CORRELATED INBREEDING AMONG RELATIVES: OCCURRENCE,MAGNITUDE, AND IMPLICATIONS

Understanding the magnitude and causes of genetic and phenotypic resemblance among relatives is key to understanding evolutionary processes. Contrary to basic expectation, individual coefficients of inbreeding ( f) were recently hypothesized to be intrinsically correlated across parents and offspring in structured populations, potentially creating an additional source of phenotypic resemblance in traits that show inbreeding depression. To test this hypothesis, we used individual‐based simulations to quantify the parent–offspring correlations in f arising under random mating in populations of different size, immigration rate, and mating system. Parent–offspring correlations in f were typically positive (median r≈ 0.2–0.4) in relatively small and isolated populations. Relatively inbred parents therefore produced relatively inbred offspring on average, although the magnitude of this effect varied considerably among replicate populations. Correlations were higher given more generations of random mating, greater variance in reproductive success, polygynous rather than monogamous mating, and for midparent–offspring rather than parent–offspring relationships. Furthermore, f was also positively correlated across half‐siblings, and closer relatives had more similar inbreeding coefficients across entire generations. Such intrinsic resemblance in f among relatives could provide an additional genetic benefit of mate choice and bias quantitative genetic analyses that do not account for correlated inbreeding depression.     

Resolving the conundrum of inbreeding depression but no inbreeding avoidance: Estimating sex‐specific selection on inbreeding by song sparrows (Melospiza melodia)

Inbreeding avoidance among interacting females and males is not always observed despite inbreeding depression in offspring fitness, creating an apparent “inbreeding paradox.” This paradox could be resolved if selection against inbreeding was in fact weak, despite inbreeding depression. However, the net magnitude and direction of selection on the degree to which females and males inbreed by pairing with relatives has not been explicitly estimated. We used long‐term pedigree data to estimate phenotypic selection gradients on the degree of inbreeding that female and male song sparrows (Melospiza melodia) expressed by forming socially persistent breeding pairs with relatives. Fitness was measured as the total numbers of offspring and grand offspring contributed to the population, and as corresponding expected numbers of identical‐by‐descent allele copies, thereby accounting for variation in offspring survival, reproduction, and relatedness associated with variation in parental inbreeding. Estimated selection gradients on the degree to which individuals paired with relatives were weakly positive in females, but negative in males that formed at least one socially persistent pairing. However, males that paired had higher mean fitness than males that remained socially unpaired. These analyses suggest that net selection against inbreeding may be weak in both sexes despite strong inbreeding depression, thereby resolving the “inbreeding paradox.”     

Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation

Numerous studies have reported associations between heterozygosity in microsatellite markers and fitness-related traits (heterozygosity-fitness correlations, HFCs). However, it has often been questioned whether HFCs reflect general inbreeding depression, because a small panel of microsatellite markers does not reflect very well an individual's inbreeding coefficient (F) as calculated from a pedigree. Here, we challenge this prevailing view. Because of chance events during Mendelian segregation, an individual's realized proportion of the genome that is identical by descent (IBD) may substantially deviate from the pedigree-based expectation (i.e. F). This Mendelian noise may result in a weak correlation between F and multi-locus heterozygosity, but this does not imply that multi-locus heterozygosity is a bad estimator of realized IBD. We examined correlations between 11 fitness-related traits measured in up to 1192 captive zebra finches and three measures of inbreeding: (i) heterozygosity across 11 microsatellite markers, (ii) heterozygosity across 1359 single-nucleotide polymorphism (SNP) markers and (iii) F, based on a 5th-generation pedigree. All 11 phenotypic traits showed positive relationships with measures of heterozygosity, especially traits that are most closely related to fitness. Remarkably, the small panel of microsatellite markers produced equally strong HFCs as the large panel of SNP markers. Both marker-based approaches produced stronger correlations with phenotypes than the pedigree-based F, and this did not seem to result from the shortness of our pedigree. We argue that a small panel of microsatellites with high allelic richness may better reflect an individual's realized IBD than previously appreciated, especially in species like the zebra finch, where much of the genome is inherited in large blocks that rarely experience cross-over during meiosis.     

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice

Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living song sparrows (Melospiza melodia), individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female song sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.     

Inbreeding in the greater white-toothed shrew, Crocidura russula

We combined mark-and-recapture studies with genetic techniques of parentage assignment to evaluate the interactions between mating, dispersal, and inbreeding, in a free-ranging population of Crocidura russula. We found a pattern of limited and female-biased dispersal, followed by random mating within individual neighborhoods. This results in significant inbreeding at the population level: mating among relatives occurs more often than random, and F(IT) analyses reveal significant deficits in heterozygotes. However, related mating partners were not less fecund, and inbred offspring had no lower lifetime reproductive output. Power analyses show these negative results to be quite robust. Absence of phenotypic evidence of inbreeding depression might result from a history of purging: local populations are small and undergo disequilibrium gene dynamics. Dispersal is likely caused by local saturation and (re)colonization of empty breeding sites, rather than inbreeding avoidance.     

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.     

Similar Performance of Diploid and Haploid Males in an Ant Species without Inbreeding Avoidance

Under haplodiploidy, a characteristic trait of all Hymenoptera, females develop from fertilised eggs, and males from unfertilised ones. Males are therefore typically haploid. Yet, inbreeding can lead to the production of diploid males that often fail in development, are sterile or are of lower fertility. In most Hymenoptera, inbreeding is avoided by dispersal flights of one or both sexes, leading to low diploid male loads. We investigated causes for the production of diploid males and their performance in a highly inbred social Hymenopteran species. In the ant Hypoponera opacior, inbreeding occurs between wingless sexuals, which mate within the mother nest, whereas winged sexuals outbreed during mating flights earlier in the season. Wingless males mate with queen pupae and guard their mating partners. We found that they mated randomly with respect to relatedness, indicating that males do not avoid mating with close kin. These frequent sib‐matings lead to the production of diploid males, which are able to sire sterile triploid offspring. We compared mating activity and lifespan of haploid and diploid wingless males. As sexual selection acts on the time of emergence and body size in this species, we also investigated these traits. Diploid males resembled haploid ones in all investigated traits. Hence, albeit diploid males cannot produce fertile offspring, they keep up with haploid males in their lifetime mating success. Moreover, by fathering viable triploid workers, they contribute to the colonies' work force. In conclusion, the lack of inbreeding avoidance led to frequent sib‐matings of wingless sexuals, which in turn resulted in the regular production of diploid males. However, in contrast to many other Hymenopteran species, diploid males exhibit normal sexual behaviour and sire viable, albeit sterile daughters.     

Variation in parent–offspring kinship in socially monogamous systems with extra‐pair reproduction and inbreeding

Female extra‐pair reproduction in socially monogamous systems is predicted to cause cuckolded socially‐paired males to conditionally reduce paternal care, causing selection against extra‐pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially‐paired female and/or to her extra‐pair mate, and therefore be related to extra‐pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra‐pair reproduction, might then be weakened. We derive metrics that quantify allele‐sharing between within‐pair and extra‐pair offspring and their mother and her socially‐paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra‐pair reproduction and inbreeding on a brood's total allelic value to its socially‐paired parents. Cuckolded male song sparrows were almost always detectably related to extra‐pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra‐pair reproduction, this decrease was reduced by within‐pair and extra‐pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra‐pair reproduction, parental care, and inbreeding.     

Inbreeding avoidance in rhesus macaques: Whose choice?

Whether nonhuman primates avoid copulating with close kin living in their social group is controversial. If sexual aversion to relatives occurs, it should be stronger in females than in males because of females' greater investment in each offspring and hence greater costs resulting from less viable offspring. Data presented here show that adult male rhesus macaques breeding in their natal groups at Cayo Santiago experienced high copulatory success, but copulated less with females of their own matrilineages than with females of other matrilineages. Adult females were never observed to copulate with males of their own matrilineage during their fertile periods. Although natal males sometimes courted their relatives, examination of two measures of female mate choice showed that females chose unrelated natal males over male kin. Female aversion to male kin was specific to the sexual context; during the birth season, females did not discriminate against their male relatives in distributing grooming. Evolved inbreeding avoidance mechanisms probably produce different outcomes at Cayo Santiago than in wild rhesus macaque populations. Gender differences in sexual aversion to relatives may be partly responsible for differences between studies in reported frequency of copulations by related pairs. © 1993 Wiley-Liss, Inc.     

Inbreeding Depression and Inbreeding Avoidance in a Natural Population of Guppies (Poecilia reticulata)

Maintenance of genetic variation in the face of strong natural selection is a long‐standing problem in evolutionary biology. One of the most extreme examples of within‐population variation is the polymorphic, genetically determined color pattern of male Trinidad guppies (Poecilia reticulata). Female mating preference for rare or novel patterns has been implicated as a factor in maintaining this variation. The origin of this preference is not understood, although inbreeding avoidance has been proposed as a mechanism. Inbreeding avoidance is advantageous when populations exhibit inbreeding depression and the opportunity for mating between relatives exists. To determine whether these conditions are met in a natural guppy population, we assessed mating and reproductive patterns using polymorphic molecular markers. Females produced more offspring with less‐related males than with more‐related ones. In addition, females were more likely to have mated with less‐related males, but this trend was only marginally significant. Male heterozygosity was positively correlated with mating success and with the number of offspring sired, consistent with strong inbreeding depression for adult male fitness. These results provide substantial insight into mating patterns of a wild guppy population: strong inbreeding depression occurs, and individuals tend to avoid mating with relatives.     

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates' extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free-living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra-pair offspring and 9% of 212 offspring were sired by extra-pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors.     

Evolution of Adaptation and Mate Choice: Parental Relatedness Affects Expression of Phenotypic Variance in a Natural Population

Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism’s sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure.     

HERITABILITIES OF DOMINANCE-RELATED TRAITS IN MALE BANK VOLES (CLETHRIONOMYS GLAREOLUS)

A number of studies have shown that in several animal species females prefer dominant males as mating partners, but fewer attempts have been made to measure possible indirect benefits of this choice. One reason for this may be that, even though dominance is a widely used concept, the definition of dominance still remains controversial Furthermore, defining and measuring the heritability of social behaviors is problematic because they are not individual traits but, by definition, involve interactions between at least two individuals. In this study we estimated heritabilities and coefficients of additive genetic variances (CV_A) for male traits that are closely associated with dominance and female mating preferences in bank voles (Clethrionomys glareolus). The heritability values were estimated using father-offspring regression. All heritability estimates were relatively high ranging from 0.531 (urine marking) to 0.767 (preputial glands). The CV_A-values indicated high levels of additive genetic variance especially in the characters most closely related to dominance: the weight of preputial glands and urine marking behavior. All phenotypic correlations among the traits measured were significantly positive and the genetic correlations were of similar magnitude as the corresponding phenotypic counterparts. Even though heritabilities may be lower in the natural environment than under controlled laboratory conditions, our results suggest that characters closely related to dominance may be at least partly genetically determined.     

Why does inbreeding reduce male paternity? Effects on sexually selected traits

Mating with relatives has often been shown to negatively affect offspring fitness (inbreeding depression). There is considerable evidence for inbreeding depression due to effects on naturally selected traits, particularly those expressed early in life, but there is less evidence of it for sexually selected traits. This is surprising because sexually selected traits are expected to exhibit strong inbreeding depression. Here, we experimentally created inbred and outbred male mosquitofish (Gambusia holbrooki). Inbred males were the offspring of matings between full siblings. We then investigated how inbreeding influenced a number of sexually selected male traits, specifically: attractiveness, sperm number and velocity, as well as sperm competitiveness based on a male's share of paternity. We found no inbreeding depression for male attractiveness or sperm traits. There was, however, evidence that lower heterozygosity decreased paternity due to reduced sperm competitiveness. Our results add to the growing evidence that competitive interactions exacerbate the negative effects of the increased homozygosity that arises when there is inbreeding.     

Quantifying inbreeding avoidance through extra-pair reproduction

Extra-pair reproduction is widely hypothesized to allow females to avoid inbreeding with related socially paired males. Consequently, numerous field studies have tested the key predictions that extra-pair offspring are less inbred than females’ alternative within-pair offspring, and that the probability of extra-pair reproduction increases with a female's relatedness to her socially paired male. However, such studies rarely measure inbreeding or relatedness sufficiently precisely to detect subtle effects, or consider biases stemming from failure to observe inbred offspring that die during early development. Analyses of multigenerational song sparrow (Melospiza melodia) pedigree data showed that most females had opportunity to increase or decrease the coefficient of inbreeding of their offspring through extra-pair reproduction with neighboring males. In practice, observed extra-pair offspring had lower inbreeding coefficients than females’ within-pair offspring on average, while the probability of extra-pair reproduction increased substantially with the coefficient of kinship between a female and her socially paired male. However, simulations showed that such effects could simply reflect bias stemming from inbreeding depression in early offspring survival. The null hypothesis that extra-pair reproduction is random with respect to kinship therefore cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra-pair reproduction requires reevaluation given such biases.     

Multilocus heterozygosity, parental relatedness and individual fitness components in a wild mountain goat, Oreamnos americanus population

Matings between relatives lead to a decrease in offspring genetic diversity which can reduce fitness, a phenomenon known as inbreeding depression. Because alpine ungulates generally live in small structured populations and often exhibit a polygynous mating system, they are susceptible to inbreeding. Here, we used marker-based measures of pairwise genetic relatedness and inbreeding to investigate the fitness consequences of matings between relatives in a long-term study population of mountain goats ( Oreamnos americanus ) at Caw Ridge, Alberta, Canada. We first assessed whether individuals avoided mating with kin by comparing actual and random mating pairs according to their estimated genetic relatedness, which was derived from 25 unlinked polymorphic microsatellite markers and reflected pedigree relatedness. We then examined whether individual multilocus heterozygosity H , used as a measure of inbreeding, was predicted by parental relatedness and associated with yearling survival and the annual probability of giving birth to a kid in adult females. Breeding pairs identified by genetic parentage analyses of offspring that survived to 1 year of age were less genetically related than expected under random matings. Parental relatedness was negatively correlated with offspring H , and more heterozygous yearlings had higher survival to 2 years of age. The probability of giving birth was not affected by H in adult females. Because kids that survived to yearling age were mainly produced by less genetically related parents, our results suggest that some individuals experienced inbreeding depression in early life. Future research will be required to quantify the levels of gene flow between different herds, and evaluate their effects on population genetic diversity and dynamics.     

Age-dependent genetic effects on a secondary sexual trait in male Alpine ibex, Capra ibex

Secondary sexual traits, such as horns in ungulates, may be good indicators of genetic quality because they are costly to develop. Genetic effects on such traits may be revealed by examining correlations between multilocus heterozygosity (MLH) and trait value. Correlations between MLH and fitness traits, termed heterozygosity-fitness correlations (HFC), may reflect inbreeding depression or associative overdominance of neutral microsatellite loci with loci directly affecting fitness traits. We investigated HFCs for horn growth, body mass and faecal counts of nematode eggs in wild Alpine ibex (Capra ibex). We also tested if individual inbreeding coefficients (f') estimated from microsatellite data were more strongly correlated with fitness traits than MLH. MLH was more strongly associated with trait variation than f'. We found HFC for horn growth but not for body mass or faecal counts of nematode eggs. The effect of MLH on horn growth was age-specific. The slope of the correlation between MLH and yearly horn growth changed from negative to positive as males aged, in accordance with the mutation accumulation theory of the evolution of senescence. Our results suggest that the horns of ibex males are an honest signal of genetic quality.     

Female choice and the relatedness of mates in the guppy (<Emphasis Type="Italic">Poecilia reticulata</Emphasis>)

Several studies suggest that females may offset the costs of genetic incompatibility by exercising pre-copulatory or post-copulatory mate choice to bias paternity toward more compatible males. One source of genetic incompatibility is the degree of relatedness among mates; unrelated males are expected to be genetically more compatible with a female than her relatives. To address this idea, we investigated the potential for inbreeding depression and paternity biasing mechanisms (pre- and post-copulatory) of inbreeding avoidance in the guppy, Poecilia reticulata. Inbreeding resulted in a reduction in offspring number and quality. Females mated to siblings gave birth to significantly fewer offspring compared to females mated to non-siblings and inbred male offspring took longer to reach sexual maturity. There was no evidence of inbreeding avoidance in pre-copulatory behaviors of females or males. Sexual responsiveness of females to courting males and the number of sexual behaviors males directed at females did not decrease as a function of the relatedness of the two individuals. We also tested whether female guppies can use post-copulatory mechanisms to bias sperm usage toward unrelated males by comparing the number of offspring produced by females mated to two of their siblings (SS), two males unrelated to the female (NN), or to one unrelated male and a sibling male (NS). We found that NS females produced a number of offspring not significantly different than what would be expected if fertilization success were halfway between completely outbreeding (NN) and completely inbreeding (SS) females. This suggests that there is no significant improvement in the number of offspring produced by females mating to both related and unrelated males, relative to that which would be expected if sperm from both males were used equally. Our results suggest that female guppies do not discriminate against closely related males or their sperm.     

The Association of Genotype-Based Inbreeding Coefficient with a Range of Physical and Psychological Human Traits

Across animal species, offspring of closely related mates exhibit lower fitness, a phenomenon called inbreeding depression. Inbreeding depression in humans is less well understood because mating between close relatives is generally rare and stigmatised, confounding investigation of its effect on fitness-relevant traits. Recently, the availability of high-density genotype data has enabled quantification of variation in distant inbreeding in ‘outbred’ human populations, but the low variance of inbreeding detected from genetic data in most outbred populations means large samples are required to test effects, and only a few traits have yet been studied. However, it is likely that isolated populations, or those with a small effective population size, have higher variation in inbreeding and therefore require smaller sample sizes to detect inbreeding effects. With a small effective population size and low immigration, Northern Finland is such a population. We make use of a sample of ∼5,500 ‘unrelated’ individuals in the Northern Finnish Birth Cohort 1966 with known genotypes and measured phenotypes across a range of fitness-relevant physical and psychological traits, including birth length and adult height, body mass index (BMI), waist-to-hip ratio, blood pressure, heart rate, grip strength, educational attainment, income, marital status, handedness, health, and schizotypal features. We find significant associations in the predicted direction between individuals'' inbreeding coefficient (measured by proportion of the genome in runs of homozygosity) and eight of the 18 traits investigated, significantly more than the one or two expected by chance. These results are consistent with inbreeding depression effects on a range of human traits, but further research is needed to replicate and test alternative explanations for these effects.     

Outbreeding depression, but no inbreeding depression in haplodiploid Ambrosia beetles with regular sibling mating

In sexual reproduction the genetic similarity or dissimilarity between mates strongly affects offspring fitness. When mating partners are too closely related, increased homozygosity generally causes inbreeding depression, whereas crossing between too distantly related individuals may disrupt local adaptations or coadaptations within the genome and result in outbreeding depression. The optimal degree of inbreeding or outbreeding depends on population structure. A long history of inbreeding is expected to reduce inbreeding depression due to purging of deleterious alleles, and to promote outbreeding depression because of increased genetic variation between lineages. Ambrosia beetles (Xyleborini) are bark beetles with haplodiploid sex determination, strong local mate competition due to regular sibling mating within the natal chamber, and heavily biased sex ratios. We experimentally mated females of Xylosandrus germanus to brothers and unrelated males and measured offspring fitness. Inbred matings did not produce offspring with reduced fitness in any of the examined life-history traits. In contrast, outcrossed offspring suffered from reduced hatching rates. Reduction in inbreeding depression is usually attributed to purging of deleterious alleles, and the absence of inbreeding depression in X. germanus may represent the highest degree of purging of all examined species so far. Outbreeding depression within the same population has previously only been reported from plants. The causes and consequences of our findings are discussed with respect to mating strategies, sex ratios, and speciation in this unusual system.