Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny

With an increasing amount of data becoming available, comparative analyses have called attention to the associations between cooperative breeding, monogamy and relatedness. We focus here upon the association between allomaternal care and relatedness among females within a social unit. Previous studies found a positive association, but such results date back to before molecular tools were in common use, they considered only a few mammalian orders, neglected phylogenetic clustering and/or did not correct for group sizes. Here, we use molecular data on relatedness from 44 species of mammals to investigate the phylogenetic clustering of, and the association between, allomaternal care and relatedness among females within a social unit. We find (i) a strong phylogenetic signal for allomaternal care and a moderate one for relatedness and group size, and (ii) a positive association between relatedness and allomaternal care, even when correcting for the smaller than average group sizes in species with allomaternal care. We also find that, in species without allomaternal care, adult females often live with unrelated females even when groups are small. We discuss these results in the light of recent evidence for the role of kin selection and the monogamy hypothesis in cooperative breeding.     

Setaria genome sequencing: an overview

The genus Setaria includes two important C₄ Panicoid grass species, namely S. italica (cultivated) and S. viridis (weed; wild ancestor), which together represent an appropriate model system for architectural, physiological, evolutionary, and genomic studies in related grasses. It is a diploid, inbreeder, self-fertile annual cereal grass having short life cycle and minimal growth requirements. There close relatedness to biofuel crops like switch grass and napier grass further signifies their importance. Further, foxtail millet is an important food and fodder grain crop grown in arid and semi-arid regions in many parts of the world. Therefore, an increasing interest in these species has led to a gradual accumulation and development of genomic data and genetic resources. Setaria genome sequencing is an outcome of such endeavors. These sequencing efforts uncovered several distinctive attributes of Setaria genome that may help in understanding its physiology, evolution and adaptation. This will not only aid in comparative genomics studies of Setaria and related crops including bioenergy grasses but also help in rapid advancements of genomics information for developing varieties with superior traits either through marker-assisted selection (MAS) or using transgenic approaches in these crops.     

Bridging meta-analysis and the comparative method: a test of seed size effect on germination after frugivores’ gut passage

Most studies using meta-analysis try to establish relationships between traits across taxa from interspecific databases and, thus, the phylogenetic relatedness among these taxa should be taken into account to avoid pseudoreplication derived from common ancestry. This paper illustrates, with a representative example of the relationship between seed size and the effect of frugivores gut on seed germination, that meta-analytic procedures can also be phylogenetically corrected by means of the comparative method. The conclusions obtained in the meta-analytical and phylogenetical approaches are very different. The meta-analysis revealed that the positive effects that gut passage had on seed germination increased with seed size in the case of gut passage through birds whereas decreased in the case of gut passage through non-flying mammals. However, once the phylogenetic relatedness among plant species was taken into account, the effects of gut passage on seed germination did not depend on seed size and were similar between birds and non-flying mammals. Some methodological considerations are given to improve the bridge between the meta-analysis and the comparative method.     

Using average nucleotide identity (ANI) to evaluate microsporidia species boundaries based on their genetic relatedness

Microsporidia are obligatory intracellular parasites related to fungi and since their discovery their classification and origin has been controversial due to their unique morphology. Early taxonomic studies of microsporidia were based on ultrastructural spore features, characteristics of their life cycle and transmission modes. However, taxonomy and phylogeny based solely on these characteristics can be misleading. SSU rRNA is a traditional marker used in taxonomical classifications, but the power of SSU rRNA to resolve phylogenetic relationships between microsporidia is considered weak at the species level, as it may not show enough variation to distinguish closely related species. Overall genome relatedness indices (OGRI), such as average nucleotide identity (ANI), allows fast and easy-to-implement comparative measurements between genomes to assess species boundaries in prokaryotes, with a 95% cutoff value for grouping genomes of the same species. Due to the increasing availability of complete genomes, metrics of genome relatedness have been applied for eukaryotic microbes taxonomy such as microsporidia. However, the distribution of ANI values and cutoff values for species delimitation have not yet been fully tested in microsporidia. In this study we examined the distribution of ANI values for 65 publicly available microsporidian genomes and tested whether the 95% cutoff value is a good estimation for circumscribing species based on their genetic relatedness.     

Association of an MHC Class II Haplotype with Increased Risk of Polymyositis in Hungarian Vizsla Dogs

A breed-specific polymyositis is frequently observed in the Hungarian Vizsla. Beneficial clinical response to immunosuppressive therapies has been demonstrated which points to an immune-mediated aetiology. Canine inflammatory myopathies share clinical and histological similarities with the human immune-mediated myopathies. As MHC class II associations have been reported in the human conditions we investigated whether an MHC class II association was present in the canine myopathy seen in this breed. 212 Hungarian Vizsla pedigree dogs were stratified both on disease status and degree of relatedness to an affected dog. This generated a group of 29 cases and 183 “graded” controls: 93 unaffected dogs with a first degree affected relative, 44 unaffected dogs with a second degree affected relative, and 46 unaffected dogs with no known affected relatives. Eleven DLA class II haplotypes were identified, of which, DLA-DRB1*02001/DQA1*00401/DQB1*01303, was at significantly raised frequency in cases compared to controls (OR = 1.92, p = 0.032). When only control dogs with no family history of the disease were compared to cases, the association was further strengthened (OR = 4.08, p = 0.00011). Additionally, a single copy of the risk haplotype was sufficient to increase disease risk, with the risk substantially increasing for homozygotes. There was a trend of increasing frequency of this haplotype with degree of relatedness, indicating low disease penetrance. These findings support the hypothesis of an immune-mediated aetiology for this canine myopathy and give credibility to potentially using the Hungarian Vizsla as a genetic model for comparative studies with human myositis.     

Preferences of newborn mice for odours indicating closer genetic relatedness: is experience necessary?

Evidence from studies with adult rodents indicates that individual recognition enables distinctions between familiar individuals irrespective of relatedness (but including close kin) and a separate mechanism enables discriminations based on genetic relatedness without prior familiarity. For example, adult mice could assess the extent of their genetic relatedness to unfamiliar individuals using perceptual similarities between their individual odours. The ontogeny of this genetic relatedness assessment mechanism, however, had not been investigated. Here, in two-choice tests, newborn mice differentially preferred odours of more genetically similar lactating females (paternal aunts to unrelated conspecific and conspecific to heterospecific) even without prior direct exposure to adults with the tested genotypes. The results provide a direct demonstration of genetic relatedness assessment abilities in newborns and show that experience with parental odours is not necessary for genetic relatedness distinctions. Future studies will be necessary to determine whether exposure to odours of other foetuses in the womb or littermates shortly after birth affects this genetic relatedness assessment process.     

Comparative aspects of transferrin-reticulocyte interactions: membrane receptors and iron uptake

1. A comparative study was made of transferrin and iron uptake by rabbit, rat and human reticulocytes and chick embryo erythrocytes from rabbit, rat, human, chicken and porcine transferrins, human lactoferrin and chicken conalbumin. 2. Three methods were used, viz. direct and competitive uptake studies of transferrin and iron by the four species of cells, and competitive studies of transferrin binding by solubilized membrane receptors (rabbit reticulocytes only). 3. Methods were devised to analyse the data so as to obtain indices of relatedness or relative affinities of each type of heterologous transferrin in rates of iron uptake found with transferrin and cells from various species are largely due to variation in the affinity of cellular receptors for different transferrins. 5. It is concluded that the procedure used in this investigation allow the assessment of phylogenetic relationships and evolutionary trends obtained by structural studies of proteins.     

Male reproductive skew, paternal relatedness, and female social relationships

Female social relationships among primates are thought to be shaped by socio-ecological factors and phylogenetic constraints. We suggest that patterns of paternal relatedness among females influence measures of social tolerance that have been used to classify species into different social relationship categories. As kin support and kin preference have only been measured for matrilineal kin and related individuals exchange less aggression and have a higher conciliatory tendency, the observed low nepotism levels and high tolerance levels may be an artifact of hidden paternal relatedness among the nonkin category. Using comparative data on macaques, we investigate this hypothesis using male reproductive skew as a proxy for paternal relatedness. Within the limitations of the study we show that populations classified as being less nepotistic, and more tolerant exhibit higher levels of reproductive skew. This first result and the reasoning behind may motivate future students of social relationships to take paternal relatedness into consideration. Potential implications of this finding if repeated with larger samples include that variation in aspects of macaque social relationships may be explained without considering phylogeny or the strength of between-group contest competition for food.     

Pedigree relatedness, not greenbeard genes, explains eusociality

The evolution of eusociality, where some individuals altruistically forgo reproduction, poses a dilemma which can be solved by kin selection, i.e. by considering relatedness among cooperating individuals. Most often, such relatedness is caused by pedigree relationships between family members. However, an alternative explanation has recently emerged in an article by Wilson and Hölldobler (2005) . Wilson and Hölldobler see the ecological benefit of group living as the principal reason for sociality. In their scenario, individuals sharing the same altruistic allele (analogous to a greenbeard gene) preferentially interact with each other, regardless of pedigree relatedness. We argue that empirical evidence has the potential to answer the question of whether pedigree relatedness plays a role in the evolution of eusociality. We conclude that both phylogenetic studies and studies of intra-genomic conflict support the importance of pedigree relatedness in the evolution of eusociality.     

related: an R package for analysing pairwise relatedness from codominant molecular markers

Analyses of pairwise relatedness represent a key component to addressing many topics in biology. However, such analyses have been limited because most available programs provide a means to estimate relatedness based on only a single estimator, making comparison across estimators difficult. Second, all programs to date have been platform specific, working only on a specific operating system. This has the undesirable outcome of making choice of relatedness estimator limited by operating system preference, rather than being based on scientific rationale. Here, we present a new R package, called related, that can calculate relatedness based on seven estimators, can account for genotyping errors, missing data and inbreeding, and can estimate 95% confidence intervals. Moreover, simulation functions are provided that allow for easy comparison of the performance of different estimators and for analyses of how much resolution to expect from a given data set. Because this package works in R, it is platform independent. Combined, this functionality should allow for more appropriate analyses and interpretation of pairwise relatedness and will also allow for the integration of relatedness data into larger R workflows.     

Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population

We investigated patterns of relatedness and reproduction in a population of striped hyenas in which individuals are behaviourally solitary but form polyandrous spatial groups consisting of one adult female and multiple adult males. Group-mate males were often close relatives, but were unrelated or distantly related in some cases, indicating that male coalitions are not strictly a result of philopatry or dispersal with cohorts of relatives. Most male-female pairs within spatial groups were unrelated or only distantly related. Considering patterns of relatedness between groups, relatedness was significantly higher among adult males living in non-neighbouring ranges than among neighbouring males. Mean relatedness among male-female dyads was highest for group-mates, but relatedness among non-neighbouring males and females was also significantly higher than among dyads of opposite-sex neighbours. Female-female relatedness also increased significantly with increasing geographic separation. These unusual and unexpected patterns may reflect selection to settle in a nonadjacent manner to reduce inbreeding and/or competition among relatives for resources (both sexes), or mates (males). Finally, resident males fathered the majority of the resident female's cubs, but extra-group paternity was likely in 31% of the cases examined, and multiple paternity was likely in half of the sampled litters.     

Confounding from cryptic relatedness in case-control association studies

Case-control association studies are widely used in the search for genetic variants that contribute to human diseases. It has long been known that such studies may suffer from high rates of false positives if there is unrecognized population structure. It is perhaps less widely appreciated that so-called “cryptic relatedness” (i.e., kinship among the cases or controls that is not known to the investigator) might also potentially inflate the false positive rate. Until now there has been little work to assess how serious this problem is likely to be in practice. In this paper, we develop a formal model of cryptic relatedness, and study its impact on association studies. We provide simple expressions that predict the extent of confounding due to cryptic relatedness. Surprisingly, these expressions are functions of directly observable parameters. Our analytical results show that, for well-designed studies in outbred populations, the degree of confounding due to cryptic relatedness will usually be negligible. However, in contrast, studies where there is a sampling bias toward collecting relatives may indeed suffer from excessive rates of false positives. Furthermore, cryptic relatedness may be a serious concern in founder populations that have grown rapidly and recently from a small size. As an example, we analyze the impact of excess relatedness among cases for six phenotypes measured in the Hutterite population.     

Conflict over male parentage in social insects

Mutual policing is an important mechanism that maintains social harmony in group-living organisms by suppressing the selfish behavior of individuals. In social insects, workers police one another (worker-policing) by preventing individual workers from laying eggs that would otherwise develop into males. Within the framework of Hamilton's rule there are two explanations for worker-policing behavior. First, if worker reproduction is cost-free, worker-policing should occur only where workers are more closely related to queen- than to worker-produced male eggs (relatedness hypothesis). Second, if there are substantial costs to unchecked worker reproduction, worker-policing may occur to counteract these costs and increase colony efficiency (efficiency hypothesis). The first explanation predicts that patterns of the parentage of males (male parentage) are associated with relatedness, whereas the latter does not. We have investigated how male parentage varies with colony kin structure and colony size in 50 species of ants, bees, and wasps in a phylogenetically controlled comparative analysis. Our survey revealed that queens produced the majority of males in most of the species and that workers produced more than half of the males in less than 10% of species. Moreover, we show that male parentage does not vary with relatedness as predicted by the relatedness hypothesis. This indicates that intra- and interspecific variation in male parentage cannot be accounted for by the relatedness hypothesis alone and that increased colony efficiency is an important factor responsible for the evolution of worker-policing. Our study reveals greater harmony and more complex regulation of reproduction in social insect colonies than that expected from simple theoretical expectations based on relatedness only.     

High relatedness in a social amoeba: the role of kin-discriminatory segregation

A major challenge for social theory is to explain the importance of kin discrimination for the evolution of altruism. One way to assess the importance of kin discrimination is to test its effects on increasing relatedness within groups. The social amoeba Dictyostelium discoideum aggregates to form a fruiting body composed of dead stalk and live spores. Previous studies of a natural population showed that where D. discoideum occurs in the soil, multiple clones are often found in the same small soil samples. However, actual fruiting bodies usually contain only one clone. We here performed experiments to gauge the effect of kin-discriminatory segregation on increasing relatedness. We mixed co-occurring clones from this population using a relatedness level found in small soil samples. We found a lower proportion of uniclonal fruiting bodies and a lower level of relatedness compared with natural fruiting bodies. We found that the amount of relatedness increase attributable to kin-discriminatory segregation was small. These findings suggest a relatively minor influence of kin-discriminatory segregation on relatedness in D. discoideum. We discuss our results comparing with the results of previous studies, including those of wild clones and laboratory mutants. We ask why wild clones of D. discoideum exhibit a low degree of kin-discriminatory segregation, and what alternative factors might account for high relatedness in D. discoideum.     

Influence of male relatedness on lethal combat in fig wasps: a theoretical analysis

In many fig wasp species, flightless males fatally fight with rivals. In a recent comparative analysis, West and colleagues found no influence of male relatedness on the frequency of fatal fighting. Inspired by this study, I used a simple theoretical model to examine the conditions that should influence the probability of fatal fighting in a closed mating system. I show that, without kin recognition, relatedness can be expected to have no influence on the frequency of fatal fighting. Under such conditions, males should fight if their chance of winning is greater than a threshold determined by the number of competitors. If males recognize kin, a non-linear relationship between relatedness and the frequency of fatal fighting can be expected. However, two other factors should also be important when there is kin recognition: male number and variance in male fighting strength can be shown to have decisive influences on the frequency of fatal fighting. My results thus corroborate and explain one finding of the empirical study--that there is no significant influence of relatedness on fatal fighting--but point to a role for other factors besides foundress number--male number and male variance in fighting strength. These are probably important factors determining the occurrence of lethal combat in fig wasps.     

Does kin structure explain the occurrence of workers in a lower termite?

Kinship plays a fundamental role in the origin of social life. It is also predicted to affect numerous details within animal societies, yet recent studies revealed equivocal results. We tested the influence of relatedness for the occurrence of workers in the termite Cryptotermes secundus. Here individuals are developmentally flexible to remain workers or to become dispersing sexuals that found new colonies. Furthermore, colony relatedness naturally increases with inbreeding and decreases when neighboring colonies fuse. Similar to recent studies on social Hymenoptera, our experimental change in relatedness gave equivocal results. Reducing relatedness within colonies did not have an effect, but individuals in inbred colonies were less likely to disperse and more likely to remain workers as predicted by kinship arguments. Several explanations for the interpretation of these equivocal results are provided.     

pedantics: an r package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing

Analyses of pedigrees and pedigree-derived parameters (e.g. relatedness and fitness) provide some of the most informative types of studies in evolutionary biology. The r package pedantics implements tools to facilitate power and sensitivity analyses of pedigree-related studies of natural populations. Functions are available to permute pedigree data in various ways with the goal of mimicking patterns of pedigree errors and missingness that occur in studies of natural populations. Another set of functions simulates genetic and phenotypic data based on arbitrary pedigrees. Finally, functions are also available with which visual and numerical representations of pedigree structure can be generated.     

Increased nest cofounding and high intra-colony relatedness in the bee Exoneura bicolor (Hymenoptera: Apidae): Results from an experimental situation

Abstract Identifying differences in a key social trait between two populations of die same species is important for understanding the evolution of sociality. Previous studies of new colonies in Exoneura bicolor, an Australian allodapine bee, have shown that there are high levels of kin cofounding in a montane population. The only study to examine intra-colony relatedness in a heathland population has found that new multifemale colonies are not formed by kin. In this study we used an experiment to investigate both cofounding behaviour and intra-colony relatedness in E. bicolor from a heathland population. Nest substrate was placed either 0.05 or 1 m distant from source nests in a novel environment. Although there were no differences in cofounding rate or intra-colony relatedness between die two treatments there was, overall, a high rate of cofounding: 53% of new nests were multifemale, approximately twice as high as found in previous field-based studies. Relatedness among cofoundresses was not only different from zero, ^r± SE = 0.597 ± 0.097, but almost identical to that found in montane populations. A constraint, such as nest substrate distribution, is suggested as a proximate factor affecting the expression of cofounding behaviour in E. bicolor. The implication of such proximate constraints for inferring the phylogenetic origins of social behaviour is discussed.     

Quality and quantity of genetic relatedness data affect the analysis of social structure

Kinship plays a fundamental role in the evolution of social systems and is considered a key driver of group living. To understand the role of kinship in the formation and maintenance of social bonds, accurate measures of genetic relatedness are critical. Genotype‐by‐sequencing technologies are rapidly advancing the accuracy and precision of genetic relatedness estimates for wild populations. The ability to assign kinship from genetic data varies depending on a species’ or population's mating system and pattern of dispersal, and empirical data from longitudinal studies are crucial to validate these methods. We use data from a long‐term behavioural study of a polygynandrous, bisexually philopatric marine mammal to measure accuracy and precision of parentage and genetic relatedness estimation against a known partial pedigree. We show that with moderate but obtainable sample sizes of approximately 4,235 SNPs and 272 individuals, highly accurate parentage assignments and genetic relatedness coefficients can be obtained. Additionally, we subsample our data to quantify how data availability affects relatedness estimation and kinship assignment. Lastly, we conduct a social network analysis to investigate the extent to which accuracy and precision of relatedness estimation improve statistical power to detect an effect of relatedness on social structure. Our results provide practical guidance for minimum sample sizes and sequencing depth for future studies, as well as thresholds for post hoc interpretation of previous analyses.     

Confounding from cryptic relatedness in haplotype-based association studies

Cryptic relatedness was suggested to be an important source of confounding in population-based association studies (PBAS). The impact of cryptic relatedness on the performance of haplotype phase inference and haplotype-based association tests is not clear. In this study, we used the Hapmap genetic data to simulate a set of related samples. We evaluated the accuracy of haplotype phase inferred by PHASE 2.1 and calculated the power, type I error rates, accuracy and positive prediction value (PPV) of haplotype frequency-based association tests (HFAT) and haplotype similarity-based association tests (HSAT) under various scenarios, considering relatedness levels, disease models and sample sizes. Cryptic relatedness appeared to slightly increase the accuracy of haplotype phase inference. We observed significant negative effect of cryptic relatedness on the performance of HFAT and HSAT. Ignoring cryptic relatedness may increase spurious association results in haplotype-based PBAS.