiments and suggests that much of the genetic variation for learning is owing to pleiotropic effects of genes affecting functions related to survival. These results suggest that genetic variation that affects learning specifically (rather than pleiotropically through general physiological condition) is either low or mostly due to alleles with additive (semi‐dominant) effects.     

Plasmid macro-evolution: selection of deletions during adaptation in a nutrient-limited environment

A study was made of the intra-and inter-population variability of the main traits involved in Trichogramma (T. brassicae and T. cacoeciae) efficiency in host exploitation: longevity, fecundity, progeny viability, progeny sex ratio and progeny allocation. The analysis of isofemale strains shows that differences in progeny viability, progeny sex ratio and progeny allocation are transmissible and relatively stable over two successive generations. Comparison of three strains of T. brassicae originating from different locations, demonstrates differences in fecundity, progeny sex ratio and progeny allocation. Differences in host exploitation strategies also exist between two sympatric populations of T. brassicae and T. cacoeciae. No significant correlation appears between the traits which discriminate populations. The ecological and evolutionary significance and the agronomical importance of the results are discussed.     

STRONG INBREEDING DEPRESSION IN TWO SCANDINAVIAN POPULATIONS OF THE SELF‐INCOMPATIBLE PERENNIAL HERB ARABIDOPSIS LYRATA

Inbreeding depression is a key factor influencing mating system evolution in plants, but current understanding of its relationship with selfing rate is limited by a sampling bias with few estimates for self‐incompatible species. We quantified inbreeding depression (δ) over two growing seasons in two populations of the self‐incompatible perennial herb Arabidopsis lyrata ssp. petraea in Scandinavia. Inbreeding depression was strong and of similar magnitude in both populations. Inbreeding depression for overall fitness across two seasons (the product of number of seeds, offspring viability, and offspring biomass) was 81% and 78% in the two populations. Chlorophyll deficiency accounted for 81% of seedling mortality in the selfing treatment, and was not observed among offspring resulting from outcrossing. The strong reduction in both early viability and late quantitative traits suggests that inbreeding depression is due to deleterious alleles of both large and small effect, and that both populations experience strong selection against the loss of self‐incompatibility. A review of available estimates suggested that inbreeding depression tends to be stronger in self‐incompatible than in self‐compatible highly outcrossing species, implying that undersampling of self‐incompatible taxa may bias estimates of the relationship between mating system and inbreeding depression.     

INBREEDING: ITS EFFECT ON RESPONSE TO SELECTION FOR PUPAL WEIGHT AND THE HERITABLE VARIANCE IN FITNESS IN THE FLOUR BEETLE,TRIBOLIUM CASTANEUM

We report our studies of the effect of inbreeding on the response to selection for increased pupal weight in the flour beetle, Tribolium castaneum. We also report the effects of inbreeding and selection for pupal weight on the heritable variation in fitness and fitness components. We created replicate and independent inbred lines with F-values of 0.00, 0.375, and 0.672, by 0, 2, and 5 generations, respectively, of brother-sister mating of adult beetles from an outbred stock population. Subsequently, we imposed artificial within-family selection for increased pupal weight in each of 15 inbred lines for eight generations; each line had its own paired, unselected control. We compared the response to selection across the three levels of inbreeding with theoretical expectation, and investigated the effects of inbreeding and selection on fitness variation among families within all 30 selected and control lines. Among-line variation in pupal weight increased with increased inbreeding prior to selection but diminished with directional selection. Inbreeding reduced the realized heritability of pupal weight concordant with quantitative predictions of additive theory. Mean fitness, measured in several ways, declined with inbreeding and declined further with selection. In contrast, the genetic variation for fitness in the inbred and selected lines lines equalled or exceeded that of the outbred controls. Our results suggest that inbreeding and selection may affect traits in different ways depending on the relative amounts of additive and nonadditive genetic variation.     

Inbreeding and inbreeding depression of early life traits in a cooperative mammal

Mating between relatives often results in negative fitness consequences or inbreeding depression. However, the expression of inbreeding in populations of wild cooperative mammals and the effects of environmental, maternal and social factors on inbreeding depression in these systems are currently not well understood. This study uses pedigree‐based inbreeding coefficients from a long‐term study of meerkats (Suricata suricatta) in South Africa to reveal that 44% of the population have detectably non‐zero (F > 0) inbreeding coefficients. 15% of these inbred individuals were the result of moderate inbreeding (F ≥ 0.125), although such inbreeding events almost solely occurred when mating individuals had no prior experience of each other. Inbreeding depression was evident for a range of traits: pup mass at emergence from the natal burrow, hind‐foot length, growth until independence and juvenile survival. However, we found no evidence of significant inbreeding depression for skull and forearm length or for pup survival. This research provides a rare investigation into inbreeding in a cooperative mammal, revealing high levels of inbreeding, considerable negative consequences and complex interactions with the social environment.