Balancing selection shapes population differentiation of major histocompatibility complex genes in wild golden snub-nosed monkeys

Small and isolated populations face several intrinsic risks,such as genetic drift,inbreeding depression,and reduced gene fow.Thus,patterns of genetic diversity and differentiation have become an important focus of conservation genetics research.The golden snub-nosed monkey Rhinopithecus roxellana,an endangered species endemic to China,has experienced rapid reduction in population size and severe population fragmentation over the past few decades.We measured the patterns of genetic diversity and population differentiation using both neutral microsatellites and adaptive major histocompatibility complex(MHC)genes in 2 R.roxellana populations(DPY and GNG)distributed on the northern and southern slopes of the Qinling Mountains,respectively.Eight MHC-linked haplotypes formed by 5 DQA1 alleles,5 DQB1 alleles,5 DRB1 alleles,and 4 DRB2 alleles were detected in the 2 populations.The larger GNG population showed higher genetic variation for both MHC and microsatellites than the smaller DPY population,suggesting an effect of genetic drift on genetic variation.Genetic differentiation index(FST)outlier analyses,principal coordinate analysis(PCoA),and inferred population genetic structure showed lower genetic differentiation in the MHC variations than microsatellites,suggesting that pathogen-mediated balancing selection,rather than local adaptation,homogenized the MHC genes of both populations.This study indicates that both balancing selection and genetic drift may shape genetic variation and differentiation in small and fragmented populations.

Allelic Polymorphism,Gene Duplication and Balancing Selection of MHC Class ⅡB Genes in the Omei Treefrog(Rhacophorus omeimontis)

The worldwide declines in amphibian populations have largely been caused by infectious fungi and bacteria. Given that vertebrate immunity against these extracellular pathogens is primarily functioned by the major histocompatibility complex（MHC） class Ⅱ molecules, the characterization and the evolution of amphibian MHC class Ⅱ genes have attracted increasing attention. The polymorphism of MHC class Ⅱ genes was found to be correlated with susceptibility to fungal pathogens in many amphibian species, suggesting the importance of studies on MHC class Ⅱ genes for amphibians. However, such studies on MHC class Ⅱ gene evolution have rarely been conducted on amphibians in China. In this study, we chose Omei treefrog（Rhacophorus omeimontis）, which lived moist environments easy for breeding bacteria, to study the polymorphism of its MHC class Ⅱ genes and the underlying evolutionary mechanisms. We amplified the entire MHC class ⅡB exon 2 sequence in the R. omeimontis using newly designed primers. We detected 102 putative alleles in 146 individuals. The number of alleles per individual ranged from one to seven, indicating that there are at least four loci containing MHC class ⅡB genes in R. omeimontis. The allelic polymorphism estimated from the 102 alleles in R. omeimontis was not high compared to that estimated in other anuran species. No significant gene recombination was detected in the 102 MHC class ⅡB exon 2 sequences. In contrast, both gene duplication and balancing selection greatly contributed to the variability in MHC class ⅡB exon 2 sequences of R. omeimontis. This study lays the groundwork for the future researches to comprehensively analyze the evolution of amphibian MHC genes and to assess the role of MHC gene polymorphisms in resistance against extracellular pathogens for amphibians in China.

Balancing selection and wild gene pool contribute to resistance in global rice germplasm against planthopper

Interactions and co-evolution between plants and herbivorous insects are critically important in agriculture.Brown planthopper(BPH)is the most severe insect of rice,and the biotypes adapt to feed on different rice genotypes.Here,we present genomics analyses on 1,520 global rice germplasms for resistance to three BPH biotypes.Genome-wide association studies identified 3,502 single nucleotide polymorphisms(SNPs)and 59 loci associated with BPH resistance in rice.We cloned a previously unidentified gene Bph37 that confers resistance to BPH.The associated loci showed high nucleotide diversity.Genome-wide scans for trans-species polymorphisms revealed ancient balancing selection at the loci.The secondarily evolved insect biotypes II and III exhibited significantly higher virulence and overcame more rice varieties than the primary biotype I.In response,more SNPs and loci evolved in rice for resistance to biotypes II and III.Notably,three exceptional large regions with high SNP density and resistance-associated loci on chromosomes 4 and 6 appear distinct between the resistant and susceptible rice varieties.Surprisingly,these regions in resistant rice might have been retained from wild species Oryza nivara.Our findings expand the understanding of long-term interactions between rice and BPH and provide resistance genes and germplasm resources for breeding durable BPH-resistant rice varieties.

MHC Class I Exon 4 in the Multiocellated Racerunners(Eremias multiocellata): Polymorphism, Duplication and Selection

The major histocompatibility complex （MHC） is a dynamic genetic region with an essential role in the adaptive immunity of jawed vertebrates. The MHC polymorphism is affected by many processes such as birth-and- death evolution, gene conversion, and concerted evolution. Studies investigating the evolution of MHC class I genes have been biased toward a few particular taxa and model species. However, the investigation of this region in nonavian reptiles is still in its infancy. We present the first characterization of MHC class I genes in a species from the family Lacertidae. We assessed genetic diversity and a role of selection in shaping the diversity of MHC class I exon 4 among 37 individuals of Eremias multiocellata from a population in Lanzhou, China. We generated 67 distinct DNA sequences using cloning and sequencing methods, and identified 36 putative functional variants as well as two putative pseudogene-variants. We found the number of variants within an individual varying between two and seven, indicating that there are at least four MHC class I loci in this species. Gene duplication plays a role in increasing copy numbers of MHC genes and allelic diversity in this species. The class I exon 4 sequences are characteristic of low nucleotide diversity. No signal of recombination is detected, but purifying selection is detected in β2-microglobulin interaction sites and some other silent sites outside of the function-constraint regions. Certain identical alleles are shared by Eremias multiocellata and E. przewalskii and E. brenchleyi, suggesting trans-species polymorphism. The data are compatible with a birth-and-death model of evolution.

An atlas of CNV maps in cattle, goat and sheep

Copy number variation(CNV)is the most prevalent type of genetic structural variation that has been recognized as an important source of phenotypic variation in humans,animals and plants.However,the mechanisms underlying the evolution of CNVs and their function in natural or artificial selection remain unknown.Here,we generated CNV region(CNVR)datasets which were diverged or shared among cattle,goat,and sheep,including 886 individuals from 171 diverse populations.Using 9 environmental factors for genome-wide association study(GWAS),we identified a series of candidate CNVRs,including genes relating to immunity,tick resistance,multi-drug resistance,and muscle development.The number of CNVRs shared between species is significantly higher than expected(P<0.00001),and these CNVRs may be more persist than the single nucleotide polymorphisms(SNPs)shared between species.We also identified genomic regions under long-term balancing selection and uncovered the potential diversity of the selected CNVRs close to the important functional genes.This study provides the evidence that balancing selection might be more common in mammals than previously considered,and might play an important role in the daily activities of these ruminant species.

csd alleles in the red dwarf honey bee （Apis florea, Hymenoptera： Apidae） show exceptionally high nucleotide diversity

The single locus complementary sex determination （sl-csd） gene is the primary gene determining the gender of honey bees （Apis spp.）. While the csd gene has been well studied in the Western honey bee （Apis mellifera）, and comparable data exist in both the Eastern honey bee （Apis cerana） and the giant honey bee （Apis dorsata）, no studies have been conducted in the red dwarf honey bee, Apisflorea. In this study we cloned the genomic region 3 of the A. florea csd gene from 60 workers, and identified 12 csd alleles. Analysis showed that similar to A. mellifera, region 3 of the csd gene contains a RS domain at the N terminal, a proline-rich domain at the C terminal, and a hypervariable region in the middle. However, the A. florea csd gene possessed a much higher level of nucleotide diversity, compared to A. mellifera, A. cerana and Apis dorsata. We also show that similar to the other three Apis species, in A. florea, nonsynonymous mutations in the csd gene are selectively favored in young alleles.

Diversity of bacteria associated with Hormaphidinae aphids (Hemiptera: Aphididae)

Bacteria are ubiquitous inhabitants of animals.Hormaphidinae is a particular aphid group exhibiting very diverse life history traits.However,the microbiota in this group is poorly known.In the present study,using high-throughput sequencing of bacterial 16S ribosomal RNA gene amplicons,we surveyed the bacterial flora in hormaphidine aphids and explored whether the aphid tribe,host plant and geographical distribution are associated with the distribution of secondary symbionts.The most dominant bacteria detected in hormaphidine species are heritable symbionts.As expected,the primary endosymbiont Buchnera aphidicola is the most abundant symbiont across all species and has cospeciated with its host aphids.Six secondary symbionts were detected in Hormaphidinae.Arsenophonus is widespread in Hormaphidinae species,suggesting the possibility of ancient acquisition of this symbiont.Ordination analyses and statistical tests show that the symbiont composition does not seem to relate to any of the aphid tribes,host plants or geographical distributions,which indicate that horizontal transfers might occur for these symbionts in Hormaphidinae.Correlation analysis exhibits negative interference between Buchnera and coexisting secondary symbionts,while the interactions between different secondary symbionts are complicated.These findings display a comprehensive picture of the microbiota in Hormaphidinae and may be helpful in understanding the symbiont diversity within a group of aphids.