Fitness‐consequences of geitonogamous selfing in a clonal marine angiosperm (Zostera marina)

Plant mating systems have received considerable attention because the proportion of selfed vs. outcrossed progeny is an important evolutionary factor. In clonally reproducing plants, geitonogamous selfing between distant ramets belonging to the same genet is expected to be widespread, yet empirical data are sparse. Nothing is known about between‐ramet selfing in aquatic flowering plants with subaqueous pollen transfer, most of which display pronounced clonal reproduction. From two locations in the western Baltic Sea, I present data on the effects of patch isolation and clonal diversity on the outcrossing rate of eelgrass, Zostera marina L., based on the genotypes of maternal plants and recently fertilized ovules scored at eight microsatellite loci. There were no differences in outcrossing rates between vegetation patches and continuous meadow although patches were nearly always composed of single genets. Quantitative effects of clonal diversity were present in the continuous vegetation where a significant positive correlation between genet diversity and the proportion of outcrossed offspring was detected (Kendall’s τ=0.82, P=0.0017). On a population‐scale as well, the genotypic diversity was positively correlated with outcrossing. The relative fitness of selfed offspring was low (ω ± 95% confidence interval=0.56 ± 0.032 and 0.322 ± 0.15) indicating that geitonogamy incurred substantial fitness costs. Selfing rates in Z. marina may not be in evolutionary equilibrium because of spatial and temporal heterogeneity of clonal size and diversity. The high prevalence of dioecy in seagrasses may have evolved to avoid the fitness costs associated with geitonogamy.     

Inbreeding depression influences genet size distribution in a marine angiosperm

Although inbreeding depression is a major genetic phenomena influencing individual fitness, it is difficult to measure in wild populations. An alternative approach is to correlate heterozygosity, measured using highly polymorphic markers, with a fitness-correlated trait. In clonal plants, genet size is predicted to be fitness correlated. Here we test the prediction that the genet size distribution of the marine clonal plant Zostera marina (eelgrass) is influenced by inbreeding depression. We used nine polymorphic microsatellite markers to access the fine scale clonal structure and to measure individual heterozygosity within 4 plots (each corresponds to 256 m2, sampled at 1-m intervals) in two populations along the German Baltic Coast. The same plots were also sampled for flowering and vegetative shoots to obtain estimates for sexual reproductive output at the level of the genetic individual. We found substantial differences in the genet size distribution between the two populations that may be explained by different disturbance frequency. In both populations, clone size was significantly positively correlated with the total number of flowering shoots, indicating that larger clones have a higher reproductive output. Individual heterozygosity was significantly positively associated with clone size. The effect was much stronger in Falkenstein (low disturbance) than in Maasholm (high disturbance). The results indicate that in a low disturbance population the relatively outbred clones occupy a higher proportion of the available space, possibly because they outcompete relatively inbred neighbours.     

A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant

We examined the genetic population structure in eelgrass (Zostera marina L.), the dominant seagrass species of the northern hemisphere, over spatial scales from 12 km to 10 000 km using the polymorphism of DNA microsatellites. Twelve populations were genotyped for six loci representing a total of 67 alleles. Populations sampled included the North Sea (four), the Baltic Sea (three), the western Atlantic (two), the eastern Atlantic (one), the Mediterranean Sea (one) and the eastern Pacific (one). Microsatellites revealed substantial genetic variation in a plant group with low allozyme diversity. Average expected heterozygosities per population (monoclonal populations excluded) ranged from 0.32 to 0.61 (mean = 0. 48) and allele numbers varied between 3.3 and 6.7 (mean = 4.7). Using the expected frequency of multilocus genotypes within populations, we distinguished ramets from genetic individuals (i.e. equivalent to clones). Differences in clonal diversity among populations varied widely and ranged from maximal diversity (i.e. all ramets with different genotype) to near or total monoclonality (two populations). All multiple sampled ramets were excluded from further analysis of genetic differentiation within and between populations. All but one population were in Hardy-Weinberg equilibrium, indicating that Zostera marina is predominantly outcrossing. From a regression of the pairwise population differentiation with distance, we obtained an effective population size Ne of 2440-5000. The overall genetic differentiation among eelgrass populations, assessed as rho (a standardized estimate of Slatkin's RST) was 0.384 (95% CI 0.34-0.44, P < 0.001). Genetic differentiation was weak among three North Sea populations situated 12-42 km distant from one another, suggesting that tidal currents result in an efficient exchange of propagules. In the Baltic and in Nova Scotia, a small but statistically significant fraction of the genetic variance was distributed between populations (rho = 0.029-0. 053) at scales of 15-35 km. Pairwise genetic differentiation between European populations were correlated with distance between populations up to a distance of 4500 km (linear differentiation-by-distance model, R2 = 0.67). In contrast, both Nova Scotian populations were genetically much closer to North Sea and Baltic populations than expected from their geographical distance (pairwise rho = 0.03-0.08, P < 0.01). A biogeographical cluster of Canadian with Baltic/North Sea populations was also supported using a neighbour-joining tree based on Cavalli-Sforza's chord distance. Relatedness between populations may be very different from predictions based on geographical vicinity.     

Development of microsatellite markers in a clonal perennial herb,Convallaria keiskei

We developed eight polymorphic microsatellite simple sequence repeat (SSR) loci from genomic DNA of a clonal perennial herb, Convallaria keiskei, using a dual‐suppression‐polymerase chain reaction (PCR) technique and an improved technique. These markers with four to 10 alleles per locus identified 29 genotypes in 82 samples collected from a population in Hokkaido, Japan. The observed and expected heterozygosities ranged from 0.241 to 0.862 and from 0.639 to 0.825, respectively. These SSR markers will be available to identify genets and evaluate genetic diversity of C. keiskei.     

Role of parasite transmission in promoting inbreeding: II. Pedigree reconstruction reveals sib‐transmission and consequent kin‐mating

Even though parasitic flatworms are one of the most species‐rich groups of hermaphroditic organisms, we know virtually nothing of their mating systems (selfing or kin‐mating rates) in nature. Hence, we lack an understanding of the role of inbreeding in parasite evolution. The natural mating systems of parasitic flatworms have remained elusive due to the inherent difficulty in generating progeny‐array data in many parasite systems. New developments in pedigree reconstruction allow direct inference of realized selfing rates in nature by simply using a sample of genotyped individuals. We built upon this advancement by utilizing the closed mating systems, that is, individual hosts, of endoparasites. In particular, we created a novel means to use pedigree reconstruction data to estimate potential kin‐mating rates. With data from natural populations of a tapeworm, we demonstrated how our newly developed methods can be used to test for cosibling transmission and inbreeding depression. We then showed how independent estimates of the two mating system components, selfing and kin‐mating rates, account for the observed levels of inbreeding in the populations. Thus, our results suggest that these natural parasite populations are in inbreeding equilibrium. Pedigree reconstruction analyses along with the new companion methods we developed will be broadly applicable across a myriad of parasite species. As such, we foresee that a new frontier will emerge wherein the diverse life histories of flatworm parasites could be utilized in comparative evolutionary studies to broadly address ecological factors or life history traits that drive mating systems and hence inbreeding in natural populations.     

Breaking linkage between mating compatibility factors: Tetrapolarity in Microbotryum

Linkage of genes determining separate self‐incompatibility mechanisms is a general expectation of sexual eukaryotes that helps to resolve conflicts between reproductive assurance and recombination. However, in some organisms, multiple loci are required to be heterozygous in offspring while segregating independently in meiosis. This condition, termed “tetrapolarity” in basidiomycete fungi, originated in the ancestor to that phylum, and there have been multiple reports of subsequent transitions to “bipolarity” (i.e., linkage of separate mating factors). In the genus Microbotryum, we present the first report of the breaking of linkage between two haploid self‐incompatibility factors and derivation of a tetrapolar breeding system. This breaking of linkage is associated with major alteration of genome structure, with the compatibility factors residing on separate mating‐type chromosome pairs, reduced in size but retaining the structural dimorphism characteristic for regions of recombination suppression. The challenge to reproductive assurance from unlinked compatibility factors may be overcome by the automictic mating system in Microbotryum (i.e., mating among products of the same meiosis). As a curious outcome, this linkage transition and its effects upon outcrossing compatibility rates may reinforce automixis as a mating system. These observations contribute to understanding mating systems and linkage as fundamental principles of sexual life cycles, with potential impacts on conventional wisdom regarding mating‐type evolution.     

Effect of recurrent selfing on inbreeding depression and mating system evolution in an autopolyploid plant

Genome duplication resulting in polyploidy can have significant consequences for the evolution of mating systems. Most theory predicts that self‐fertilization will be selectively favored in polyploids; however, many autopolyploids are outcrossing or mixed‐mating. Here, we examine the hypothesis that the evolution of selfing is restricted in autopolyploids because the genetic cost of selfing (i.e., inbreeding depression) increases monotonically with successive generations of inbreeding. Using the herbaceous, autotetraploid plant Chamerion angustifolium, we generated populations with different inbreeding coefficients (F= 0, 0.17 and 0.36) through three consecutive generations of selfing and compared their magnitudes of inbreeding depression in a common environment. Mating system estimates for four natural populations confirmed that tetraploid selfing rates (s_m= 0.25, SE = 0.02) are similar to those of diploids (s_m= 0.12, SE = 0.12; F_1,2= 1.34, P= 0.37) indicating that both cytotypes are predominantly outcrossing. Compared to an outbred control line, mean inbreeding depression for seed production, survival, and height (vegetative and total) in the inbred line differed among generations (inbreeding coefficients). Across all stages, inbreeding depression (relative to control) was positively related to generation (inbreeding coefficient). Although the initial costs of inbreeding in extant and newly synthesized polyploids may be low compared to diploids, the monotonic increase in inbreeding depression with repeated inbreeding may limit the extent to which selfing variants are favored.     

Evolutionary dynamics of mating system shifts in Arabidopsis lyrata

Outcrossing is the prevalent mode of reproduction in plants and animals despite its substantial costs, while selfing and mixed mating occur at much lower frequency. Comparative research on plants has demonstrated the lability of self‐incompatibility, but there is little information about the transition on a within‐species level from self‐incompatibility to predominant selfing. We studied variation in mating system among 18 populations of Arabidopsis lyrata within a phylogenetic context to shed light on the evolution of selfing. Realized and potential mating systems were assessed by genetic analysis with microsatellite markers and hand‐self‐pollinations on 30 plants from each population. The fraction of self‐incompatible plants in a population was highly correlated with the outcrossing rate, showing that the spread of self‐compatibility is accompanied by or soon followed by an increase in the rate of selfing. The four predominantly selfing populations (outcrossing rates < 0.25) fell into more than one phylogenetic cluster, suggesting that the transition to selfing occurred more than once independently. Hence, A. lyrata offers an opportunity for the comparative analysis of outcrossing as a predominant mode of reproduction in plants and of the causes of the shift to selfing.     

Experimental and genetic analyses reveal that inbreeding depression declines with increased self‐fertilization among populations of a coastal dune plant

Theory predicts that inbreeding depression (ID) should decline via purging in self‐fertilizing populations. Yet, intraspecific comparisons between selfing and outcrossing populations are few and provide only mixed support for this key evolutionary process. We estimated ID for large‐flowered (LF), predominantly outcrossing vs. small‐flowered (SF), predominantly selfing populations of the dune endemic Camissoniopsis cheiranthifolia by comparing selfed and crossed progeny in glasshouse environments differing in soil moisture, and by comparing allozyme‐based estimates of the proportion of seeds selfed and inbreeding coefficient of mature plants. Based on lifetime measures of dry mass and flower production, ID was stronger in nine LF populations [mean δ = 1?(fitness of selfed seed/fitness of outcrossed seed) = 0.39] than 16 SF populations (mean δ = 0.03). However, predispersal ID during seed maturation was not stronger for LF populations, and ID was not more pronounced under simulated drought, a pervasive stress in sand dune habitat. Genetic estimates of δ were also higher for four LF (δ = 1.23) than five SF (δ = 0.66) populations; however, broad confidence intervals around these estimates overlapped. These results are consistent with purging, but selective interference among loci may be required to maintain strong ID in partially selfing LF populations, and trade‐offs between selfed and outcrossed fitness are likely required to maintain outcrossing in SF populations.     

Evolution of mating types in finite populations: The precarious advantage of being rare

Sexually reproducing populations with self‐incompatibility bear the cost of limiting potential mates to individuals of a different type. Rare mating types escape this cost since they are unlikely to encounter incompatible partners, leading to the deterministic prediction of continuous invasion by new mutants and an ever‐increasing number of types. However, rare types are also at an increased risk of being lost by random drift. Calculating the number of mating types that a population can maintain requires consideration of both the deterministic advantages and the stochastic risks. By comparing the relative importance of selection and drift, we show that a population of size N can maintain a maximum of approximately N^1/3 mating types for intermediate population sizes, whereas for large N, we derive a formal estimate. Although the number of mating types in a population is quite stable, the rare‐type advantage promotes turnover of types. We derive explicit formulas for both the invasion and turnover probabilities in finite populations.     

Estimation of mating systems in Short and Tall ecomorphs of the coral Favia fragum

We used 15 microsatellite markers to estimate the selfing rate (s), outcrossing rate (t_O) and hybridization between partially sympatric ecomorphs (t_H) of the coral Favia fragum. Genotyping of progeny arrays revealed complete self‐fertilization in the Tall ecomorph and low outcrossing (t_O + t_H < 1%) in the Short ecomorph. Further, all larvae could be assigned with high probability to the same population as their parental dam, indicating no hybridization between ecomorphs (t_H = 0). Despite low ecological estimates of outcrossing, Q values from highly structured adult populations indicated that 9% of the adult samples were the products of outcrossing, and an additional 11% were hybrids. Reproductive isolation appears to have a strong geographical component, as we did not detect hybrids at a second site where the two ecomorphs were distributed in complete microallopatry. Adult estimates of gene flow within ecomorphs may be positively biased by ecomorph‐specific patterns of inbreeding depression, but cryptic gene flow between ecomorphs is most likely explained by undetected outcrossing and the fact that hybrid lineages persist after repeated generations of self‐fertilization. Our microsatellite data show that phenotypic differences between ecomorphs are maintained in sympatry despite evidence for hybridization.     

Experimental analysis of mating patterns in a clonal plant reveals contrasting modes of self‐pollination

Hermaphrodite plants commonly practice self‐fertilization (selfing), but the mechanisms responsible vary depending on the mode of self‐pollination, pollinator behavior, and degree of clonality. Whether selfing occurs within (autogamy) or between flowers (geitonogamy) is of evolutionary significance because their fitness consequences differ. We used floral manipulations and genetic markers to determine the relative contribution of autogamy and within‐ versus between‐ramet geitonogamy to the selfing rate of the bumblebee‐pollinated, clonal herb Aconitum kusnezoffii. Data on flowering phenology and bumblebee foraging were also collected to determine opportunities for different modes of self‐pollination. Autogamy accounted for only 12% of the selfing rate with the remainder resulting from geitonogamy. Whole‐ramet emasculation of clones with multiple ramets reduced selfing by 78%, indicating that within‐ramet geitonogamy contributed significantly (68%) to total selfing. Selfing of single‐ramet plants was 44% less than multiple‐ramet plants, indicating that the contribution of between‐ramet geitonogamy was substantially less (20%) than within‐ramet geitonogamy, probably because of bumblebee foraging behavior. Our results demonstrate for the first time in a clonal plant that within‐ramet geitonogamy is substantially greater than between‐ramet geitonogamy and highlight the importance of considering the influence of clonal architecture and pollinator foraging on modes of self‐pollination.     

S-allele diversity suggests no mate limitation in small populations of a self-incompatible plant

Small populations of self-incompatible plants are assumed to be threatened by a limitation of compatible mating partners due to low genetic diversity at the self-incompatibility (S) locus. In contrast, we show by using a PCR-RFLP approach for S-genotype identification that 15 small populations (N = 8-88) of the rare wild pear (Pyrus pyraster) displayed no mate limitation. S-allele diversity within populations was high (N = 9-21) as was mate availability (92.9-100%). Although population size and S-allele diversity were strongly related, no relationship was found between population size and mate availability, gene diversity (He), or fixation index (F(IS)), based on five neutral microsatellite loci. As we determined the principal mate availability within populations based on the S-genotypes observed, the realized mate availability under natural conditions may differ from our estimates, for example, due to spatially limited pollen dispersal. We therefore urge studies on self-incompatible plants to proceed from the simple assessment of principal mate availability to the determination of realized mate availability in natural populations.     

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Pollen movements and mating patterns are key features that influence population genetic structure. When gene flow is low, small populations are prone to increased genetic drift and inbreeding, but naturally disjunct species may have features that reduce inbreeding and contribute to their persistence despite genetic isolation. Using microsatellite loci, we investigated outcrossing levels, family mating parameters, pollen dispersal, and spatial genetic structure in three populations of Hakea oldfieldii, a fire‐sensitive shrub with naturally disjunct, isolated populations prone to reduction in size and extinction following fires. We mapped and genotyped a sample of 102 plants from a large population, and all plants from two smaller populations (28 and 20 individuals), and genotyped 158–210 progeny from each population. We found high outcrossing despite the possibility of geitonogamous pollination, small amounts of biparental inbreeding, a limited number of successful pollen parents within populations, and significant correlated paternity. The number of pollen parents for each seed parent was moderate. There was low but significant spatial genetic structure up to 10 m around plants, but the majority of successful pollen came from outside this area including substantial proportions from distant plants within populations. Seed production varied among seven populations investigated but was not correlated with census population size. We suggest there may be a mechanism to prevent self‐pollination in H. oldfieldii and that high outcrossing and pollen dispersal within populations would promote genetic diversity among the relatively small amount of seed stored in the canopy. These features of the mating system would contribute to the persistence of genetically isolated populations prone to fluctuations in size.     

Reproductive compensation in the evolution of plant mating systems

Reproductive compensation, the replacement of dead embryos by potentially viable ones, is known to play a major role in the maintenance of deleterious mutations in mammalian populations. However, it has received little attention in plant evolution. Here we model the joint evolution of mating system and inbreeding depression with reproductive compensation. We used a dynamic model of inbreeding depression, allowing for partial purging of recessive lethal mutations by selfing. We showed that reproductive compensation tended to increase the mean number of lethals in a population, but favored self-fertilization by effectively decreasing early inbreeding depression. When compensation depended on the selfing rate, stable mixed mating systems can occur, with low to intermediate selfing rates. Experimental evidence of reproductive compensation is required to confirm its potential importance in the evolution of plant mating systems. We suggest experimental methods to detect reproductive compensation.     

Insight into post-mating interactions between the sexes: relatedness suppresses productivity of singly mated female Drosophila melanogaster

Post-mating, prefertilization inbreeding avoidance (PPIA) is well established in plants but not in animals. Support for animal PPIA comes from sperm competition studies showing success of a male's gametes declining with his relatedness to the multiply mated female; however, such studies confound female-male and male-male interaction. To avoid this problem, we investigated offspring productivity of singly mated Drosophila melanogaster females using flies from four different genetic backgrounds. Our experiments established that intrapopulation crosses using highly related parents (within-strain) were significantly less productive than intrapopulation crosses using unrelated individuals from the same population (between-strain). Furthermore, we showed that these effects were not due to inbreeding depression. The average decrease in offspring productivity of within-strain crosses relative to between-strain crosses was 18.3% [nonlaboratory populations: Zimbabwe 20.3%, Riverside 11.4%, neither of which showed inbreeding depression; and temperature-adapted laboratory populations, uncorrected (corrected) for nonsignificant inbreeding depression: 18 degrees C, 26.5% (24.2%) and 29 degrees C, 20.1% (9.5%)]. The significant reduction of within-cross productivity demonstrates PPIA in the absence of multiple mating.     

How relatedness between mates influences reproductive success: An experimental analysis of self‐fertilization and biparental inbreeding in a marine bryozoan

Kin associations increase the potential for inbreeding. The potential for inbreeding does not, however, make inbreeding inevitable. Numerous factors influence whether inbreeding preference, avoidance, or tolerance evolves, and, in hermaphrodites where both self‐fertilization and biparental inbreeding are possible, it remains particularly difficult to predict how selection acts on the overall inbreeding strategy, and to distinguish the type of inbreeding when making inferences from genetic markers. Therefore, we undertook an empirical analysis on an understudied type of mating system (spermcast mating in the marine bryozoan, Bugula neritina) that provides numerous opportunities for inbreeding preference, avoidance, and tolerance. We created experimental crosses, containing three generations from two populations to estimate how parental reproductive success varies across parental relatedness, ranging from self, siblings, and nonsiblings from within the same population. We found that the production of viable selfed offspring was extremely rare (only one colony produced three selfed offspring) and biparental inbreeding more common. Paternity analysis using 16 microsatellite markers confirmed outcrossing. The production of juveniles was lower for sib mating compared with nonsib mating. We found little evidence for consistent inbreeding, in terms of nonrandom mating, in adult samples collected from three populations, using multiple population genetic inferences. Our results suggest several testable hypotheses that potentially explain the overall mating and dispersal strategy in this species, including early inbreeding depression, inbreeding avoidance through cryptic mate choice, and differential dispersal distances of sperm and larvae.     

克隆植物矮嵩草对放牧的等级性反应

对高寒草甸克隆植物矮嵩草（Kobresio humilis）基株、分株片断和分株3个层次构件单元的数量、生物量性状及其变异系数在不同放牧强度处理间以及构件等级间的变化进行了研究。研究工作于1999年至2001年在中国科学院海北高寒草甸生态系统定位站矮嵩草草甸内进行。家畜放牧实验设4个放牧强度水平。研究结果显示,3a中矮嵩草克隆等级基株层次只有分株数和叶数在放牧处理间表现出显著差异（F（3.56）〉F0.05,P〈0．05）,而死亡分株百分数、死亡叶片百分数、基株大小以及繁殖分配4个性状在3a中未表现出显著差异（F（3.56）〈F0.05,P〉0．05）,占被测性状的57．1％;与此同时,分株片断和分株两个层次在第1年就有50％以上的性状达到显著差异,到第3年时全部被测性状都表现出显著差异（F（3.56）〉F0.05,P〈0．05）。放牧第3年时,基株、分株片断和分株层次达到显著差异的性状数分别为42％、100％和100％。性状的变异系数在等级间的变化均表现为分株〉分株片断〉基株层次或分株〉分株片断的顺序。被测性状的变异系数在放牧强度间无显著差异,在放牧第1、第2和第3年,变异系数在等级间有显著差异的性状比例分别为42％、71％和85％。这说明克隆植物矮嵩草基株、分株片断和分株各层次被测性状在放牧强度处理问表现出的差异性不同,具有显著差异的性状比例在基株层次少,在分株片断和分株层次高,相同性状在处理间的差异可能先出现在分株和分株片断层次,后出现在基株层次。放牧强度不影响性状的相对变异,但长期持续的放牧扰动使性状在等级间变异性逐渐增大。这些结果说明矮嵩草构件等级对放牧扰动具有明显的等级性反应,并可概括为“分株层次〉分株片断层次〉基株层次”的等级反应模式。研究结果证实我们关于克隆植物等级选择模式的推断。     

The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor

The social spiders are unusual among cooperatively breeding animals in being highly inbred. In contrast, most other social organisms are outbred owing to inbreeding avoidance mechanisms. The social spiders appear to originate from solitary subsocial ancestors, implying a transition from outbreeding to inbreeding mating systems. Such a transition may be constrained by inbreeding avoidance tactics or fitness loss due to inbreeding depression. We examined whether the mating system of a subsocial spider, in a genus with three social congeners, is likely to facilitate or hinder the transition to inbreeding social systems. Populations of subsocial Stegodyphus lineatus are substructured and spiders occur in patches, which may consist of kin groups. We investigated whether male mating dispersal prevents matings within kin groups in natural populations. Approximately half of the marked males that were recovered made short moves (< 5m) and mated within their natal patch. This potential for inbreeding was counterbalanced by a relatively high proportion of immigrant males. In mating experiments, we tested whether inbreeding actually results in lower offspring fitness. Two levels of inbreeding were tested: full sibling versus non-sib matings and matings of individuals within and between naturally occurring patches of spiders. Neither full siblings nor patch mates were discriminated against as mates. Sibling matings had no effect on direct fitness traits such as fecundity, hatching success, time to hatching and survival of the offspring, but negatively affected offspring growth rates and adult body size of both males and females. Neither direct nor indirect fitness measures differed significantly between within patch and between-patch pairs. We tested the relatedness between patch mates and nonpatch mates using DNA fingerprinting (TE-AFLP). Kinship explained 30% of the genetic variation among patches, confirming that patches are often composed of kin. Overall, we found limited male dispersal, lack of kin discrimination, and tolerance to low levels of inbreeding. These results suggest a history of inbreeding which may reduce the frequency of deleterious recessive alleles in the population and promote the evolution of inbreeding tolerance. It is likely that the lack of inbreeding avoidance in subsocial predecessors has facilitated the transition to regular inbreeding social systems.