Lack of inbreeding avoidance in the Argentine ant Linepithema humile

Although workers might increase their inclusive fitness by favoringcloser over more distant kin, evidence suggest that nepotismgenerally does not occur within colonies of social insects.It has been suggested that this may be due to the cost of recognitionerrors. We tested whether recognition occurs in a system wherea better than random ability to recognize kin should be selected for. Using DNA microsatellites, we show that sexuals of theArgentine ant Linepithema humile fail to use genetic cues toavoid sib-mating. When offspring of two queens were allowedto mate, the percentage of matings among siblings was not significantlylower than expected under the hypothesis of random mating.The finding that sexuals fail to use genetic cues to avoid sib-matings cannot be attributed to the cost of recognitionerrors because any recognition system that would lead to abetter than random ability to avoid sib-mating should be selectedfor when there are costs to inbreeding. These data are thusconsistent with the view that kin recognition mediated solelyby genetic cues might be intrinsically error prone within coloniesof social insects.     

Queen mating and paternity variation in the ant Lasius niger

We have electrophoretically analysed the variation in queen mating and worker paternity across and within seven populations of the ant Lasius niger in northwestern Europe. Populations were panmictic and not genetically differentiated ( F _ST = 0.003 ± 0.004; range c. 1000 km). Queens ( n = 535) were shown to mostly mate with a single male, but double mating occurred in all populations and triple mating was found in one case (the total number of worker offspring analysed for paternity was 4825). The genetically effective queen mating frequency was 1.16 on average across populations (range 1.04–1.42). Double sampling of six out of the seven populations showed that most of the variation in queen mating occurred among populations and not within populations among years. Also, paternity skew in colonies with double-mated queens was relatively constant per site but varied across populations. Paternity skew was high in populations with low frequencies of double queen-mating, low in populations with intermediate frequencies of double queen mating and ambiguous in a single population where more than half of the queens mated multiply. Double-mated queens were only collected halfway through a nuptial flight, suggesting that double mating is time consuming and that the mating swarm sex ratio may affect the likelihood of multiple mating towards the end of a flight. No difference in fresh weight between single- and double-mated queens from the same population was found.     

No inbreeding depression but increased sexual investment in highly inbred ant colonies

Inbreeding can lead to the expression of deleterious recessive alleles and to a subsequent fitness reduction. In Hymenoptera, deleterious alleles are purged in haploid males moderating inbreeding costs. However, in these haplodiploid species, inbreeding can result in the production of sterile diploid males. We investigated the effects of inbreeding on the individual and colony level in field colonies of the highly inbred ant Hypoponera opacior. In this species, outbreeding winged sexuals and nest‐mating wingless sexuals mate during two separate reproductive periods. We show that regular sib‐matings lead to high levels of homozygosity and the occasional production of diploid males, which sporadically sire triploid offspring. On the individual level, inbreeding was associated with an increased body size in workers. On the colony level, we found no evidence for inbreeding depression as productivity was unaffected by the level of homozygosity. Instead, inbred colonies altered their allocation strategies by investing more resources into sexuals than into workers. This shift towards sexual production was due to an increased investment in both males and queens, which was particularly pronounced in the dispersive generation. The absence of inbreeding depression combined with increased reproductive investment, especially in outbreeding sexuals, suggests that these ants have evolved active strategies to regulate the extent and effects of frequent inbreeding.     

An analysis of mating biases in trees

Assortative mating is a deviation from random mating based on phenotypic similarity. As it is much better studied in animals than in plants, we investigate for trees whether kinship of realized mating pairs deviates from what is expected from the set of potential mates and use this information to infer mating biases that may result from kin recognition and/or assortative mating. Our analysis covers 20 species of trees for which microsatellite data is available for adult populations (potential mates) as well as seed arrays. We test whether mean relatedness of observed mating pairs deviates from null expectations that only take pollen dispersal distances into account (estimated from the same data set). This allows the identification of elevated as well as reduced kinship among realized mating pairs, indicative of positive and negative assortative mating, respectively. The test is also able to distinguish elevated biparental inbreeding that occurs solely as a result of related pairs growing closer to each other from further assortativeness. Assortative mating in trees appears potentially common but not ubiquitous: nine data sets show mating bias with elevated inbreeding, nine do not deviate significantly from the null expectation, and two show mating bias with reduced inbreeding. While our data sets lack direct information on phenology, our investigation of the phenological literature for each species identifies flowering phenology as a potential driver of positive assortative mating (leading to elevated inbreeding) in trees. Since active kin recognition provides an alternative hypothesis for these patterns, we encourage further investigations on the processes and traits that influence mating patterns in trees.     

Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population

Inbreeding is common in small and threatened populations and often has a negative effect on individual fitness and genetic diversity. Thus, inbreeding can be an important factor affecting the persistence of small populations. In this study, we investigated the effects of inbreeding on fitness in a small, wild population of house sparrows (Passer domesticus) on the island of Aldra, Norway. The population was founded in 1998 by four individuals (one female and three males). After the founder event, the adult population rapidly increased to about 30 individuals in 2001. At the same time, the mean inbreeding coefficient among adults increased from 0 to 0.04 by 2001 and thereafter fluctuated between 0.06 and 0.10, indicating a highly inbred population. We found a negative effect of inbreeding on lifetime reproductive success, which seemed to be mainly due to an effect of inbreeding on annual reproductive success. This resulted in selection against inbred females. However, the negative effect of inbreeding was less strong in males, suggesting that selection against inbred individuals is at least partly sex specific. To examine whether individuals avoided breeding with close relatives, we compared observed inbreeding and kinship coefficients in the population with those obtained from simulations of random mating. We found no significant differences between the two, indicating weak or absent inbreeding avoidance. We conclude that there was inbreeding depression in our population. Despite this, birds did not seem to actively avoid mating with close relatives, perhaps as a consequence of constraints on mating possibilities in such a small population.     

Family level inbreeding depression and the evolution of plant mating systems

Variation in the magnitude of inbreeding depression (ID) among families may have important consequences for mating system evolution. Experimental studies have shown that such variation is a common feature of natural plant populations. Unfortunately, the genetic and evolutionary significance of family level estimates remains obscure. Almost any kind of genetic variation will generate differences in ID among families, and as a consequence, a non-zero variance in family level ID is not sufficient to distinguish genetic architectures with wholly different implications for mating system evolution. Quantitative genetic methods provide a means to extract more information from ID experiments. Estimates of quantitative genetic variance components directly inform questions about the genetic basis of ID and should ultimately allow tests of alternative theories of mating system evolution.     

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.     

Interpopulation variation in mating system and late-stage inbreeding depression in Magnolia stellata

Inbreeding has the potential to cause evolutionary changes in populations, although these changes are likely to drive populations to extinction through inbreeding depression and reductions in genetic diversity. We investigated the mating system and late-stage inbreeding depression (δ) in 10 populations of Magnolia stellata using nine microsatellite markers and evaluated the effects of population size and the degree of population isolation through inbreeding and inbreeding depression on the persistence of populations. The outcrossing rates were very similar (~0.7) among populations, but the correlations of paternity, fractions of biparental inbreeding and inbreeding coefficients at the seed stage ( F _S) varied among populations, suggesting that the level of outcrossing was similar among populations, while the quality of it was not. A significant negative correlation was detected between F _S and population size. The average value of δ was 0.709, and the values in six of the 10 populations were significant. The values of δ differed among populations, although clear relationships with population size and the degree of population isolation were not detected. However, in one population, which was very small and located in the edge of the species' range, we obtained a very low value of δ (–0.096), which may be indicative of purging or the fixation of deleterious alleles. Existing M. stellata populations that are small (and thus might be expected to have higher frequencies of inbreeding) and have large values of δ may be in danger of declining, even if the populations are located within the central region of the species' range.     

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.     

Little to no inbreeding depression in a tapeworm with mixed mating

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

Odor diversity decreases with inbreeding in the ant Hypoponera opacior

Reduction in heterozygosity can lead to inbreeding depression. This loss of genetic variability especially affects diverse loci, such as immune genes or those encoding recognition cues. In social insects, nestmates are recognized by their odor, that is their cuticular hydrocarbon profile. Genes underlying hydrocarbon production are thought to be under balancing selection. If so, inbreeding should result in a loss of chemical diversity. We show here that cuticular hydrocarbon diversity decreases with inbreeding. Studying an ant with a facultative inbreeding lifestyle, we found inbred workers to exhibit both a lower number of hydrocarbons and less diverse, that is less evenly proportioned profiles. The association with inbreeding was strong for methyl‐branched alkanes, which play a major role in nestmate recognition, and for n‐alkanes, whereas unsaturated compounds were unaffected. Shifts in allocation strategies with inbreeding in our focal species indicate that these ants can detect their inbreeding level and use this information to adjust their reproductive strategy. Our study is the first to demonstrate that odor profiles can encode information on inbreeding, with broad implications not only for social insects, but for sexual selection and mate choice in general. Odor profiles may constitute an honest signal of inbreeding, a fitness‐relevant trait in many species.     

Interpopulation variation in inbreeding is primarily driven by tolerance of mating with relatives in a spermcasting invertebrate

The degree to which individuals inbreed is a fundamental aspect of population biology shaped by both passive and active processes. Yet, the relative influences of random and non-random mating on the overall magnitude of inbreeding are not well characterized for many taxa. We quantified variation in inbreeding among qualitatively accessible and isolated populations of a sessile marine invertebrate (the colonial ascidian Lissoclinum verrilli) in which hermaphroditic colonies cast sperm into the water column for subsequent uptake and internal fertilization. We compared estimates of inbreeding to simulations predicting random mating within sites to evaluate if levels of inbreeding were (1) less than expected because of active attempts to limit inbreeding, (2) as predicted by genetic subdivision and passive inbreeding tolerance, or (3) greater than simulations due to active attempts to promote inbreeding via self-fertilization or a preference for related mates. We found evidence of restricted gene flow and significant differences in the genetic diversity of L. verrilli colonies among sites, indicating that on average colonies were weakly related in accessible locations, but their levels of relatedness matched that of first cousins or half-siblings on isolated substrates. Irrespective of population size, progeny arrays revealed variation in the magnitude of inbreeding across sites that tracked with the mean relatedness of conspecifics. Biparental reproduction was confirmed in most offspring (86%) and estimates of total inbreeding largely overlapped with simulations of random mating, suggesting that interpopulation variation in mother–offspring resemblance was primarily due to genetic subdivision and passive tolerance of related mates. Our results highlight the influence of demographic isolation on the genetic composition of populations, and support theory predicting that tolerance of biparental inbreeding, even when mates are closely related, may be favoured under a broad set of ecological and evolutionary conditions.     

Three queen morphs with alternative nest-founding behaviors in the ant, Temnothorax longispinosus

In many ant species, multiple modes of founding new colonies occur in the same population. These modes include dependent founding, independent founding by haplometrosis (single queen), and independent founding by pleometrosis (multiple queens). In several cases, a dimorphism in queen size has been found, such that each morph specializes in a particular nest-founding behavior. I investigated queen size in the ant Temnothorax longispinosus in several southern Wisconsin populations and found three distinct queen morphs: small queens with very low fat content and short wings, large queens with low fat and long wings, and large queens with high fat and very long wings. Several traits associated with founding behavior correlated with these queen sizes. Small queens were produced in lower numbers, were more common in polygynous nests, and returned to the nest in higher proportions than both large queen morphs. The size ranges and fat levels of each queen morph were similar to those of other species that specialize in either haplometrosis (very large, high fat), pleometrosis (large, low fat), or dependent founding (small and low fat). However, there was extensive overlap in several of the founding behaviors, suggesting that the morphs in these populations have some flexibility in founding behavior. The queen morphs in these populations of T. longispinosus may resemble early stages in the evolution of more specialized dispersal polymorphisms found in other ant species. Received 11 January 2006; revised 15 September 2006; accepted 18 September 2006.     

Mating strategies with genomic information reduce rates of inbreeding in animal breeding schemes without compromising genetic gain

We tested the hypothesis that mating strategies with genomic information realise lower rates of inbreeding (∆F) than with pedigree information without compromising rates of genetic gain (∆G). We used stochastic simulation to compare ∆F and ∆G realised by two mating strategies with pedigree and genomic information in five breeding schemes. The two mating strategies were minimum-coancestry mating (MC) and minimising the covariance between ancestral genetic contributions (MCAC). We also simulated random mating (RAND) as a reference point. Generations were discrete. Animals were truncation-selected for a single trait that was controlled by 2000 quantitative trait loci, and the trait was observed for all selection candidates before selection. The criterion for selection was genomic-breeding values predicted by a ridge-regression model. Our results showed that MC and MCAC with genomic information realised 6% to 22% less ∆F than MC and MCAC with pedigree information without compromising ∆G across breeding schemes. MC and MCAC realised similar ∆F and ∆G. In turn, MC and MCAC with genomic information realised 28% to 44% less ∆F and up to 14% higher ∆G than RAND. These results indicated that MC and MCAC with genomic information are more effective than with pedigree information in controlling rates of inbreeding. This implies that genomic information should be applied to more than just prediction of breeding values in breeding schemes with truncation selection.     

Variation in self-fertility,inbreeding depression and levels of inbreeding in four Cyclamen species

The ability to self in the absence of pollinators, i.e. reproductive assurance, and the detrimental consequences of inbreeding, i.e. inbreeding depression, are central factors influencing plant mating system evolution. The purpose of this study was to quantify whether self-fertility and inbreeding depression are related to levels of inbreeding in four Cyclamen species, namely C. balearicum (mean F_is = 0.930), C. creticum (mean F_is = 0.748), C. repandum (mean F_is = 0.658) and C. hederifolium (mean F_is = 0.329). C. balearicum showed a markedly greater capacity to autonomously self-fertilize than the three other species, which may have favoured inbreeding in this species. Levels of inbreeding depression were highest in C. creticum and C. hederifolium at the fruit maturation (δ = 0.18 and 0.20, respectively) and seed number (δ = 0.32 and 0.30, respectively) stages, and for C. repandum at the seed weight stage (δ = 0.23). Although C. balearicum showed inbreeding depression on seed germination (δ = 0.45), this may be an artefact of the generally low levels of seed germination in the experiment. Overall, we observed only limited evidence for the predicted negative relation between inbreeding coefficients and levels of inbreeding since C. creticum had high levels of inbreeding and inbreeding depression. Other factors may thus influence the relationship between inbreeding and inbreeding depression in these species.     

Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula

Reproductive skew - the extent to which reproduction is unevenly shared between individuals in a social group - varies greatly between and within animal species. In this study, we investigated how queens share parentage in polygynous (multiple queen) colonies of the Mediterranean ant Pheidole pallidula. We used highly polymorphic microsatellites markers to determine parentage of gynes (new queens), males and workers in P. pallidula field colonies. The comparison of the genotypes of young and adult workers revealed a very low queen turnover (less than 2%). The first main finding of the study of reproductive skew in these colonies was that there was a significant departure from equal contribution of queens to gyne, male and worker production. Reproductive skew was greater for male production than for queen and worker production. There was no relationship between the magnitude of the reproductive skew and the number of reproductive queens per colony, their relatedness and the overall colony productivity, some of the factors predicted to influence the extent of reproductive skew. Finally, our study revealed for the first time a trade-off in the relative contribution of nestmate queens to gyne and worker production. The queens contributing more to gyne production contributed significantly less to worker production.     

Reduction of inbreeding in commercial females by rotational mating with several sire lines

A mating system to reduce the inbreeding of commercial females in the lower level was examined theoretically, assuming a hierarchical breed structure, in which favorable genes are accumulated in the upper level by artificial selection and the achieved genetic progress is transferred to the lower level through migration of males. The mating system examined was rotational mating with several closed sire lines in the upper level. Using the group coancestry theory, we derived recurrence equations for the inbreeding coefficient of the commercial females. The asymptotic inbreeding coefficient was also derived. Numerical computations showed that the critical factor for determining the inbreeding is the number of sire lines, and that the size of each sire line has a marginal effect. If four or five sire lines were available, rotational mating was found to be quite an effective system to reduce the short- and long-term inbreeding of the commercial females, irrespective of the effective size of each sire line. Oscillation of the inbreeding coefficient under rotational mating with initially related sire lines could be minimized by avoiding the consecutive use of highly related lines. Extensions and perspectives of the system are discussed in relation to practical application.     

Evolution of precopulatory and post‐copulatory strategies of inbreeding avoidance and associated polyandry

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

Reproductive specialization in multiple-queen colonies of the ant Formica exsecta

In polygynous (multiple queens per nest) colonies of socialinsects, queens can increase their reproductive share by layingmore eggs or by increasing the proportion of eggs that developinto reproductive individuals instead of workers. We used polymorphicmicrosatellite loci to determine the genetically effective contributionof queens to the production of gynes (new queens), males, and2 different cohorts of workers in a polygynous population ofthe ant Formica exsecta. For this purpose, we developed a newmethod that can be used for diploid and haplodiploid organismsto quantify the degree of reproductive specialization amongbreeders in societies where there are too many breeders to ascertainparentage. Using this method, we found a high degree of reproductivespecialization among nest-mate queens in both female- and male-producingcolonies (sex ratio is bimodally distributed in the study population).For example, a high effective proportion of queens (25% and79%, respectively) were specialized in the production of malesin female- and male-producing colonies. Our analyses furtherrevealed that in female-producing colonies, significantly fewerqueens contributed to gyne production than to worker production.Finally, we found significant changes in the identity of queenscontributing to different cohorts of workers. Altogether, thesedata demonstrate that colonies of F. exsecta, and probably thoseof many other highly polygynous social insect species, are composedof reproductive individuals differing in their investment togynes, males, and workers. These findings demonstrate a newaspect of the highly dynamic social organization of complexanimal societies.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.