Long-term overlap of social and genetic structure in free-ranging house mice reveals dynamic seasonal and group size effects

Associating with relatives in social groups can bring benefits such as reduced risk of aggression and increased likelihood of cooperation.Competition among relatives over limited resources,on the other hand,can induce individuals to alter their patterns of association.Population density might further affect the costs and benefits of associating with relatives by altering resource competition or by changing the structure of social groups;preventing easy association with relatives.Consequently,the overlap between genetic and social structure is expected to decrease with increasing population size,as well as during times of increased breeding activity.Here,we use multi-layer network techniques to quantify the similarity between long-term,high resolution genetic,and behavioral data from a large population of free-ranging house mice(Mus musculus domesticus),studied over 10years.We infer how the benefit of associating with genetically similar individuals might fluctuate in relation to breeding behavior and environmental conditions.We found a clear seasonal effect,with decreased overlap between social and genetic structure during summer months,characterized by high temperatures and high breeding activity.Though the effect of overall population size was relatively weak,we found a clear decrease in the overlap between genetic similarity and social associations within larger groups.As well as longer-term within-group changes,these results reveal population-wide short-term shifts in how individuals associate with relatives.Our study suggests that resource competition modifies the trade-off between the costs and benefits of interacting with relatives.     

Population structure, demographic history, and evolutionary patterns of a green-fruited tomato, Solanum peruvianum (Solanaceae), revealed by spatial genetics analyses

? Premise of the study: Wild relatives of crop species have long been viewed as an important genetic resource for crop improvement, but basic information about the population biology of these species is often lacking. This study investigated the population structure, demographic history, and evolutionary patterns of a green-fruited relative of the cultivated tomato, Solanum peruvianum. ? Methods: We investigated spatial genetics of S. peruvianum and screened for loci potentially under natural selection by integrating amplified fragment length polymorphism (AFLP) genotypes, phenotypic data, geography, and geographic information system (GIS)-derived climate data of 19 natural populations. ? Key results: Solanum peruvianum had a moderate degree of population differentiation, likely reflecting partial geographic isolation between species. Populations had a distribution pattern consistent with north-to-south "stepping-stone" dispersal with significant isolation by distance (IBD), similar to other tomato species. Several AFLP loci showed evidence of selection and associated with climate variables. However, phenotypic traits generally did not correlate with climate variables. ? Conclusions: Geographic features of the coastal Andes is likely an important factor that determines the migration pattern and population structure of S. peruvianum, but climatic factors do not appear to be critical for its phenotypic evolution, perhaps due to a high degree of phenotypic plasticity. Spatial genetics of wild relatives of crop species is a powerful approach to understand their evolutionary patterns and to accelerate the discovery of their potential for crop improvements.     

Visual Discrimination of Kin in Mandrills

Phenotype matching, a learning mechanism that evolved based on phenotypic cues shared among relatives, may provide animals with the ability to recognize unfamiliar kin. The generalization of this mechanism across animal species is debated, however, because appropriate tests are difficult to design due to possible confounding effects of familiarity. Hence, only a few studies have examined evidence for the existence of such a mechanism in natural populations. Here, we tested the phenotype matching hypothesis based on visual cues in a semi‐free‐ranging population of mandrills (Mandrillus sphinx) that contains individuals related to different degrees and where familiarity is controlled for. Using an experimental design based on the presentation of photographs, we show that mandrills discriminate unfamiliar relatives using facial cues alone. Our results build on earlier studies, showing that primates use phenotype matching to recognize and subsequently discriminate unfamiliar kin. We suggest that facial features along with other visual and non‐visual cues provide a proximate mechanism for kin selection to operate.     

The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis

The inference of population genetic structures is essential in many research areas in population genetics, conservation biology and evolutionary biology. Recently, unsupervised Bayesian clustering algorithms have been developed to detect a hidden population structure from genotypic data, assuming among others that individuals taken from the population are unrelated. Under this assumption, markers in a sample taken from a subpopulation can be considered to be in Hardy-Weinberg and linkage equilibrium. However, close relatives might be sampled from the same subpopulation, and consequently, might cause Hardy-Weinberg and linkage disequilibrium and thus bias a population genetic structure analysis. In this study, we used simulated and real data to investigate the impact of close relatives in a sample on Bayesian population structure analysis. We also showed that, when close relatives were identified by a pedigree reconstruction approach and removed, the accuracy of a population genetic structure analysis can be greatly improved. The results indicate that unsupervised Bayesian clustering algorithms cannot be used blindly to detect genetic structure in a sample with closely related individuals. Rather, when closely related individuals are suspected to be frequent in a sample, these individuals should be first identified and removed before conducting a population structure analysis.     

Sociality and the rate of molecular evolution

The molecular clock does not tick at a uniform rate in all taxa but may be influenced by species characteristics. Eusocial species (those with reproductive division of labor) have been predicted to have faster rates of molecular evolution than their nonsocial relatives because of greatly reduced effective population size; if most individuals in a population are nonreproductive and only one or few queens produce all the offspring, then eusocial animals could have much lower effective population sizes than their solitary relatives, which should increase the rate of substitution of "nearly neutral" mutations. An earlier study reported faster rates in eusocial honeybees and vespid wasps but failed to correct for phylogenetic nonindependence or to distinguish between potential causes of rate variation. Because sociality has evolved independently in many different lineages, it is possible to conduct a more wide-ranging study to test the generality of the relationship. We have conducted a comparative analysis of 25 phylogenetically independent pairs of social lineages and their nonsocial relatives, including bees, wasps, ants, termites, shrimps, and mole rats, using a range of available DNA sequences (mitochondrial and nuclear DNA coding for proteins and RNAs, and nontranslated sequences). By including a wide range of social taxa, we were able to test whether there is a general influence of sociality on rates of molecular evolution and to test specific predictions of the hypothesis: (1) that social species have faster rates because they have reduced effective population sizes; (2) that mitochondrial genes would show a greater effect of sociality than nuclear genes; and (3) that rates of molecular evolution should be correlated with the degree of sociality. We find no consistent pattern in rates of molecular evolution between social and nonsocial lineages and no evidence that mitochondrial genes show faster rates in social taxa. However, we show that the most highly eusocial Hymenoptera do have faster rates than their nonsocial relatives. We also find that social parasites (that utilize the workers from related species to produce their own offspring) have faster rates than their social relatives, which is consistent with an effect of lower effective population size on rate of molecular evolution. Our results illustrate the importance of allowing for phylogenetic nonindependence when conducting investigations of determinants of variation in rate of molecular evolution.     

Genotypic probabilities for pairs of inbred relatives

Expressions for the joint genotypic probabilities of two related individuals are used in many population and quantitative genetic analyses. These expressions, resting on a set of 15 probabilities of patterns of identity by descent among the four alleles at a locus carried by the relatives, are generally well known. There has been recent interest in special cases where the two individuals are both related and inbred, although there have been differences among published results. Here, we return to the original 15-probability treatment and show appropriate reductions for relatives when they are drawn from a population that itself is inbred or when the relatives have parents who are related. These results have application in affected-relative tests for linkage, and in methods for interpreting forensic genetic profiles.     

Familial identification: population structure and relationship distinguishability

With the expansion of offender/arrestee DNA profile databases, genetic forensic identification has become commonplace in the United States criminal justice system. Implementation of familial searching has been proposed to extend forensic identification to family members of individuals with profiles in offender/arrestee DNA databases. In familial searching, a partial genetic profile match between a database entrant and a crime scene sample is used to implicate genetic relatives of the database entrant as potential sources of the crime scene sample. In addition to concerns regarding civil liberties, familial searching poses unanswered statistical questions. In this study, we define confidence intervals on estimated likelihood ratios for familial identification. Using these confidence intervals, we consider familial searching in a structured population. We show that relatives and unrelated individuals from population samples with lower gene diversity over the loci considered are less distinguishable. We also consider cases where the most appropriate population sample for individuals considered is unknown. We find that as a less appropriate population sample, and thus allele frequency distribution, is assumed, relatives and unrelated individuals become more difficult to distinguish. In addition, we show that relationship distinguishability increases with the number of markers considered, but decreases for more distant genetic familial relationships. All of these results indicate that caution is warranted in the application of familial searching in structured populations, such as in the United States.     

Evidence for inheritance in patients with VACTERL association

VACTERL/VATER association is typically a sporadic disorder. We present data on inheritance in 78 probands with VACTERL association, and show that 9% of probands have a primary relative with at least one component feature of VACTERL association. The prevalence of component features in first-degree relatives is significantly higher than expected in the general population, which has implications for counseling of affected families and for research into possible etiologies.     

Covariances of relatives stemming from a population undergoing mixed self and random mating

We consider covariances of all parent and first-generation relatives from outcrossing or self-fertilization in a parent population that is in equilibrium with respect to these processes. The results, which are for any number of alleles and loci with additive and dominance effects, are phrased in terms of six quadratic genetic components whose coefficients are given by descent measures for equilibrium populations. Because of the variation in the inbreeding coefficients for this system of mating, the expressions include joint contributions of loci to the variances and covariances of relatives. By inclusion of the full complement of relatives, all quadratic components can be estimated. The findings of Ghai (1982, Biometrics 38, 87-92) for compound functions of the covariances with two alleles at a single locus are analyzed in terms of the more general model.     

The evolution of floral signals in relation to range overlap in a clade of California Jewelflowers (Streptanthus s.l.)

Because of their function as reproductive signals in plants, floral traits experience distinct selective pressures related to their role in speciation, reinforcement, and prolonged coexistence with close relatives. However, few studies have investigated whether population‐level processes translate into detectable signatures at the macroevolutionary scale. Here, we ask whether patterns of floral trait evolution and range overlap across a clade of California Jewelflowers reflect processes hypothesized to shape floral signal differentiation at the population level. We found a pattern of divergence in floral scent composition across the clade such that close relatives had highly disparate floral scents given their age. Accounting for range overlap with close relatives explained additional variation in floral scent over time, with sympatric species pairs having diverged more than allopatric species pairs given their age. However, three other floral traits (flower size, scent complexity and flower color) did not fit these patterns, failing to deviate from a null Brownian motion model of evolution. Together, our results suggest that selection for divergence among close relatives in the composition of floral scents may play a key, sustained role in mediating speciation and coexistence dynamics across this group, and that signatures of these dynamics may persist at the macroevolutionary scale.     

The population genetics of assortative mating based on imprinting

This paper is concerned with the population effects of mating preferences for inherited traits. We suppose that the trait is determined by a pair of alleles and concentrate on the autosomal case with complete dominance. We are interested in the case when the mating preferences are determined by the phenotype of relatives, such as parents or sibs. This is a possible consequence of imprinting, a kind of learning process which occurs early after birth in warmblooded vertebrates. In spite of the greater analytical complexity of these models, their results are very similar to those found when the preference is determined by the phenotype of the mating individual itself. In particular the preference for the same phenotype as that of relatives usually leads to the fixation of either morph, depending on the initial frequency. Polymorphism, on the other hand, always results when the preference is for a phenotype which differs from that of relatives.     

Family and Fertility: Kin Influence on the Progression to a Second Birth in the British Household Panel Study

Particular features of human female life history, such as short birth intervals and the early cessation of female reproduction (menopause), are argued to be evidence that humans are ‘cooperative breeders’, with a reproductive strategy adapted to conditions where mothers receive substantial assistance in childraising. Evolutionary anthropologists have so far largely focussed on measuring the influence of kin on reproduction in natural fertility populations. Here we look at the effect in a present-day low-fertility population, by analysing whether kin affect parity progression in the British Household Panel Study. Two explanatory variables related to kin influence significantly increase the odds of a female having a second birth: i) having relatives who provide childcare and ii) having a larger number of frequently contacted and emotionally close relatives. Both effects were measured subject to numerous socio-economic controls and appear to be independent of one another. We therefore conclude that kin may influence the progression to a second birth. This influence is possibly due to two proximate mechanisms: kin priming through communication and kin assistance with childcare.     

Family based studies and genetic epidemiology: theory and practice

Family based studies have underpinned many successes in uncovering the causes of monogenic and oligogenic diseases. Now research is focussing on the identification and characterisation of genes underlying common diseases and it is widely accepted that these studies will require large population based samples. Population based family study designs have the potential to facilitate the analysis of the effects of both genes and environment. These types of studies integrate the population based approaches of classic epidemiology and the methods enabling the analysis of correlations between relatives sharing both genes and environment. The extent to which such studies are feasible will depend upon population- and disease-specific factors. To review this topic, a symposium was held to present and discuss the costs, requirements and advantages of population based family study designs. This article summarises the features of the meeting held at The University of Sheffield, August 2006.     

Cancer in relatives of leukemic patients with chromosomal rearrangements at rare (heritable) fragile-site locations in their malignant cells.

The cancer occurrence in relatives (N = 407) of 40 case probands (who had leukemia and rearrangements at the same chromosomal location as at least one of 23 recognized rare [heritable] autosomal fragile sites [Sutherland and Mattei 1987]) was compared both to cancer occurrence in relatives (N = 390) of 40 control probands (who had leukemia or other hematologic illness but no recognized chromosomal rearrangements) and to cancer incidence in the general population of the United States. Fragile-site carrier status was not determined in case or control probands. No significant excess of cancer in case relatives, compared with either control relatives or to general (SEER) population expectancies, was found. Furthermore, there was neither evidence of cancer at younger ages, when cases were compared with control relatives, nor an excess of cancer at multiple sites. Male relatives of cases did, however, show a small excess of cancer, especially in older age groups. There was a slight, but not statistically significant, excess of lung cancer in case relatives, with this deviation occurring almost exclusively in relatives of probands having rearrangements at 11q23 and having lymphoid leukemia. It is possible that heritable tendency to chromosomal rearrangement--and thus to cancer--is expressed in such a small proportion of family members that cancer excess in these families could not be detected with the numbers of relatives analyzed in this study, although there was no significant evidence for a hereditary predisposition to cancer in the families of probands with leukemia and with chromosomal rearrangements at the same apparent chromosomal location as rare fragile sites.     

Evidence for frequent incest in a cooperatively breeding mammal

As breeding between relatives often results in inbreeding depression, inbreeding avoidance is widespread in the animal kingdom. However, inbreeding avoidance may entail fitness costs. For example, dispersal away from relatives may reduce survival. How these conflicting selection pressures are resolved is challenging to investigate, but theoretical models predict that inbreeding should occur frequently in some systems. Despite this, few studies have found evidence of regular incest in mammals, even in social species where relatives are spatio-temporally clustered and opportunities for inbreeding frequently arise. We used genetic parentage assignments together with relatedness data to quantify inbreeding rates in a wild population of banded mongooses, a cooperatively breeding carnivore. We show that females regularly conceive to close relatives, including fathers and brothers. We suggest that the costs of inbreeding avoidance may sometimes outweigh the benefits, even in cooperatively breeding species where strong within-group incest avoidance is considered to be the norm.     

Correlations between relatives in small populations

Correlations between relatives in small, closed populations can be substantially smaller than predicted by the classical formulas of population genetics. This effect is especially pronounced for relatives whose most recent common ancestor is several generations removed. When the effective population size is small, correlations between even close relatives can be negative. This implies that in small populations conventional estimators of quantitative genetics parameters will be biased and that preferential treatment of close relatives will be less likely to evolve.     

Familial predisposition to cancer and age at onset of disease in randomly selected cancer patients

Incidence of malignancy among close relatives was used to evaluate the relationship of early age at diagnosis and familial cancer predisposition in a general population of cancer patients. The occurrence of cancer and other conditions in families of more than 1,350 randomly selected patients with a wide variety of malignancies was ascertained. Each patient was assigned to one of four study groups based on comparison of his age at diagnosis with the distribution of ages at diagnosis for his cancer site compiled by the Third National Cancer Survey. These groups consisted of patients whose ages at diagnosis were in: (1) the lowest decile, (2) the median decile, (3) above the median decile, and (4) between the lowest and median deciles. Person-years and calendar time at risk were calculated for first-degree relatives in each group. The numbers of cancers expected among these relatives were calculated using age- and time-specific incidence rates of a standard population. Statistical analysis of (1) the numbers of reported vs. expected cancers in relatives and (2) the numbers of families reporting cancer in parents or siblings of patients showed that a familial tendency to develop cancer exists in this randomly selected population of cancer patients, regardless of age at onset of malignancy in the proband. Conversely, early age at diagnosis of cancer may indicate genetic predisposition to malignancy only in exceptional cases.     

Analysis of “nontraditional” relationships under assortative mating

The set of conditions on the genetical and developmental mechanisms of quantitative characters as well as on selection and mating system presented in (Gimelfarb, 1981) is expanded, thus enabling one to obtain the genotypic covariances between relatives for a larger variety of relationships. It is also demonstrated that the frequency of a relationship in a population under assortative mating may in general be different from the frequency of this relationship in the population under random mating. A subpopulation of relatives is not necessarily a representative sample of the whole population with respect to the quantitative character distribution. However, for any relationship which is a combination of descendant-ancestor, full sib, Type 1 and Nth uncle-niece relationships, its frequency in a population under assortative mating is the same as in the population under random mating, and the subpopulation of such relatives is a representative sample of the whole population.Paper No. 6620 of the Journal Series of the North Carolina Agricultural Research Service, Raleigh, North Carolina. This investigation was supported in part by NIH Research Grant No. GM 11546 from the National Institute of General Medical Sciences     

Evidence for maternally inherited factors favouring male homosexuality and promoting female fecundity

The Darwinian paradox of male homosexuality in humans is examined, i.e. if male homosexuality has a genetic component and homosexuals reproduce less than heterosexuals, then why is this trait maintained in the population? In a sample of 98 homosexual and 100 heterosexual men and their relatives (a total of over 4600 individuals), we found that female maternal relatives of homosexuals have higher fecundity than female maternal relatives of heterosexuals and that this difference is not found in female paternal relatives. The study confirms previous reports, in particular that homosexuals have more maternal than paternal male homosexual relatives, that homosexual males are more often later-born than first-born and that they have more older brothers than older sisters. We discuss the findings and their implications for current research on male homosexuality.     

Genetic structure of an Apis dorsata population: the significance of migration and colony aggregation

Eight microsatellite loci were used to investigate the genetic structure of the giant honeybee (Apis dorsata) population in northeast India. This species migrates seasonally between summer and winter nesting sites, and queens appear to return to their previously occupied site. Furthermore, there is a strong tendency for colonies of this species to aggregate at perennially utilized nesting sites that may be shared by more than 150 colonies. These behavioral features suggest that colonies within aggregations should be more related than random colonies, but that the long-distance migration could act to minimize genetic differentiation both between geographical areas and within aggregations. Our genetic study supports these conjectures arising from natural history. A. dorsata aggregations are comprised of colonies that share more alleles than expected by chance. Although queens heading neighboring colonies are not close relatives, fixation indices show significant genetic differentiation among aggregation sites. However, there appears to be sufficient gene flow among aggregations to prevent high degrees of relatedness developing between colonies within aggregations. The results also suggest that there is significant population structuring between geographical regions, although the level of structuring caused by aggregation exceeds the differentiation attributable to geographic region.