Social heterosis and the maintenance of genetic diversity

Genetic diversity in species is often high in spite of directional selection or strong genetic drift. One resolution to this paradox may be through fitness benefits arising from interactions of genetically diverse individuals. Advantageous phenotypes that are impossible in single individuals (e.g. being simultaneously bold and shy) can be expressed by groups composed of genetically different individuals. Genetic diversity, therefore, can produce mutualistic benefits shared by all group members. We define this effect as 'social heterosis', and mathematically demonstrate maintenance of allelic diversity when diverse groups or neighbourhoods are more reproductively successful than homogenous ones. Through social heterosis, genetic diversity persists without: frequency dependence within groups, migration, balancing selection, genetic linkages, overdominance, antagonistic pleiotropy or nonrandom allele assortment. Social heterosis may also offer an alternative evolutionary pathway to cooperation that does not require clustering of related individuals, nepotistic favouritism towards kin, or overt reciprocity.     

'Social heterosis' as a process that maintains genetic variation--a comment

In the 'mating pool' mode of reproduction, offspring genotypes at each generation are taken randomly from a common population and subdivided into groups where individuals representing a finite sample from the pooled distribution reproduce proportional to their fitness. Assuming that genetically diverse groups contribute more offspring, a recent article by Nonacs & Kapheim [J. Evol. Biol. 20 (2007) 2253] shows that allelic diversity can be easily maintained and proposes the process of 'social heterosis' as a potentially powerful mechanism that accounts for a significant amount of genetic variation. Contrary to their suggestions, I show here that there is a reduced efficiency of selection and an increased probability of fixation of segregating alleles when many loci are simultaneously undergoing social heterosis even if independence of action of the different loci and linkage equilibrium are assumed. The critical issue is that linkage disequilibria are generated by the sampling process of creating small groups and interfere with selection.     

Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome

Properly estimating genetic diversity in populations of nonmodel species requires a basic understanding of how diversity is distributed across the genome and among individuals. To this end, we analysed whole‐genome resequencing data from 20 collared flycatchers (genome size ≈1.1 Gb; 10.13 million single nucleotide polymorphisms detected). Genomewide nucleotide diversity was almost identical among individuals (mean = 0.00394, range = 0.00384–0.00401), but diversity levels varied extensively across the genome (95% confidence interval for 200‐kb windows = 0.0013–0.0053). Diversity was related to selective constraint such that in comparison with intergenic DNA, diversity at fourfold degenerate sites was reduced to 85%, 3′ UTRs to 82%, 5′ UTRs to 70% and nondegenerate sites to 12%. There was a strong positive correlation between diversity and chromosome size, probably driven by a higher density of targets for selection on smaller chromosomes increasing the diversity‐reducing effect of linked selection. Simulations exploring the ability of sequence data from a small number of genetic markers to capture the observed diversity clearly demonstrated that diversity estimation from finite sampling of such data is bound to be associated with large confidence intervals. Nevertheless, we show that precision in diversity estimation in large outbred population benefits from increasing the number of loci rather than the number of individuals. Simulations mimicking RAD sequencing showed that this approach gives accurate estimates of genomewide diversity. Based on the patterns of observed diversity and the performed simulations, we provide broad recommendations for how genetic diversity should be estimated in natural populations.     

Multiple Mating But Not Recombination Causes Quantitative Increase in Offspring Genetic Diversity for Varying Genetic Architectures

Explaining the evolution of sex and recombination is particularly intriguing for some species of eusocial insects because they display exceptionally high mating frequencies and genomic recombination rates. Explanations for both phenomena are based on the notion that both increase colony genetic diversity, with demonstrated benefits for colony disease resistance and division of labor. However, the relative contributions of mating number and recombination rate to colony genetic diversity have never been simultaneously assessed. Our study simulates colonies, assuming different mating numbers, recombination rates, and genetic architectures, to assess their worker genotypic diversity. The number of loci has a strong negative effect on genotypic diversity when the allelic effects are inversely scaled to locus number. In contrast, dominance, epistasis, lethal effects, or limiting the allelic diversity at each locus does not significantly affect the model outcomes. Mating number increases colony genotypic variance and lowers variation among colonies with quickly diminishing returns. Genomic recombination rate does not affect intra- and inter-colonial genotypic variance, regardless of mating frequency and genetic architecture. Recombination slightly increases the genotypic range of colonies and more strongly the number of workers with unique allele combinations across all loci. Overall, our study contradicts the argument that the exceptionally high recombination rates cause a quantitative increase in offspring genotypic diversity across one generation. Alternative explanations for the evolution of high recombination rates in social insects are therefore needed. Short-term benefits are central to most explanations of the evolution of multiple mating and high recombination rates in social insects but our results also apply to other species.     

The effects of sample size on population genetic diversity estimates in song sparrows Melospiza melodia

To empirically determine the effects of sample size on commonly used measures of average genetic diversity, we genotyped 200 song sparrows Melospiza melodia from two populations, one genetically depauperate (n=100) and the other genetically diverse (n=100), using eight microsatellite loci. These genotypes were used to randomly create 10,000 datasets of differing sizes (5 to 50) for each population to determine what the effects of sample size might be on several estimates of genetic diversity (number of alleles per locus, average observed heterozygosity, and unbiased average expected heterozygosity) in natural populations of conservation concern. We found that at small sample sizes of 5 to 10 individuals, estimates of unbiased heterozygosity outperformed those based on observed heterozygosity or allelic diversity for both low- and high-diversity populations. We also found that when comparing across populations in which different numbers of individuals were sampled, rarefaction provided a useful way to compare estimates of allelic diversity. We recommend that standard errors should be reported for all diversity estimators, especially when sample sizes are small. We also recommend that at least 20 to 30 individuals be sampled in microsatellite studies that assess genetic diversity when working in a population that has an unknown level of diversity. However, research on critically endangered populations (where large sample sizes are impossible or extremely difficult to obtain) should include measures of genetic diversity even if sample sizes are less than ideal. These estimates can be useful in assessing the genetic diversity of the population.     

海南岛中华蜜蜂遗传多样性的微卫星DNA分析

为了解海南岛中华蜜蜂Apis cerana cerana的遗传多样性和遗传结构及其与大陆种群的关系, 本研究应用10个微卫星DNA标记对海南岛11个地点627个蜂群的627头工蜂样本和大陆2个地点102个蜂群的102头工蜂样本进行了分析。结果表明： 海南岛中华蜜蜂遗传多样性较高, 单个位点检测到等位基因5～17个; 各种群平均等位基因数为4.5～7.0个, 平均杂合度为0.59～0.65。海南岛中华蜜蜂在10个位点上表现出相似遗传结构, 文昌和屯昌种群在AT101位点的等位基因频率较特殊。岛内 岛外中华蜜蜂的遗传分化系数F_ST范围为0.06～0.13; 文昌、 屯昌种群分别同海南岛内其他9个种群的F_ST（0.06～0.12）大于这9个种群间的FST（0～0.05）。海南岛中华蜜蜂同邻近大陆种群发生了明显的遗传分化; 除文昌、 屯昌种群发生中等程度的分化外, 海南岛内其他种群之间遗传分化较小。本研究结果对海南岛中华蜜蜂资源的保护和合理利用具有重要的指导意义。     

Multiple sexual ornaments signal heterozygosity in male blue tits

Higher individual genetic quality has been hypothesized to be associated with the expression of conspicuous ornaments. However, the relationship between multicomponent sexual signals and heterozygosity is poorly understood. In this study, we examined whether different ornaments, including song (repertoire size and bout length) and plumage coloration (yellow breast and blue crown), reflect individual genetic diversity in male blue tits (Aves: Cyanistes caeruleus). We estimated genetic diversity using 26 microsatellite markers that were classified as putatively functional (12 loci) and neutral (14 loci). We found that yellow breast carotenoid chroma, blue crown brightness, bout length and body condition were positively associated with heterozygosity at functional loci, but not with genetic diversity estimated at all typed loci or the subset of neutral markers. The lack of strong single‐locus effects and the presence of identity disequilibrium in our population suggest that the observed heterozygosity‐phenotype associations are driven by loci widely distributed across the genome. The predominant role of putatively functional loci evidences that the expression of secondary sexual characters is more tightly reflected by heterozygosity at genomic regions containing coding genes that are being actively expressed, a fact that may make ornamental traits more reliable indicators of the genetic quality of individuals. Overall, this study shows that multiple secondary sexual characters reflect male genetic diversity and lends support to the good‐genes‐as‐heterozygosity hypothesis. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 362–375.     

Microsatellite and major histocompatibility complex variation in an endangered rattlesnake,the Eastern Massasauga (Sistrurus catenatus)

Genetic diversity is fundamental to maintaining the long‐term viability of populations, yet reduced genetic variation is often associated with small, isolated populations. To examine the relationship between demography and genetic variation, variation at hypervariable loci (e.g., microsatellite DNA loci) is often measured. However, these loci are selectively neutral (or near neutral) and may not accurately reflect genomewide variation. Variation at functional trait loci, such as the major histocompatibility complex (MHC), can provide a better assessment of adaptive genetic variation in fragmented populations. We compared patterns of microsatellite and MHC variation across three Eastern Massasauga (Sistrurus catenatus) populations representing a gradient of demographic histories to assess the relative roles of natural selection and genetic drift. Using 454 deep amplicon sequencing, we identified 24 putatively functional MHC IIB exon 2 alleles belonging to a minimum of six loci. Analysis of synonymous and nonsynonymous substitution rates provided evidence of historical positive selection at the nucleotide level, and Tajima's D provided support for balancing selection in each population. As predicted, estimates of microsatellite allelic richness, observed, heterozygosity, and expected heterozygosity varied among populations in a pattern qualitatively consistent with demographic history and abundance. While MHC allelic richness at the population and individual levels revealed similar trends, MHC nucleotide diversity was unexpectedly high in the smallest population. Overall, these results suggest that genetic variation in the Eastern Massasauga populations in Illinois has been shaped by multiple evolutionary mechanisms. Thus, conservation efforts should consider both neutral and functional genetic variation when managing captive and wild Eastern Massasauga populations.     

High levels of genetic diversity throughout the range of the Portuguese wheat landrace 'Barbela'

BACKGROUND AND AIMS: Landrace populations represent an important intra-crop reservoir of biodiversity and source of novel gene alleles for use in breeding programmes. Here the aim was to measure the diversity of a wheat landrace, 'Barbela', from the north of Portugal. METHODS: DNA was extracted from 59 accessions of Barbela collected across its geographical range. Diversity was measured by microsatellite length polymorphisms using 27 primer pairs amplifying 34 polymorphic microsatellite loci. KEY RESULTS: High levels of polymorphism were found, with an average polymorphism information content of 0.52; an average of 4.77 alleles (range 2-11) were present at each locus, and half of these loci showed an additional allele in the reference variety 'Chinese Spring'. CONCLUSIONS: 'Barbela' is maintained from seeds collected by farmers, but it maintains high allelic variation, and no groupings of accessions were detected when analysed by geographical region, farm or climate, indicating that the wheat landrace is a homogeneous entity. The diversity within the farmer-maintained landrace demonstrates the importance of characterization and maintenance of landrace collections before valuable genetic combinations are lost as uniform commercial crops are introduced.     

Small‐ and large‐scale heterogeneity in genetic variation across the collard flycatcher genome: implications for estimating genetic diversity in nonmodel organisms

Population genetic studies in nonmodel organisms are often hampered by a lack of reference genomes that are essential for whole‐genome resequencing. In the light of this, genotyping methods have been developed to effectively eliminate the need for a reference genome, such as genotyping by sequencing or restriction site‐associated DNA sequencing (RAD‐seq). However, what remains relatively poorly studied is how accurately these methods capture both average and variation in genetic diversity across an organism's genome. In this issue of Molecular Ecology Resources, Dutoit et al. (2016) use whole‐genome resequencing data from the collard flycatcher to assess what factors drive heterogeneity in nucleotide diversity across the genome. Using these data, they then simulate how well different sequencing designs, including RAD sequencing, could capture most of the variation in genetic diversity. They conclude that for evolutionary and conservation‐related studies focused on the estimating genomic diversity, researchers should emphasize the number of loci analysed over the number of individuals sequenced.     

Isolation and characterization of 11 polymerase chain reaction primers for microsatellite loci for the Chilean marine isopod Excirolana hirsuticauda

The Chilean isopod Excirolana hirsuticauda is a marine benthic brooder with wide distributional range and low potential for long-distance dispersal. Eleven microsatellite markers were developed for E. hirsuticauda using enriched libraries. Characterization of those loci in 35 individuals from Playa Blanca beach showed high allelic diversity with a mean of 10.9 alleles per locus. The average expected and observed heterozygosities were 0.65 and 0.41. These microsatellite loci are the first published for any Excirolana species and should be useful to study the genetic structure of E. hirsuticauda.     

A genome scan to detect candidate regions influenced by local natural selection in human populations

As human populations dispersed throughout the world, they were subjected to new selective forces, which must have led to local adaptation via natural selection and hence altered patterns of genetic variation. Yet, there are very few examples known in which such local selection has clearly influenced human genetic variation. A potential approach for detecting local selection is to screen random loci across the genome; those loci that exhibit unusually large genetic distances between human populations are then potential markers of genomic regions under local selection. We investigated this approach by genotyping 332 short tandem repeat (STR) loci in Africans and Europeans and calculating the genetic differentiation for each locus. Patterns of genetic diversity at these loci were consistent with greater variation in Africa and with local selection operating on populations as they moved out of Africa. For 11 loci exhibiting the largest genetic differences, we genotyped an additional STR locus located nearby; the genetic distances for these nearby loci were significantly larger than average. These genomic regions therefore reproducibly exhibit larger genetic distances between populations than the "average" genomic region, consistent with local selection. Our results demonstrate that genome scans are a promising means of identifying candidate regions that have been subjected to local selection.     

Specific microsatellite loci for brook charr reveal strong population subdivision on a microgeographic scale

We have isolated specific microsatellite loci from a partial genomic library of brook charr Salvelinus fontinalis. Their usefulness was investigated by measuring intra- and inter-population genetic diversity at four loci among 20 individuals from each of five lakes located 3 to 22 km apart in La Mauricie national park (Canada). These markers were moderately to highly polymorphic. A total of five, six, 16 and 18 alleles per locus were detected, and their overall expected heterozygosity was 0.53, 0.58, 0.86 and 0.87. Strong inter-population diversity was detected. Highly significant differences in allelic frequencies were found in all but two pairwise χ² permutation tests between populations at all loci. Numerous population unique alleles were observed in all five lakes. Consequently, a highly significant component of total genetic diversity was due to interpopulation variance, as exemplified by G _ST values of 0.33, 0.42, 0.47 and 0.84 for each individual locus. Altogether, the results indicated that these loci should be valuable in addressing fine scale population genetics questions in brook charr. To our knowledge, they also represent the first available microsatellites developed in the genus Salvelinus.     

Three representative inter and intra‐subspecific crosses reveal the genetic architecture of reproductive isolation in rice

Systematic characterization of genetic and molecular mechanisms in the formation of hybrid sterility is of fundamental importance in understanding reproductive isolation and speciation. Using ultra‐high‐density genetic maps, 43 single‐locus quantitative trait loci (QTLs) and 223 digenic interactions for embryo‐sac, pollen, and spikelet fertility are depicted from three crosses between representative varieties of japonica and two varietal groups of indica, which provide an extensive archive for investigating the genetic basis of reproductive isolation in rice. Ten newly detected single‐locus QTLs for inter‐ and intra‐subspecific fertility are identified. Three loci for embryo‐sac fertility are detected in both Nip × ZS97 and Nip × MH63 crosses, whereas QTLs for pollen fertility are not in common between the two crosses thus leading to fertility variation. Five loci responsible for fertility and segregation distortion are observed in the ZS97 × MH63 cross. The importance of two‐locus interactions on fertility are quantified in the whole genome, which identify that three types of interaction contribute to fertility reduction in the hybrid. These results construct the genetic architecture with respect to various forms of reproductive barriers in rice, which have significant implications in utilization of inter‐subspecific heterosis along with improvement in the fertility of indica–indica hybrids at single‐ and multi‐locus level.     

Genetic signature of the northward expansion of the Egyptian mongoose Herpestes ichneumon (Herpestidae) in the Iberian Peninsula

In the last three decades, the range of the Egyptian mongoose (Herpestes ichneumon) has increased in the Iberian Peninsula. A panel of microsatellites was used to confront the patterns of genetic diversity of the species with the scenario of its recent northward expansion in its Iberian range. Evidence of substructure and significant genetic differentiation within the studied population were recorded, with a central‐northern subpopulation (CNorth) and a southern subpopulation (S). Northward range expansion was supported by the observed allelic frequencies, diversity parameters, and observed heterozygosity of the studied loci, with S showing a higher allelic diversity and a higher number of private alleles than CNorth. Patterns of isolation‐by‐distance and isolation‐by‐barrier as a result of the Tagus River were demonstrated, suggesting that the river acted as a semi‐permeable barrier, possibly leading to genetic differentiation of the studied population. The observed individuals from CNorth in southern locations and individuals from S in central/northern areas might comprise evidence for long‐range dispersals across the studied range. A bottleneck event after population expansion was supported by a significant heterozygosity deficiency in CNorth, which is in agreement with a scenario of founder events occurring in recently colonized areas after the crossing of the Tagus River.     

High level of variation at Abies alba chloroplast microsatellite loci in Europe

Based on two polymorphic chloroplast microsatellites that had been previously identified and sequence characterized in the genus Abies, genetic variation was studied in a total of 714 individuals from 17 European silver fir (Abies alba Mill.) populations distributed all over the natural range. We found eight and 18 different length variants at each locus, respectively, which combined into 90 different haplotypes. Genetic distances between most populations were high and significant. There is also evidence for spatial organization of the distribution of haplotypes, as shown by permutation tests, which demonstrate that genetic distances increase with spatial distances. A large heterogeneity in levels of diversity across populations was observed. Furthermore, there is good congruence in the levels of allelic richness of the two loci across populations. The present organization of levels of allelic richness across the range of the species is likely to have been shaped by the distribution of refugia during the last glaciation and the subsequent recolonization processes.     

Indigenous domestic breeds as reservoirs of genetic diversity: the Argentinean Creole cattle

Contrary to highly selected commercial breeds, indigenous domestic breeds are composed of semi-wild or feral populations subjected to reduced levels of artificial selection. As a consequence, many of these breeds have become locally adapted to a wide range of environments, showing high levels of phenotypic variability and increased fitness under natural conditions. Genetic analyses of three loci associated with milk production (alpha(S1)-casein, kappa-casein and prolactin) and the locus BoLA-DRB3 of the major histocompatibility complex indicated that the Argentinean Creole cattle (ACC), an indigenous breed from South America, maintains high levels of genetic diversity and population structure. In contrast to the commercial Holstein breed, the ACC showed considerable variation in heterozygosity (H(e)) and allelic diversity (A) across populations. As expected, bi-allelic markers showed extensive variation in He whereas the highly polymorphic BoLA-DRB3 showed substantial variation in A, with individual populations having 39-74% of the total number of alleles characterized for the breed. An analysis of molecular variance (AMOVA) of nine populations throughout the distribution range of the ACC revealed that 91.9-94.7% of the total observed variance was explained by differences within populations whereas 5.3-8.1% was the result of differences among populations. In addition, the ACC breed consistently showed higher levels of genetic differentiation among populations than Holstein. Results from this study emphasize the importance of population genetic structure within domestic breeds as an essential component of genetic diversity and suggest that indigenous breeds may be considered important reservoirs of genetic diversity for commercial domestic species.     

A meta‐analysis reveals a positive correlation between genetic diversity metrics and environmental status in the long‐lived seagrass Posidonia oceanica

The seagrass Posidonia oceanica is a key engineering species structuring coastal marine systems throughout much of the Mediterranean basin. Its decline is of concern, leading to the search for short‐ and long‐term indicators of seagrass health. Using ArcGIS maps from a recent, high‐resolution (1–4 km) modelling study of 18 disturbance factors affecting coastal marine systems across the Mediterranean (Micheli et al. 2013, http://globalmarine.nceas.ucsb.edu/mediterranean/ ), we tested for correlations with genetic diversity metrics (allelic diversity, genotypic/clonal diversity and heterozygosity) in a meta‐analysis of 56 meadows. Contrary to initial predictions, weak but significantly positive correlations were found for commercial shipping, organic pollution (pesticides) and cumulative impact. This counterintuitive finding suggests greater resistance and resilience of individuals with higher genetic and genotypic diversity under disturbance (at least for a time) and/or increased sexual reproduction under an intermediate disturbance model. We interpret the absence of low and medium levels of genetic variation at impacted locations as probable local extinctions of individuals that already exceeded their resistance capacity. Alternatively, high diversity at high‐impact sites is likely a temporal artefact, reflecting the mismatch with pre‐environmental impact conditions, especially because flowering and sexual recruitment are seldom observed. While genetic diversity metrics are a valuable tool for restoration and mitigation, caution must be exercised in the interpretation of correlative patterns as found in this study, because the exceptional longevity of individuals creates a temporal mismatch that may falsely suggest good meadow health status, while gradual deterioration of allelic diversity might go unnoticed.     

Does harvest affect genetic diversity in grey wolves?

Harvest can affect vital rates such as reproduction and survival, but also genetic measures of individual and population health. Grey wolves (Canis lupus) live and breed in groups, and effective population size is a small fraction of total abundance. As a result, genetic diversity of wolves may be particularly sensitive to harvest. We evaluated how harvest affected genetic diversity and relatedness in wolves. We hypothesized that harvest would (a) reduce relatedness of individuals within groups in a subpopulation but increase relatedness of individuals between groups due to increased local immigration, (b) increase individual heterozygosity and average allelic richness across groups in subpopulations and (c) add new alleles to a subpopulation and decrease the number of private alleles in subpopulations due to an increase in breeding opportunities for unrelated individuals. We found harvest had no effect on observed heterozygosity of individuals or allelic richness at loci within subpopulations but was associated with a small, biologically insignificant effect on within‐group relatedness values in grey wolves. Harvest was, however, positively associated with increased relatedness of individuals between groups and a net gain (+16) of alleles into groups in subpopulations monitored since harvest began, although the number of private alleles in subpopulations overall declined. Harvest likely created opportunities for wolves to immigrate into nearby groups and breed, thereby making groups in subpopulations more related over time. Harvest appears to affect genetic diversity in wolves at the group and population levels, but its effects are less apparent at the individual level given the population sizes we studied.     

High variability and disomic segregation of microsatellites in the octoploid Fragaria virginiana Mill. (Rosaceae)

The objectives of the present study were to develop microsatellite markers for the wild strawberry, Fragaria virginiana, to evaluate segregation patterns of microsatellite alleles in this octoploid species, and assess genetic variability at microsatellite loci in a wild population. A genomic library was screened for microsatellite repeats and several PCR primers were designed and tested. We also tested the use of heterologous primers and found that F. virginiana primers amplified products in cultivated strawberry, Fragaria × ananassa Duch. and Fragaria chiloensis. Similarly, microsatellite loci developed from cultivated strawberry also successfully amplified F. virginiana loci. We investigated four microsatellite loci in detail, three developed from F. virginiana and one from cultivated strawberry. A survey of 100 individuals from a population of F. virginiana in Pennsylvania demonstrated high heterozygosities (H_e or gene diversity ranged from 0.80 to 0.88 per locus) and allelic diversity (12–17 alleles per locus), but individual plants had no more than two alleles per locus. Segregation patterns in parents and progeny of two controlled crosses at these four loci were consistent with disomic Mendelian inheritance. Together these findings suggest that the genome of F. virginiana is "highly diploidized" and at least a subset of microsatellite loci can be treated as codominant, diploid markers. Significant heterozygote deficiencies were found at three of the four loci for hermaphroditic individuals but for only one locus among females in this gynodioecious species.Communicated by J. Dvorak