Sex-biased Transcriptomic Study Of Three Cryptic Species Of The Bemisia Tabaci Whitefly Complex Reveals Patterns Of Gene Evolution

The whitefly Bemisia tabaci has a cosmopolitan distribution,and is an important pest in cotton,tobacco and a wide range of vegetables and ornamental plants.Bemisia tabaci is a species complex with at least 35 morphologically indistinguishable but genetically divergent cryptic species.Among them,two cryptic species,MEAM 1 and MED,have exercised global invasion in recent years and have been displacing native whiteflies in many regions of invasion.Asia ?3 is one of the native whiteflies in China,which usually cause less harm than the invasive whiteflies.MEAM 1 can displace Asia ? 3 by asymmetric mating interactions and can obtain benefits from the interactions with begomoviruses via host plants.MED has developed high resistance to major classes of insecticides.In habitat where insecticide application is frequent,MED can displace MEAM 1.MEAM 1 and MED can efficiently transmit plant viruses.Whitefly is haplodiploidy,where males develop from unfertilized zygotes and females develop from fertilized zygotes.Females and males have obvious differences in morphology and behavior,however they share the identical set of chromosome:females have 2 sets and males have 1 set.This means that the differences between the two sexes are to a great extend the results of gene differential expression.Sex-biased genes contain the genes that only express in one sex(sex-specific expression),and the genes that express in two sexes,but in one sex the expression is significantly higher than the other(sex-enriched expression).Sex-biased genes trend to evolve fast in Drosophila,mammals and birds.Similar to protein sequence,gene expression has also evolved under natural selection,and the evolution of gene expression may have positive correlations with the evolution of protein sequences.The technology of RNA-seq enables researchers to retrieve gene coding sequences and expression levels cost-ffectively.Combining the evolutionary study of coding sequences and gene expression profile of orthologs in MEAM 1,MED and Asia ? 3 cryptic species,we want to discern the evolutionary patterns of sex-biased gene coding sequences and gene expression.The main results of this study are as follows:(1)By the analysis of evolution of coding sequences of orthologs in MEAM 1,MED and Asia? 3 cryptic species,we found 160 genes that are under positive selection between two or more species.These genes may be closely related to different characteristics across species and may be important to species differentiation.The distribution of positive evolution genes is not related with sex-bias.Genes showing faster evolutionary rates among the three species are enriched in genes related to digestion,metabolism,drug metabolism,interaction with hosts,nervous system and olfaction,which may relate to some invasive character in the two invasive whiteflies MEAM 1 and MED.(2)Combining the evolutionary analysis of gene coding sequences and gene expression profile,we found that male-biased expression genes in whiteflies,especially 2-8 times in male-bias,have evolved slower than female-biased and non-biased expression genes.The evolution pattern of coding sequence between two sexes differs from that of diplody animals with sex-chromosome.The pattern has somewhat similarity to the evolution patterns of queens and males of red fire ant which is social haplodiploidy.These characters may relate to the genetics of haplodiploidy.(3)By the analysis of gene expression in orthologous genes in MEAM 1,MED and Asia ? 3,we found that genes with non-bias expression between sexes have smaller expression variation within species than between species,which are under stronger positive selection.While sex-biased genes have large expression variations both within and between species,which may under weaker selection.The evolution pattern of expression may also relate to the genetics of haplodiploidy.Genes related to gene silencing and signaling pathway have larger expression variations between species than within species variations.Therefore,these genes are considered as fast evolving in gene expression,which may also relate to some invasive characteristics in these two invasive whiteflies.(4)A large-scale RNA-seq data were obtained by comparative transcriptomics and gene expression in the study.By using these data and some bioinformatics tools,we have developed a website for gene expression analysis,in which users can query for gene annotation and expression,and also can mine data with differential expression analysis across RNA-seq samples.In summary,this is the first study to investigate the evolution of sex-biased gene in non-social haplodiploidy insects,and elucidate the relations between evolution and sex-biased expression genes.By scanning the evolutionary rate of orthologous genes in two invasive species MEAM 1,MED and a native species Asia ? 3,we found some genes were potentially under positive selection,which provides important clues to study the differences of the genes among different whitefly species and also provides some candidate genes involved in speciation.By studying the evolution of gene expression in whiteflies,we found some patterns in non-social haplodiploidy insects.In addition,this study has developed a website for gene expression analysis in whiteflies,providing a platform for future studies on gene expression analysis.