Literature DB >> 30519425

Social environment affects the transcriptomic response to bacteria in ant queens.

Lumi Viljakainen1, Jaana Jurvansuu1, Ida Holmberg1, Tobias Pamminger2, Silvio Erler3, Sylvia Cremer4.   

Abstract

Social insects have evolved enormous capacities to collectively build nests and defend their colonies against both predators and pathogens. The latter is achieved by a combination of individual immune responses and sophisticated collective behavioral and organizational disease defenses, that is, social immunity. We investigated how the presence or absence of these social defense lines affects individual-level immunity in ant queens after bacterial infection. To this end, we injected queens of the ant Linepithema humile with a mix of gram+ and gram- bacteria or a control solution, reared them either with workers or alone and analyzed their gene expression patterns at 2, 4, 8, and 12 hr post-injection, using RNA-seq. This allowed us to test for the effect of bacterial infection, social context, as well as the interaction between the two over the course of infection and raising of an immune response. We found that social isolation per se affected queen gene expression for metabolism genes, but not for immune genes. When infected, queens reared with and without workers up-regulated similar numbers of innate immune genes revealing activation of Toll and Imd signaling pathways and melanization. Interestingly, however, they mostly regulated different genes along the pathways and showed a different pattern of overall gene up-regulation or down-regulation. Hence, we can conclude that the absence of workers does not compromise the onset of an individual immune response by the queens, but that the social environment impacts the route of the individual innate immune responses.

Entities:  

Keywords:  Hymenoptera; RNA‐seq; immunity; social insect; transcriptomics

Year:  2018        PMID： 30519425      PMCID： PMC6262927          DOI： 10.1002/ece3.4573

Source DB:  PubMed          Journal:  Ecol Evol        ISSN： 2045-7758            Impact factor:   2.912


INTRODUCTION

Social insects (ants, bees, wasps, and termites) are nearly ubiquitously distributed and ecologically very successful due to their advanced sociality including division of labor between castes and cooperation between individuals in a colony (Bourke & Franks, 1995). Importantly, they form colonies that show reproductive division of labor between the reproductive queen(s) and the sterile workerforce, which help the queen reproduce. Social insect societies are under particular threat of pathogens and disease, because individuals in the colony usually are closely related offspring of the mother queen(s) and because the high number of individuals facilitates pathogen transmission (Schmid‐Hempel, 1998). Each individual is protected against disease by its own hygiene behavior and physiological immune system. Yet, in order to keep infections at bay, additional colony‐level defenses have evolved that consist of collectively performed hygiene behaviors and organizational defenses, together forming the “social immunity” of the colony (Cremer, Armitage, & Schmid‐Hempel, 2007; Evans & Spivak, 2010). Social immunity is employed to protect contaminated colony members from developing infections and to inhibit disease transmission through the colony (Cremer, Pull, & Fürst, 2018). To this end, colonies of social insects perform intense nest hygiene, for example, by enriching their nest with antimicrobial material (Chapuisat, Oppliger, Magliano, & Christe, 2007; Christe, Oppliger, Bancalà, Castella, & Chapuisat, 2003; Simone, Evans, & Spivak, 2009), cleaning their nestmates from infectious particles by grooming and chemical disinfection (Hughes, Eilenberg, & Boomsma, 2002; Rosengaus, Maxmen, Coates, & Traniello, 1998; Theis, Ugelvig, Marr, & Cremer, 2015; Tragust, Mitteregger, et al., 2013), removing diseased brood from the nest (“hygienic behavior”; Rothenbuhler, 1964; Tragust, Ugelvig, Chapuisat, Heinze, & Cremer, 2013; Ugelvig, Kronauer, Schrempf, Heinze, & Cremer, 2010), and performing destructive disinfection to stop pathogen replication and to prevent disease transmission through the colony (Pull et al., 2018). Proximately, these social immunity behaviors occur in response to pathogen exposure, and it was shown that individual infection after bacterial injection in honeybees affects the behavior of their nestmates already 6 hr after injection so that the bacteria‐injected individuals are subject to increased allogrooming and aggression (Richard, Holt, & Grozinger, 2012). This suggests that nestmates can sense immune response, and in honeybees and ants, this has recently been shown to be mediated by cuticular hydrocarbons (Hernández López, Riessberger‐Gallé, Crailsheim, & Schuehly, 2017; Pull et al., 2018)—important cues for chemical communication in insects (Howard & Blomquist, 2005). Ultimately, all social immunity measures help to keep the colony free from disease, and to—in particular—prevent disease spread to the most valuable colony members, the reproductive queens (Cremer et al., 2018). It has been suggested that these social immune measures may interfere with the evolution as well as expression of individual immunity (Barribeau et al., 2015; Evanset al., 2006; Viljakainen et al., 2009), possibly reducing the need for individual immune responses. Most studies have focused on the analysis of the genome and immune components, where it was found that social insects have neither strongly reduced nor enlarged immune repertoires (Barribeau et al., 2015; Simola et al., 2013), and all major insect immune pathways being represented (Toll, Imd, JAK/STAT, JNK). Recent work has shown that social, colony‐level pathogen defenses affect the functionality of individual‐level immune responses. In ants and honeybees, exposure to resin, which has antibacterial properties and which these insects use as a nest building material, leads to decreased investment in physiological immune response (Borba, Klyczek, Mogen, & Spivak, 2015; Castella, Chapuisat, Moret, & Christe, 2008; Simone et al., 2009). The physiological immune defenses in insects comprise cellular and humoral responses, the former including phagocytosis of small microorganisms and encapsulation of larger parasites and the latter composed of several signaling pathways that culminate in the production of antimicrobial peptides and other effector molecules (Ferrandon, Imler, Hetru, & Hoffmann, 2007). The core genes encoding for these immune system components are retained across several insect orders (Viljakainen, 2015). Moreover, the immune responses are interconnected with stress responses, which in insects have an immune‐enhancing effect via stress hormones releasing energy for both stress and immune responses (Adamo, 2017). This interconnection may be particularly relevant for our study where we test the effect of worker presence or absence in the context of infection, as it is known that social isolation may induce stress and interfere with disease defense abilities in insects (Boulay, Quagebeur, Godzinska, & Lenoir, 1999; Kohlmeier, Holländer, & Meunier, 2016; Koto, Mersch, Hollis, & Keller, 2015). While previous work has focused mostly on worker–worker interactions, we here test how ant queens, the most important individuals of the colony, modulate their individual immune defenses after bacterial infection when they have access to social immunity or not (presence or absence of workers). We control for the fact of social isolation by also determining gene expression patterns of uninfected queens when alone or in the presence of their workers. We used queens of the Argentine ant Linepithema humile (Figure 1) that we injected with a combination of gram+ and gram− bacteria or sterile saline solution and then kept in either isolation or with workers. After injection, changes in gene expression patterns were analyzed at four time points using RNA‐seq: shortly after injection (2 hr), during the development of the immune response (4 and 8 hr post‐injection), and when the immune response was expected to be fully activated (12 hr post‐injection) (Erler, Popp, & Lattorff, 2011). We hypothesized that both the infection state and the social environment will affect gene expression of the queens and tested for an interaction between the two, in particular if the response to bacterial infection differed between the two rearing conditions.
Figure 1

Linepithema humile queen (on the left) and worker. Image © Alex Wild, used by permission

Linepithema humile queen (on the left) and worker. Image © Alex Wild, used by permission

MATERIAL AND METHODS

Samples

Workers and queens of the Argentine ant L. humile were collected from the European main supercolony in Castell d'Aro, Spain, in April 2011 and kept in artificial nests in climate chambers (Sanyo) set to 27°C for 14 hr of light and 21°C for 10 hr of dark. The ants were fed with honey and cockroaches three times per week. Approximately 3 weeks prior to the experiments, small sub‐colonies originating from two stock colonies and each consisting of a single queen and 10 workers were placed into petri dishes (diameter 9 cm) with a plastered ground and fed with 10% sugar water.

Bacteria used for infections

We used the gram‐positive bacterium Staphylococcus aureus and the gram‐negative bacterium Serratia marcescens in combination for infecting the queens with the aim to induce gene expression of both Toll and Imd innate immune signaling pathways, since in Drosophila, gram‐positive bacteria are known to induce mainly the Toll pathway and gram‐negative bacteria the Imd pathway (Ferrandon et al., 2007). The bacteria were grown overnight in LB medium (Merck). The bacterial suspension was centrifuged, and the pellet was washed three times in sterile saline solution (hereafter called Ringer) prepared following the protocol described in Aubert & Richard (2008). The pellet from the final wash was suspended in Ringer. For the injections, bacterial suspensions were diluted, bacterial cells counted using Neubauer counting chamber, and S. marcescens and S. aureus dilutions mixed to get a solution representing both bacterial species in equal quantity.

Injections and social environment

Linepithema humile queens were studied for effects on genomewide expression patterns at four time points (2, 4, 8, and 12 hr) after bacterial versus control injections in the presence or absence of five workers in a full factorial design. All the injections were made at the same time of day (in the morning) within a time window of 3 hr. Sample information is summarized in Table 1. The queens were randomly assigned for either bacterial or Ringer injection and were first transferred to small petri dishes on ice to cold‐immobilize them for injection. Microinjections were performed using Picoliter Injector PLI‐100 Plus (Harvard Apparatus) set at 10 psi for 1 s using spiked glass needles with inner diameter of 11.9 μm (Biomedical Instruments), resulting in an injection volume of about 65 nl. This volume was injected twice between the second and third tergite of the abdomen, containing approx. 1,300 bacterial cells (50:50 mix of S. marcescens and S. aureus). The controls were injected twice with 65 nl of sterile Ringer. After injection, the queens were transferred back to their original petri dish nests and kept together with five workers (social environment, the queens referred to as “social queens” hereafter) or reared alone by removing the workers (the queens referred to as “isolated queens” hereafter) at constant room temperature (22°C) and with 10% sugar water ad libitum. Each treatment at each time point was repeated three times.
Table 1

Sample information

Sample ID of biological replicates[Link] InjectionEnvironmentTime[Link]
B21, B37, B50 BacteriaS2
B5, B29, B45BacteriaS4
B9, B41, B53BacteriaS8
B1, B17, B33 BacteriaS12
B14, B22, B38BacteriaI2
B6,B30, B46BacteriaI4
B26, B42, B49BacteriaI8
B2, B18, B55BacteriaI12
C15, C39,C52RingerS2
C7, C47, C54 RingerS4
C11, C27, C43RingerS8
C3, C35, C51RingerS12
C16, C24, C40RingerI2
C8, C32, C48RingerI4
C12, C28, C57RingerI8
C4, C20, C56RingerI12

I: isolated; S: social.

Underlining indicates samples excluded from the analysis due to low mapping rate.

Post‐injection time point (hours) of sample collection.

Sample information I: isolated; S: social. Underlining indicates samples excluded from the analysis due to low mapping rate. Post‐injection time point (hours) of sample collection.

RNA extractions and sequencing

At 2, 4, 8, or 12 hr post‐injection (hpi), the ants were frozen in liquid nitrogen and kept in −80°C freezer until RNA extraction. The whole‐body samples were disrupted and homogenized in TissueLyser II (Qiagen) using stainless steel beads (5 mm diameter). Total RNA was extracted using RNeasy Micro Kit (Qiagen) following the protocol provided with the kit and including DNA removal using RNase‐free DNase I. RNA was quantified using Agilent 2100 Bioanalyzer, and the samples were sent to BGI Tech Solutions (Hong Kong) for library preparation (Illumina TruSeq RNA Sample Prep Kit) and mRNA sequencing (100 bp paired‐end reads) with Illumina HiSeq2000.

Bioinformatic analyses

The filtering of raw sequence data was performed by BGI and included adapter removal, removal of reads with more than 10% of undetermined bases, and removal of reads with more than 50% of low quality bases (Q < 10). Quality controlled clean data obtained from BGI were used for further analyses. The clean reads were mapped to the L. humile reference genome (GCF_000217595.1) using STAR v.2.4.1b (Dobin & Gingeras, 2015). The mapped reads were counted for all exons defined in the NCBI L. humile Annotation Release 100 (GCF_000217595.1_Lhum_UMD_V04_genomic.gff) and counts per exons were summarized for genes using HTSeq 0.9.1 (Anders, Pyl, & Huber, 2015). The count data of the samples were visualized by principal component analysis (PCA) in R version 3.4.1 (R Core Team, 2015). Analysis of differential gene expression in each contrast at each time point was carried out using DESeq2 version 1.16.1 (Love, Huber, & Anders, 2014) in R. In DESeq2, the count data for each gene in a sample are modeled with a negative binomial distribution where the mean and dispersion are estimated from the data. The mean is the read count of a gene normalized by a size factor based on the median of the ratios of observed counts (the read count of a gene in a given sample divided by the geometric mean of the read counts of that gene across all samples), thus allowing comparison of samples with variable sequencing depth. The dispersion estimate is obtained by first estimating dispersion for each gene using maximum likelihood, then fitting a curve to the maximum likelihood estimates (MLEs), and finally, shrinking the per gene dispersion estimates toward the expected dispersion values represented by the curve using empirical Bayes’ approach. Differential expression of a given gene between two conditions of interest is analyzed by using empirical Bayes shrinkage by fitting generalized linear model (GLM) to obtain MLEs for log2 fold change (LFC) between the conditions, then fitting normal distribution (µ = 0) to the MLEs of all genes, and repeating the GLM fit for the given gene using this distribution as a prior. The maximum of the a posteriori distribution is the final estimate of the LFC, and the curvature of the distribution at its maximum is the standard error of the LFC. The significance of the LFCs is tested by Wald test, and the obtained p values are corrected for multiple testing by the method of Benjamini and Hochberg (1995). In this study, we used a false discovery rate (FDR) <10%. Insects, including L. humile, are known to harbor RNA viruses (Gruber et al., 2017; Shi et al., 2016) which may have an effect on host gene expression (Doublet et al., 2017; Gerth & Hurst, 2017). We studied whether viruses are present and potentially have an effect on the gene expression patterns by assembling all the reads that could not be mapped to the L. humile genome by using default settings in Trinity v2.5.1, and by doing database searches with the obtained contigs against National Center for Biotechnology Information (NCBI Resource Coordinators, 2017) RefSeq virus databases “viral.1.protein.faa” and “viral.2.protein.faa” (accessed 7 January 2018) using BLASTX 2.6.0+ with an e‐value threshold of 10−4. Contigs that matched insect viruses and that had a query coverage of at least 400 amino acids were used in the following steps. The unmapped reads from each sample were mapped against the selected blast‐annotated virus contigs using default settings in BWA‐MEM v.0.7.17 (Li & Durbin, 2009), and the mapped reads were counted using samtools v1.4 (Li et al., 2009) and normalized with the sum of genome‐mapped and virus‐mapped reads per sample. The resulting viral load per sample was ordered by magnitude, divided into three equal sized bins, and classified as low (normalized read count range 4.27 × 10−5–4.45 × 10−4, n = 14), medium (normalized read count range 4.64 × 10−4–1.38 × 10−3, n = 16), or high (normalized read count range 2.16 × 10−3–0.18, n = 14). The virus load classification was incorporated as a factor in the analysis of differential gene expression. A list of manually annotated immune genes, hereafter called “the core immune genes”, of the L. humile genome including key genes for the main signaling pathways Toll, Imd, JAK‐STAT, and JNK and additionally, genes involved in pathogen recognition, modulation of immune response, melanization, RNA interference, and clearance of microbes (antimicrobial peptides and phagocytosis; Viljakainen, 2015), was retrieved from Smith et al. (2011), Table S16. Thirteen C‐type lectins, nine scavenger receptors, two Toll‐like proteins, and transferrin were added to the list, which now totaled 121 immune genes. These immune genes were searched against the list of differentially expressed genes (DEGs). Predicted function for all the other DEGs outside the core immune genes was searched using PaperBLAST (Price & Arkin, 2017) and NCBI databases (NCBI Resource Coordinators, 2017). A BED formatted file was parsed from the NCBI L. humile Annotation Release 100. The parsed BED file included the coding sequence (CDS) coordinates for genes, exon coordinates for non‐coding RNAs, and exon coordinates for some other genes without CDS annotation, excluding 210 pseudogenes and 46 tRNA genes, and merging overlapping CDS and exon regions. Based on the genomic coordinates in the BED file, the CDS or exon sequences were retrieved from the genome and concatenated for each gene in FASTA format. This resulted in total of 12,696 gene sequences. Gene Ontology (GO) annotation was carried out for the 12,696 genes using Blast2GO version 3.3.5 (Conesa et al., 2005). First, BLASTX search was done with an E‐value of 10−25 against all ant sequences in the NCBI non‐redundant database restricting the number of BLAST hits to 20. In addition, InterProScan annotation was run for the sequences (Jones et al., 2014). For the resulting hits, GO mapping and annotation were performed and InterProScan GOs were merged to annotation. The first step resulted in 9,406 sequences with GO annotations. Next, a second round of BLASTX search was done with the sequences that remained without hits in the first step with an E‐value of 10−25 against all arthropod sequences in the NCBI non‐redundant database restricting the number of BLAST hits to 100. Again, mapping and annotation were run for the resulting hits and InterProScan GOs were merged to the annotations. After the second step, 9,702 genes had GO annotations. GO term enrichment analysis was performed for all comparisons and time points to find significantly over‐ and under‐represented GO terms in the test set (DEGs, N > 10) with respect to the 9,702 genes with annotations as a reference set by using FatiGO package and a FDR <5% (Al‐Shahrour, Diaz‐Uriarte, & Dopazo, 2004) implemented in Blast2Go. Only the results with significant enrichment are presented in the Results.

RESULTS

In this study, 48 transcriptomes of L. humile queens were sequenced (Table 1). The mean number of clean reads per sample was 32 million of which on average 93% were mapped to the L. humile genome and 79% mapped to the 12,952 NCBI annotated genes including protein‐coding, non‐coding, and pseudogenes (Table 2). The genome‐mapping rate was markedly lower (about 65%) for four samples: B30, B33, B50, and C54 (Tables 1 and 2), which were excluded from further analyses. The removal affected the following data points: bacteria‐injected social queens at 2 and 12 hpi, bacteria‐injected isolated queens at 4 hpi, and Ringer‐injected social queens at 4 hpi, which all involved two instead of three biological replicates. In the PCA, the first PC explaining 37% of the variation in gene expression did not separate the samples according to the treatments, but the second PC explaining 9% of variance roughly separated the samples according to the type of injection (Figure 2).
Table 2

RNA‐sequencing statistics

SampleClean readsMapped reads[Link] Mapping rate (%)Reads mapped to genesGene mapping rate (%)
B124,597,75623,968,0269719,918,94281
B1426,624,41625,858,9469721,931,22082
B1723,999,19622,651,2789417,802,80874
B1823,322,16822,207,5769518,369,70679
B223,555,68622,880,5369719,149,84881
B2134,493,49233,386,0349728,086,62481
B2224,617,92623,694,5029619,953,83081
B2629,655,47028,194,8289524,070,26081
B2930,939,65429,544,1149524,867,17480
B3036,209,76624,433,2806720,189,92656
B3345,625,02828,638,8286323,836,07052
B3744,147,54043,202,8689836,453,03883
B3827,820,67224,703,2508921,374,22677
B4129,808,49827,583,4549323,167,50478
B4242,889,88441,943,0309835,365,47282
B4536,409,12235,492,6469729,598,51681
B4635,596,74634,842,9049829,326,36682
B4932,376,28431,729,9189827,374,74085
B523,006,50222,439,3869819,046,86883
B5027,917,92618,466,0446615,435,31255
B5340,673,65039,796,8469834,006,42084
B5535,647,64634,806,4669829,083,61482
B629,826,01623,599,5087919,401,85065
B923,367,01822,771,1629719,052,47882
C1127,657,99426,788,8689722,619,38082
C1226,274,85025,191,6329621,050,25480
C1526,534,29224,556,0929320,509,98477
C1622,399,50621,708,5689717,984,01880
C2026,934,68226,215,6089721,817,70081
C2429,162,75627,998,2989623,807,76682
C2722,016,85421,160,5629617,886,56081
C2820,395,71019,525,0389616,514,58881
C333,093,14832,073,2329726,728,79481
C3240,544,88637,664,9049332,121,40079
C3540,764,37639,594,3629733,079,89281
C3938,215,07837,412,8729830,819,54081
C426,290,79625,462,5249721,168,05681
C4028,242,68227,614,7809823,711,61684
C4335,737,58034,957,4889829,299,62082
C4744,515,82643,220,5129736,959,31283
C4834,970,55034,112,5309828,931,71883
C5132,295,29231,631,6589826,822,39483
C5239,323,20438,495,1809832,743,42483
C5444,103,73427,761,6126323,261,20053
C5639,100,62638,055,4269731,667,75481
C5731,438,69830,558,7389726,153,75683
C728,206,32827,338,5309723,073,00882
C821,029,55020,324,2529717,309,04682
Mean31,507,85529,297,0569324,643,82579

Both reads of the read pair properly mapped.

Figure 2

Scatterplot of the first and second principal components from principal component analysis of variance stabilized gene expression counts showing that the type of injection explains 9% of variance in gene expression

RNA‐sequencing statistics Both reads of the read pair properly mapped. Scatterplot of the first and second principal components from principal component analysis of variance stabilized gene expression counts showing that the type of injection explains 9% of variance in gene expression

Viral load of queens

Eight RNA viruses were identified in the Trinity‐assembled contigs of reads that could not be mapped to the L. humile genome (Viljakainen, Holmberg, Abril, & Jurvansuu, 2018). We found that all our samples contained RNA viruses at different loads. The type of injection (bacteria or Ringer) did not affect the virus loads per sample (two‐tailed t test: t = −1.36, df = 22.49, p = 0.19), neither did the rearing condition (two‐tailed t test: t = 0.05, df = 41.55, p = 0.95), suggesting an a priori viral load of the ants, which ranged from low to high levels. Importantly, we found that the gene expression profiles of the ants were affected by viral load (Figure 3), so that we controlled for viral load in the analysis of differential gene expression.
Figure 3

Differentially expressed genes induced by (a) isolation in Ringer‐injected control queens without viral load as a cofactor, (b) isolation in Ringer‐injected control queens and viral load taken into account as a cofactor, (c) bacterial injection in queens at social environment without viral load as a cofactor, (d) bacterial injection in queens at social environment and viral load taken into account as a cofactor, (e) bacterial injection in isolated queens without viral load as a cofactor, (f) bacterial injection in isolated queens and viral load taken into account as a cofactor

Differentially expressed genes induced by (a) isolation in Ringer‐injected control queens without viral load as a cofactor, (b) isolation in Ringer‐injected control queens and viral load taken into account as a cofactor, (c) bacterial injection in queens at social environment without viral load as a cofactor, (d) bacterial injection in queens at social environment and viral load taken into account as a cofactor, (e) bacterial injection in isolated queens without viral load as a cofactor, (f) bacterial injection in isolated queens and viral load taken into account as a cofactor

Effect of social context

We first investigated the effect of social isolation per se by analyzing differentially expressed genes in Ringer‐injected queens that were either reared alone or with their workers (Figure 3, Table 3, and Appendix: Table A1). The total number of DEGs across all time points was 134 with 82 up‐regulated and 52 down‐regulated genes. GO enrichment analysis showed enrichment of biological processes “single‐organism metabolic process,” “carbohydrate phosphorylation,” and “cellular glucose homeostasis” in the up‐regulated genes at 12 hpi (Appendix: Table A2). We hence found that social context affected queen energy metabolism, but had no effect on immune gene expression.
Table 3

Differentially expressed genes in all treatment contrasts and time points

ContrastHpiUpDownDEG total
BS versus CS27613
413662198
8353368
1211213
Total189103292
BI versus CI21895113
4164258
89514
126545110
Total108187295
BI versus BS2101
4077
8011
129211
Total101020
CI versus CS2314
4101
8262854
12522375
Total8252134

B: bacteria; C: control; Hpi: Hours post‐injection; I: isolated; S: social.

Table A1

Differentially expressed genes in Ringer‐injected isolated queens with false discovery rate <10%. T2, T4, T8, and T12 indicate the post‐injection time points

Time pointLocusDescriptionLFC p‐ValueAdjusted p‐value
T2LOC105680010Uncharacterized LOC105680010 (LOC105680010)7.625.41E−062.25E−02
LOC105671203Uncharacterized LOC105671203 (LOC105671203)4.289.72E−131.21E−08
LOC105675063Alkaline phosphatase 4‐like (LOC105675063)3.351.55E−079.66E−04
LOC105670077DNA repair protein RAD50‐like (LOC105670077)−20.671.56E−054.87E−02
T4LOC105668186Uncharacterized LOC105668186 (LOC105668186)7.473.34E−074.14E−03
T8LOC105668186Uncharacterized LOC105668186 (LOC105668186)8.894.74E−049.11E−02
LOC105670097Spidroin‐1 (LOC105670097)6.861.91E−061.34E−03
LOC105678335Gephyrin‐like (LOC105678335)2.947.95E−053.06E−02
LOC105677347Uncharacterized LOC105677347 (LOC105677347)2.342.36E−117.87E−08
LOC105677332Uncharacterized LOC105677332 (LOC105677332)2.171.20E−071.99E−04
LOC1056786721.822.49E−051.13E−02
LOC105671207A disintegrin and metalloproteinase with thrombospondin motifs 7‐like (LOC105671207)1.661.08E−044.00E−02
LOC105677333Uncharacterized LOC105677333 (LOC105677333)1.652.00E−061.34E−03
LOC105679161A disintegrin and metalloproteinase with thrombospondin motifs 17‐like (LOC105679161)1.612.17E−046.99E−02
LOC1056786641.572.57E−061.61E−03
LOC105674354Tyrosine aminotransferase (LOC105674354)1.473.40E−047.94E−02
LOC105667964THAP domain‐containing protein 4‐like (LOC105667964)1.275.27E−049.77E−02
LOC105677348Uncharacterized LOC105677348 (LOC105677348)1.179.58E−077.80E−04
LOC105673216Putative fatty acyl‐CoA reductase CG5065 (LOC105673216)1.153.47E−047.94E−02
LOC105679050Transcription termination factor 2‐like (LOC105679050)1.122.35E−051.12E−02
LOC105671872Vitellogenin‐2‐like (LOC105671872)0.981.88E−072.35E−04
LOC105675620Aminopeptidase N‐like (LOC105675620)0.964.00E−048.24E−02
LOC105670430Aminopeptidase N‐like (LOC105670430)0.903.45E−047.94E−02
LOC105667719Uncharacterized protein PFB0145c‐like (LOC105667719)0.871.13E−055.97E−03
LOC105668487Uncharacterized LOC105668487 (LOC105668487)0.852.60E−047.42E−02
LOC105678648Protein toll‐like (LOC105678648)0.842.11E−051.06E−02
LOC105672608Facilitated trehalose transporter Tret1‐like (LOC105672608)0.844.20E−048.24E−02
LOC105669158Sorbitol dehydrogenase‐like (LOC105669158)0.732.90E−047.60E−02
LOC105674664Cytochrome P450 6a2‐like (LOC105674664)0.712.59E−047.42E−02
LOC105670239Uncharacterized LOC105670239 (LOC105670239)0.672.52E−047.42E−02
LOC105671841Pleckstrin homology domain‐containing family M member 2 (LOC105671841)0.662.85E−047.60E−02
LOC105676405Fatty acid synthase (LOC105676405)−0.641.67E−045.58E−02
LOC105678111Uncharacterized LOC105678111 (LOC105678111)−0.641.41E−044.87E−02
LOC105675000Cartilage oligomeric matrix protein (LOC105675000)−0.662.23E−046.99E−02
LOC105676540Uncharacterized LOC105676540 (LOC105676540)−0.784.14E−048.24E−02
LOC105674426Beta‐1−0.793.03E−047.60E−02
LOC105675528Angiotensin‐converting enzyme (LOC105675528)−0.813.89E−048.24E−02
LOC105674352Aromatic‐l‐amino acid decarboxylase (LOC105674352)−0.954.96E−049.37E−02
LOC105677051Protein Malvolio (LOC105677051)−0.954.00E−048.24E−02
LOC105670059Probable serine/threonine‐protein kinase kinX (LOC105670059)−0.965.60E−052.44E−02
LOC105672810Protein yellow (LOC105672810)−1.027.95E−053.06E−02
LOC105678067Facilitated trehalose transporter Tret1‐like (LOC105678067)−1.057.31E−053.05E−02
LOC105677852Uncharacterized LOC105677852 (LOC105677852)−1.053.56E−062.10E−03
LOC105677615Alpha‐tocopherol transfer protein‐like (LOC105677615)−1.083.51E−047.94E−02
LOC105674532ETS homologous factor‐like (LOC105674532)−1.103.64E−089.11E−05
LOC105677500Glucosylceramidase‐like (LOC105677500)−1.152.75E−047.60E−02
LOC105671381Uncharacterized LOC105671381 (LOC105671381)−1.168.44E−064.69E−03
LOC105668572Uncharacterized LOC105668572 (LOC105668572)−1.182.42E−072.69E−04
LOC105673352Sodium‐coupled neutral amino acid transporter 9‐like (LOC105673352)−1.263.04E−047.60E−02
LOC105667677Zinc carboxypeptidase‐like (LOC105667677)−1.271.52E−072.17E−04
LOC1056761975‐aminolevulinate synthase−1.345.32E−081.06E−04
LOC105670776Endocuticle structural glycoprotein SgAbd‐4‐like (LOC105670776)−1.341.35E−044.82E−02
LOC105670441Uncharacterized LOC105670441 (LOC105670441)−1.437.43E−077.44E−04
LOC105670071Glucosylceramidase‐like (LOC105670071)−1.454.18E−048.24E−02
LOC105679194Muscle segmentation homeobox‐like (LOC105679194)−1.822.81E−121.40E−08
LOC105668025Transmembrane protease serine 9‐like (LOC105668025)−2.013.57E−047.94E−02
LOC105676839 l‐lactate dehydrogenase‐like (LOC105676839)−2.061.01E−067.80E−04
LOC105679457Uncharacterized LOC105679457 (LOC105679457)−6.729.72E−077.80E−04
LOC105670077DNA repair protein RAD50‐like (LOC105670077)−7.901.99E−121.40E−08
T12LOC105668565Uncharacterized LOC105668565 (LOC105668565)6.551.98E−043.56E−02
LOC105669318Kynurenine/alpha‐aminoadipate aminotransferase4.729.56E−052.29E−02
LOC105671889Synaptobrevin homolog YKT6‐like (LOC105671889)3.732.30E−057.35E−03
LOC1056728973.371.56E−143.29E−11
LOC105679180Solute carrier family 23.226.66E−151.75E−11
LOC105669922Uncharacterized LOC105669922 (LOC105669922)3.054.44E−073.60E−04
LOC105674428Uncharacterized LOC105674428 (LOC105674428)2.831.64E−122.19E−09
LOC105672083Cytochrome P450 4c21‐like (LOC105672083)2.711.01E−042.33E−02
LOC1056744242.544.95E−151.74E−11
LOC105670688Uncharacterized LOC105670688 (LOC105670688)2.531.17E−054.57E−03
LOC105678416Pancreatic lipase‐related protein 2‐like (LOC105678416)2.447.24E−074.77E−04
LOC105672219Leucine‐rich repeat‐containing protein 4‐like (LOC105672219)2.411.32E−042.67E−02
LOC105672698Uncharacterized LOC105672698 (LOC105672698)2.366.73E−063.08E−03
LOC1056673102.345.18E−073.81E−04
LOC105674425Uncharacterized LOC105674425 (LOC105674425)2.281.81E−043.35E−02
LOC105668386Trifunctional purine biosynthetic protein adenosine‐3 (LOC105668386)2.249.29E−052.27E−02
LOC105671469 d‐arabinitol dehydrogenase 1‐like (LOC105671469)2.221.99E−043.56E−02
LOC105673823Glucose dehydrogenase [FAD2.164.39E−062.31E−03
LOC105668392Succinate dehydrogenase [ubiquinone] iron‐sulfur subunit2.161.30E−042.67E−02
LOC105669349Uncharacterized LOC105669349 (LOC105669349)2.151.24E−042.60E−02
LOC105669805Facilitated trehalose transporter Tret1‐2 homolog (LOC105669805)2.085.43E−048.40E−02
LOC105667792Synaptotagmin‐6 (LOC105667792)2.001.08E−042.33E−02
LOC105676997Patatin‐like phospholipase domain‐containing protein 3 (LOC105676997)1.973.37E−093.22E−06
LOC105667804Uncharacterized family 31 glucosidase KIAA1161 (LOC105667804)1.925.44E−073.81E−04
LOC1056744203'(2')1.892.22E−057.30E−03
LOC105670888Hexokinase type 2‐like (LOC105670888)1.882.23E−102.61E−07
LOC105678328T‐lymphocyte activation antigen CD86‐like (LOC105678328)1.856.15E−051.59E−02
LOC105674418Beta‐11.788.76E−075.43E−04
LOC105668703Membrane metalloendopeptidase‐like 1 (LOC105668703)1.711.61E−055.70E−03
LOC105668747C‐1‐tetrahydrofolate synthase1.702.05E−043.59E−02
LOC105674681Cytochrome P450 6j1‐like (LOC105674681)1.631.68E−043.21E−02
LOC105677243Uncharacterized LOC105677243 (LOC105677243)1.531.67E−043.21E−02
LOC105676329Insulin‐like growth factor‐binding protein complex acid labile subunit (LOC105676329)1.535.78E−062.77E−03
LOC105674747Cytosolic purine 5'‐nucleotidase (LOC105674747)1.512.64E−061.46E−03
LOC105680118Cysteine proteinase 1‐like (LOC105680118)1.495.94E−048.74E−02
LOC105675420Protein yellow‐like (LOC105675420)1.485.08E−051.37E−02
LOC1056691996‐phosphofructo‐2‐kinase/fructose‐21.431.35E−055.09E−03
LOC105674352Aromatic‐l‐amino acid decarboxylase (LOC105674352)1.371.03E−054.32E−03
LOC105667680Probable hydroxyacid‐oxoacid transhydrogenase1.371.59E−043.16E−02
LOC105675723Serine protease snake‐like (LOC105675723)1.361.62E−055.70E−03
LOC105668704Organic cation transporter protein (LOC105668704)1.364.04E−051.15E−02
LOC105674248Branched‐chain‐amino acid aminotransferase1.352.78E−058.59E−03
LOC105680007Protein toll (LOC105680007)1.352.01E−061.18E−03
LOC105668437CCAAT/enhancer‐binding protein (LOC105668437)1.331.81E−043.35E−02
LOC105675016Peroxidase‐like (LOC105675016)1.277.08E−049.94E−02
LOC105677240General odorant‐binding protein 56d‐like (LOC105677240)1.181.06E−042.33E−02
LOC105677283Alpha‐aminoadipic semialdehyde synthase1.144.72E−047.52E−02
LOC105671238Exosome component 10 (LOC105671238)1.146.13E−048.85E−02
LOC105675407Inhibin beta E chain (LOC105675407)1.103.55E−045.92E−02
LOC105667297Protein LTV1 homolog (LOC105667297)1.084.42E−047.27E−02
LOC105671942Hexokinase‐2‐like (LOC105671942)1.088.18E−052.05E−02
LOC105677187Serine protease easter‐like (LOC105677187)1.051.09E−042.33E−02
LOC105677615Alpha‐tocopherol transfer protein‐like (LOC105677615)−1.383.07E−059.22E−03
LOC105675717Defensing‐2 (LOC105675717)−1.394.68E−047.52E−02
LOC105679818Cytosolic 10‐formyltetrahydrofolate dehydrogenase (LOC105679818)−1.475.42E−048.40E−02
LOC105672088Lipid storage droplets surface‐binding protein 2‐like (LOC105672088)−1.655.61E−048.55E−02
LOC105677041Cytochrome P450 4C1‐like (LOC105677041)−1.656.99E−049.94E−02
LOC105671746Probable cytochrome P450 304a1 (LOC105671746)−1.676.10E−085.35E−05
LOC105667919Protein crumbs‐like (LOC105667919)−1.725.98E−048.74E−02
LOC105677480Uncharacterized LOC105677480 (LOC105677480)−1.735.26E−062.64E−03
LOC1056681441‐acyl‐sn‐glycerol‐3‐phosphate acyltransferase alpha‐like (LOC105668144)−1.828.58E−063.76E−03
LOC105677809Uncharacterized LOC105677809 (LOC105677809)−1.861.81E−056.14E−03
LOC105674506Annulin (LOC105674506)−1.921.09E−054.43E−03
LOC105675090Uncharacterized LOC105675090 (LOC105675090)−1.944.21E−051.17E−02
LOC105679194Muscle segmentation homeobox‐like (LOC105679194)−1.983.61E−051.05E−02
LOC105679722Uncharacterized LOC105679722 (LOC105679722)−2.062.27E−043.92E−02
LOC105670118Uncharacterized methyltransferase‐like protein SPBC21C3.07c (LOC105670118)−2.075.80E−048.72E−02
LOC105667917Protein crumbs‐like (LOC105667917)−2.451.06E−042.33E−02
LOC105670857Leucine‐rich repeat‐containing protein egg‐6 (LOC105670857)−2.496.19E−051.59E−02
LOC105671854Uncharacterized LOC105671854 (LOC105671854)−3.693.19E−093.22E−06
LOC105672186Uncharacterized LOC105672186 (LOC105672186)−6.093.40E−045.78E−02
LOC105668152Uncharacterized LOC105668152 (LOC105668152)−6.681.66E−122.19E−09
LOC105675449Uncharacterized LOC105675449 (LOC105675449)−8.832.13E−133.74E−10
LOC105670525Chondroadherin‐like (LOC105670525)−9.318.47E−308.92E−26
LOC105668043Uncharacterized LOC105668043 (LOC105668043)−10.323.15E−181.66E−14
Table A2

Results of gene ontology enrichment analysis

GO_nameGO_CategoryFDR p‐Value
Enrichment of up‐regulated genes in bacteria‐injected queens in social environment at 4 hpi
Serine‐type endopeptidase inhibitor activityMOLECULAR_FUNCTION1.13E−332.00E−37
Endopeptidase inhibitor activityMOLECULAR_FUNCTION6.65E−333.51E−36
Endopeptidase regulator activityMOLECULAR_FUNCTION6.65E−333.51E−36
Peptidase inhibitor activityMOLECULAR_FUNCTION8.42E−327.41E−35
Peptidase regulator activityMOLECULAR_FUNCTION8.42E−327.41E−35
Enzyme inhibitor activityMOLECULAR_FUNCTION8.24E−308.70E−33
Enzyme regulator activityMOLECULAR_FUNCTION1.89E−202.33E−23
Molecular function regulatorMOLECULAR_FUNCTION4.10E−175.77E−20
Metallopeptidase activityMOLECULAR_FUNCTION1.07E−101.69E−13
Peptidase activity, acting on l‐amino acid peptidesMOLECULAR_FUNCTION1.80E−063.16E−09
Peptidase activityMOLECULAR_FUNCTION3.77E−067.30E−09
ProteolysisBIOLOGICAL_PROCESS1.21E−042.54E−07
Metalloendopeptidase activityMOLECULAR_FUNCTION0.00882.01E−05
Transition metal ion bindingMOLECULAR_FUNCTION0.04661.15E−04
Enrichment of down‐regulated genes in bacteria‐injected isolated queens at 2 hpi
Serine‐type endopeptidase inhibitor activityMOLECULAR_FUNCTION9.33E−241.64E−27
Endopeptidase inhibitor activityMOLECULAR_FUNCTION2.11E−231.12E−26
Endopeptidase regulator activityMOLECULAR_FUNCTION2.11E−231.12E−26
Peptidase inhibitor activityMOLECULAR_FUNCTION9.97E−238.77E−26
Peptidase regulator activityMOLECULAR_FUNCTION9.97E−238.77E−26
Enzyme inhibitor activityMOLECULAR_FUNCTION2.17E−212.29E−24
Enzyme regulator activityMOLECULAR_FUNCTION8.09E−159.96E−18
Metallopeptidase activityMOLECULAR_FUNCTION5.74E−138.08E−16
Molecular function regulatorMOLECULAR_FUNCTION1.73E−122.74E−15
Peptidase activity, acting on l‐amino acid peptidesMOLECULAR_FUNCTION2.26E−073.98E−10
Peptidase activityMOLECULAR_FUNCTION4.47E−078.65E−10
ProteolysisBIOLOGICAL_PROCESS2.95E−066.23E−09
Metalloendopeptidase activityMOLECULAR_FUNCTION3.96E−059.05E−08
Zinc ion bindingMOLECULAR_FUNCTION5.47E−041.35E−06
Hydrolase activityMOLECULAR_FUNCTION0.00164.33E−06
Transition metal ion bindingMOLECULAR_FUNCTION0.00328.95E−06
Molybdopterin cofactor metabolic processBIOLOGICAL_PROCESS0.04031.35E−04
Prosthetic group metabolic processBIOLOGICAL_PROCESS0.04031.35E−04
Molybdopterin cofactor biosynthetic processBIOLOGICAL_PROCESS0.04031.35E−04
Endopeptidase activityMOLECULAR_FUNCTION0.04791.77E−04
Exopeptidase activityMOLECULAR_FUNCTION0.04791.77E−04
Enrichment of down‐regulated genes in bacteria‐injected isolated queens at 12 hpi
Oxidoreductase activityMOLECULAR_FUNCTION0.02167.60E−06
Oxidation‐reduction processBIOLOGICAL_PROCESS0.02167.49E−06
Enrichment of up‐regulated genes in Ringer‐injected isolated queens at 12 hpi
Single‐organism metabolic processBIOLOGICAL_PROCESS0.00244.28E−07
Carbohydrate kinase activityMOLECULAR_FUNCTION0.01206.36E−06
Carbohydrate phosphorylationBIOLOGICAL_PROCESS0.01204.47E−06
Cellular glucose homeostasisBIOLOGICAL_PROCESS0.03104.37E−05
Glucose bindingMOLECULAR_FUNCTION0.03104.37E−05
Carbohydrate homeostasisBIOLOGICAL_PROCESS0.03104.37E−05
Hexokinase activityMOLECULAR_FUNCTION0.03104.37E−05
Glucose homeostasisBIOLOGICAL_PROCESS0.03104.37E−05
Differentially expressed genes in all treatment contrasts and time points B: bacteria; C: control; Hpi: Hours post‐injection; I: isolated; S: social.

Effect of bacterial infection depending on social context

We found that the effect of bacterial infection depended strongly on the social context the queens were reared at, even if the overall number of DEGs across all time points induced by the bacterial injection was similar across the social contexts, with 292 and 295 regulated genes in the presence and absence of workers, respectively (Figure 3, Table 3, Appendix: Tables A3 and A4). Some of the genes were regulated at several time points, and taking this into account, the number of unique DEGs was 272 in the socially reared and 268 in the isolated queens with 110 of the genes shared between the social contexts. Despite these similar numbers, the direction of regulation differed greatly: In the presence of workers, queens typically showed gene up‐regulation as compared to their Ringer control (65% of DEGs up‐regulated, χ2 = 25.33, df = 1, p = 4.83 × 10−7), whereas queens reared alone showed mostly down‐regulation (63% of DEGs down‐regulated; χ2 = 21.16, df = 1, p = 4.23 × 10−6), and only 22 of the up‐regulated genes and 27 of the down‐regulated genes were shared between the social treatments. Contrary to this overall difference in up‐regulation versus down‐regulation, both social and isolated queens showed a consistent up‐regulation of core immune genes after bacterial injection (64% up‐regulated out of 14 regulated core immune genes in social queens and 65% out of 23 in isolated queens; Table 4).
Table A3

Differentially expressed genes in bacteria‐injected social queens with false discovery rate <10%. T2, T4, T8, and T12 indicate the post‐injection time points

Time pointLocusDescriptionLFC p‐ValueAdjusted p‐value
T2LOC105671203Uncharacterized LOC105671203 (LOC105671203)3.697.03E−133.11E−09
LOC105668751Uncharacterized LOC105668751 (LOC105668751) (Naickin‐2)3.063.29E−087.27E−05
LOC105670685Glycine‐rich RNA‐binding protein 1‐like (LOC105670685)2.451.41E−049.84E−02
LOC105677480Uncharacterized LOC105677480 (LOC105677480)2.291.74E−062.56E−03
LOC105677479Uncharacterized LOC105677479 (LOC105677479)2.241.45E−049.84E−02
LOC105675449Uncharacterized LOC105675449 (LOC105675449)1.793.19E−053.52E−02
LOC105676587Trypsin‐like (LOC105676587)1.739.33E−059.17E−02
LOC105674885Purine nucleoside phosphorylase‐like (LOC105674885)−1.991.41E−049.84E−02
LOC105678691Scavenger receptor class B member 1‐like (LOC105678691)−2.281.65E−052.08E−02
LOC105668207Chymotrypsin‐1‐like (LOC105668207)−4.019.23E−148.16E−10
LOC105677784Uncharacterized LOC105677784 (LOC105677784)−4.125.07E−101.49E−06
LOC105668184Uncharacterized LOC105668184 (LOC105668184)−22.701.35E−049.84E−02
LOC105670097Spidroin‐1 (LOC105670097)−26.147.82E−071.38E−03
T4LOC105670077DNA repair protein RAD50‐like (LOC105670077)9.962.39E−064.18E−04
LOC105670097Spidroin‐1 (LOC105670097)9.006.39E−393.58E−35
LOC105679457Uncharacterized LOC105679457 (LOC105679457)8.371.61E−041.54E−02
LOC105679565A disintegrin and metalloproteinase with thrombospondin motifs 4‐like (LOC105679565)7.511.67E−039.52E−02
LOC105679203Cytochrome P450 4g15‐like (LOC105679203)7.216.19E−114.34E−08
LOC105671203Uncharacterized LOC105671203 (LOC105671203)6.801.90E−722.13E−68
LOC105677347Uncharacterized LOC105677347 (LOC105677347)6.212.74E−053.41E−03
LOC105668553A disintegrin and metalloproteinase with thrombospondin motifs 2‐like (LOC105668553)5.687.90E−045.11E−02
LOC105677333Uncharacterized LOC105677333 (LOC105677333)5.435.89E−071.32E−04
LOC105676228Glutamyl aminopeptidase‐like (LOC105676228)5.373.28E−053.89E−03
LOC105677348Uncharacterized LOC105677348 (LOC105677348)5.281.98E−183.70E−15
LOC105677332Uncharacterized LOC105677332 (LOC105677332)5.237.15E−126.16E−09
LOC105671207A disintegrin and metalloproteinase with thrombospondin motifs 7‐like (LOC105671207)5.206.21E−056.82E−03
LOC105670873Uncharacterized LOC105670873 (LOC105670873)4.972.43E−042.01E−02
LOC105674384Uncharacterized LOC105674384 (LOC105674384)4.952.04E−041.82E−02
LOC105676577Glutamyl aminopeptidase‐like (LOC105676577)4.812.18E−041.88E−02
LOC105674526Uncharacterized LOC105674526 (LOC105674526)4.805.82E−071.32E−04
LOC105676006Uncharacterized LOC105676006 (LOC105676006)4.629.75E−105.20E−07
LOC105678717Uncharacterized LOC105678717 (LOC105678717)4.601.09E−036.68E−02
LOC105676008Uncharacterized LOC105676008 (LOC105676008)4.472.62E−053.34E−03
LOC105670188Luciferin 4‐monooxygenase‐like (LOC105670188)4.373.59E−091.68E−06
LOC105671772Uncharacterized LOC105671772 (LOC105671772)4.285.57E−043.81E−02
LOC105674010Phosphotriesterase‐related protein‐like (LOC105674010)4.141.41E−041.37E−02
LOC105673254Thyrotropin‐releasing hormone‐degrading ectoenzyme‐like (LOC105673254)4.112.68E−042.19E−02
LOC105672921Zinc finger protein 468‐like (LOC105672921)4.101.10E−036.71E−02
LOC105672283Uncharacterized threonine‐rich GPI‐anchored glycoprotein PJ4664.02‐like (LOC105672283)4.046.91E−061.08E−03
LOC105679148Uncharacterized LOC105679148 (LOC105679148)3.986.36E−071.40E−04
LOC105678936Uncharacterized LOC105678936 (LOC105678936)3.921.05E−095.37E−07
LOC105671306A disintegrin and metalloproteinase with thrombospondin motifs 17‐like (LOC105671306)3.834.76E−043.37E−02
LOC105674631Uncharacterized LOC105674631 (LOC105674631)3.823.84E−042.89E−02
LOC105679175Uncharacterized LOC105679175 (LOC105679175)3.734.82E−067.60E−04
LOC105671771Uncharacterized LOC105671771 (LOC105671771)3.575.05E−055.66E−03
LOC105679161A disintegrin and metalloproteinase with thrombospondin motifs 17‐like (LOC105679161)3.527.78E−045.08E−02
LOC105674893Uncharacterized LOC105674893 (LOC105674893)3.485.07E−043.55E−02
LOC105670869Uncharacterized LOC105670869 (LOC105670869)3.291.47E−109.16E−08
LOC105670598A disintegrin and metalloproteinase with thrombospondin motifs 12‐like (LOC105670598)3.282.82E−042.26E−02
LOC105673458Thyrotropin‐releasing hormone‐degrading ectoenzyme‐like (LOC105673458)3.182.90E−064.84E−04
LOC105668847Uncharacterized LOC105668847 (LOC105668847)3.141.58E−039.20E−02
LOC105674525Uncharacterized LOC105674525 (LOC105674525)3.123.41E−065.62E−04
LOC105679050Transcription termination factor 2‐like (LOC105679050)3.109.41E−093.63E−06
LOC105668490Uncharacterized LOC105668490 (LOC105668490)2.859.94E−051.03E−02
LOC105670243Uncharacterized LOC105670243 (LOC105670243)2.812.94E−077.38E−05
LOC105678344Gephyrin‐like (LOC105678344)2.773.07E−053.70E−03
LOC105674779Fatty acid synthase‐like (LOC105674779)2.721.61E−142.00E−11
LOC105671607Uncharacterized LOC105671607 (LOC105671607)2.691.24E−037.41E−02
LOC105675620Aminopeptidase N‐like (LOC105675620)2.641.15E−073.22E−05
LOC105672800Uncharacterized LOC105672800 (LOC105672800)2.643.30E−053.89E−03
LOC105678986Uncharacterized LOC105678986 (LOC105678986)2.645.65E−081.71E−05
LOC105674397Uncharacterized LOC105674397 (LOC105674397)2.604.40E−081.37E−05
LOC105670868Uncharacterized LOC105670868 (LOC105670868)2.562.31E−088.08E−06
LOC105669605A disintegrin and metalloproteinase with thrombospondin motifs 20‐like (LOC105669605)2.511.21E−037.34E−02
LOC105670022Chymotrypsin‐2‐like (LOC105670022)2.473.77E−123.84E−09
LOC105679174Uncharacterized LOC105679174 (LOC105679174)2.412.83E−042.26E−02
LOC105670219Uncharacterized LOC105670219 (LOC105670219)2.384.34E−043.10E−02
LOC105674484RCC1 and BTB domain‐containing protein 1‐like (LOC105674484)2.353.58E−042.78E−02
LOC105670871Uncharacterized LOC105670871 (LOC105670871)2.343.47E−054.04E−03
LOC105670872Uncharacterized LOC105670872 (LOC105670872)2.311.42E−062.65E−04
LOC105668795Flavin‐containing monooxygenase FMO GS‐OX‐like 3 (LOC105668795)2.307.32E−093.04E−06
LOC105667907Thyroid receptor‐interacting protein 11‐like (LOC105667907)2.296.90E−071.43E−04
LOC105668248Uncharacterized LOC105668248 (LOC105668248)2.281.80E−052.41E−03
LOC105670430Aminopeptidase N‐like (LOC105670430)2.272.06E−052.68E−03
LOC105673464Venom carboxylesterase‐6‐like (pseudo)2.274.42E−081.37E−05
LOC105678987Uncharacterized LOC105678987 (LOC105678987)2.242.97E−077.38E−05
LOC105670899Uncharacterized LOC105670899 (LOC105670899)2.236.89E−071.43E−04
LOC105679177Uncharacterized LOC105679177 (LOC105679177)2.212.08E−041.83E−02
LOC105674677Uncharacterized LOC105674677 (LOC105674677)2.201.81E−074.83E−05
LOC105674740Zinc carboxypeptidase‐like (LOC105674740)2.167.34E−061.11E−03
LOC105674403Uncharacterized LOC105674403 (LOC105674403)2.131.16E−037.09E−02
LOC105671625Uncharacterized LOC105671625 (LOC105671625)2.101.12E−041.12E−02
LOC105678984Uncharacterized LOC105678984 (LOC105678984)2.088.18E−071.64E−04
LOC105676005Uncharacterized LOC105676005 (LOC105676005)1.992.92E−042.31E−02
LOC105668487Uncharacterized LOC105668487 (LOC105668487)1.972.73E−053.41E−03
LOC105674716Zinc carboxypeptidase A 1‐like (LOC105674716)1.921.45E−052.03E−03
LOC105672402Fatty acid synthase‐like (LOC105672402)1.917.20E−061.11E−03
LOC105674892Uncharacterized LOC105674892 (LOC105674892)1.913.83E−042.89E−02
LOC105670241Uncharacterized LOC105670241 (LOC105670241)1.907.66E−061.13E−03
LOC105676597Uncharacterized LOC105676597 (LOC105676597)1.871.43E−085.17E−06
LOC105678934Uncharacterized LOC105678934 (LOC105678934)1.862.95E−053.59E−03
LOC105671177 l‐xylulose reductase‐like (LOC105671177)1.851.63E−041.55E−02
LOC105671446A disintegrin and metalloproteinase with thrombospondin motifs 7‐like (LOC105671446)1.855.42E−043.75E−02
LOC105670897Uncharacterized LOC105670897 (LOC105670897)1.859.23E−082.72E−05
LOC105674728Muscle M‐line assembly protein unc‐89‐like (LOC105674728)1.844.24E−043.08E−02
LOC105678217Uncharacterized LOC105678217 (LOC105678217)1.841.42E−073.88E−05
LOC105668988Uncharacterized LOC105668988 (LOC105668988)1.835.66E−103.17E−07
LOC105679014Uncharacterized LOC105679014 (LOC105679014)1.831.73E−041.60E−02
LOC105671241Aminopeptidase N‐like (LOC105671241)1.834.86E−055.50E−03
LOC105670900Uncharacterized LOC105670900 (LOC105670900)1.821.23E−041.22E−02
LOC105678353Aminopeptidase N‐like (LOC105678353)1.818.06E−045.19E−02
LOC105676303N‐(5‐amino‐5‐carboxypentanoyl)‐l‐cysteinyl‐d‐valine synthase (LOC105676303)1.816.33E−092.73E−06
LOC105670239Uncharacterized LOC105670239 (LOC105670239)1.792.90E−064.84E−04
LOC105674406Uncharacterized LOC105674406 (LOC105674406)1.782.50E−042.06E−02
LOC105678342Gephyrin‐like (LOC105678342)1.771.53E−052.12E−03
LOC105679156Uncharacterized LOC105679156 (LOC105679156)1.761.78E−041.63E−02
LOC105668244Uncharacterized LOC105668244 (LOC105668244)1.759.96E−071.92E−04
LOC105672123Uncharacterized LOC105672123 (LOC105672123)1.741.01E−036.24E−02
LOC105667677Zinc carboxypeptidase‐like (LOC105667677)1.722.13E−101.26E−07
LOC105676007Uncharacterized LOC105676007 (LOC105676007)1.705.98E−044.06E−02
LOC105678817Protein toll‐like (LOC105678817)1.691.02E−041.05E−02
LOC105670238Uncharacterized LOC105670238 (LOC105670238)1.677.51E−061.12E−03
LOC105677480Uncharacterized LOC105677480 (LOC105677480)1.669.46E−071.86E−04
LOC105677501Venom acid phosphatase Acph‐1‐like (LOC105677501)1.661.03E−041.05E−02
LOC105670214Tissue factor pathway inhibitor‐like (LOC105670214)1.608.25E−058.80E−03
LOC105673951Chymotrypsin‐1‐like (LOC105673951)1.596.92E−071.43E−04
LOC105668779Troponin C1.558.95E−061.30E−03
LOC105675453Serine racemase‐like (LOC105675453)1.556.50E−044.39E−02
LOC105676003Uncharacterized LOC105676003 (LOC105676003)1.531.96E−041.78E−02
LOC105676004Uncharacterized LOC105676004 (LOC105676004)1.528.36E−045.32E−02
LOC105676346Uncharacterized LOC105676346 (LOC105676346)1.522.24E−063.99E−04
LOC105678648Protein toll‐like (LOC105678648)1.505.55E−043.81E−02
LOC10566736846 kDa FK506‐binding nuclear protein‐like (LOC105667368)1.494.87E−043.43E−02
LOC105667585Laccase‐1‐like (LOC105667585)1.489.34E−059.87E−03
LOC105670240Uncharacterized LOC105670240 (LOC105670240)1.471.27E−041.25E−02
LOC105668195Uncharacterized LOC105668195 (LOC105668195)1.453.80E−078.88E−05
LOC105671544Isthmin‐like (LOC105671544)1.442.33E−041.95E−02
LOC105679722Uncharacterized LOC105679722 (LOC105679722)1.432.16E−041.88E−02
LOC105670898Uncharacterized LOC105670898 (LOC105670898)1.432.15E−041.88E−02
LOC105674374Uncharacterized LOC105674374 (LOC105674374)1.424.32E−043.10E−02
LOC105675133Mitochondrial uncoupling protein 2‐like (LOC105675133)1.422.67E−076.96E−05
LOC105672982Chromosome‐associated kinesin KIF4 (LOC105672982)1.397.11E−057.73E−03
LOC105677706Bipolar kinesin KRP‐130‐like (LOC105677706)1.376.99E−044.69E−02
LOC105677471Facilitated trehalose transporter Tret1‐like (LOC105677471)1.333.92E−054.53E−03
LOC105670134Uncharacterized LOC105670134 (LOC105670134)1.321.59E−039.20E−02
LOC105677684E3 ubiquitin‐protein ligase TRIM71 (LOC105677684)1.281.59E−052.17E−03
LOC105672089Lipid storage droplets surface‐binding protein 2‐like (LOC105672089)1.282.24E−063.99E−04
LOC105671386Organic cation transporter 1‐like (LOC105671386)1.259.68E−046.03E−02
LOC105675373Cyclin‐dependent kinase 4 (LOC105675373)1.242.52E−053.25E−03
LOC105669176Organic cation transporter protein‐like (LOC105669176)1.221.69E−041.59E−02
LOC105671746Probable cytochrome P450 304a1 (LOC105671746)1.222.24E−041.90E−02
LOC105671768Uncharacterized LOC105671768 (LOC105671768)1.155.39E−043.75E−02
LOC105668043Uncharacterized LOC105668043 (LOC105668043)1.131.31E−037.71E−02
LOC1056681441‐acyl‐sn‐glycerol‐3‐phosphate acyltransferase alpha‐like (LOC105668144)1.097.80E−045.08E−02
LOC105675016Peroxidase‐like (LOC105675016)1.013.90E−042.91E−02
LOC105677622Uncharacterized LOC105677622 (LOC105677622)0.991.63E−039.34E−02
LOC105676083Baculoviral IAP repeat‐containing protein 7‐A‐like (LOC105676083)0.977.21E−044.81E−02
LOC105668364Mesencephalic astrocyte‐derived neurotrophic factor homolog (LOC105668364)0.911.74E−039.83E−02
LOC105668947Endoplasmin (LOC105668947)0.831.69E−039.60E−02
LOC105669096Spondin‐1 (LOC105669096)−0.901.22E−037.34E−02
LOC105668946Uncharacterized LOC105668946 (LOC105668946)−0.967.27E−044.82E−02
LOC105673575Venom metalloproteinase 3‐like (LOC105673575)−0.983.16E−042.47E−02
LOC105670254Glycine‐rich cell wall structural protein‐like (LOC105670254)−1.002.02E−041.81E−02
LOC105672527Venom allergen 3‐like (LOC105672527)−1.002.70E−042.19E−02
LOC105670714Alpha‐amylase A (LOC105670714)−1.013.79E−042.88E−02
LOC105672704Receptor‐type tyrosine‐protein phosphatase epsilon‐like (LOC105672704)−1.048.56E−045.42E−02
LOC105675546Uncharacterized LOC105675546 (LOC105675546)−1.058.23E−045.27E−02
LOC105676883Serine hydroxymethyltransferase−1.084.27E−043.08E−02
LOC105676184Troponin C−1.092.32E−041.95E−02
LOC105678432Acetyl‐CoA carboxylase (LOC105678432)−1.119.56E−046.02E−02
LOC105671942Hexokinase‐2‐like (LOC105671942)−1.129.69E−046.03E−02
LOC105672608Facilitated trehalose transporter Tret1‐like (LOC105672608)−1.147.47E−044.92E−02
LOC105678761Serine protease inhibitor 3/4‐like (LOC105678761)−1.174.04E−042.98E−02
LOC105675773Peptidoglycan‐recognition protein SC2‐like (LOC105675773)−1.209.78E−061.40E−03
LOC105669805Facilitated trehalose transporter Tret1‐2 homolog (LOC105669805)−1.224.34E−054.97E−03
LOC105674040Apolipophorins (LOC105674040)−1.234.34E−067.05E−04
LOC105679189Uncharacterized LOC105679189 (LOC105679189)−1.284.03E−042.98E−02
LOC105677003Aminopeptidase N‐like (LOC105677003)−1.281.09E−041.10E−02
LOC105668704Organic cation transporter protein (LOC105668704)−1.301.95E−052.57E−03
LOC105670974Uncharacterized LOC105670974 (LOC105670974)−1.301.87E−063.43E−04
LOC105674681Cytochrome P450 6j1‐like (LOC105674681)−1.311.57E−041.51E−02
LOC105677248Protein phosphatase 1 regulatory subunit 3C‐B (LOC105677248)−1.347.82E−058.42E−03
LOC105672092Uncharacterized LOC105672092 (LOC105672092)−1.359.67E−051.01E−02
LOC105675916Major royal jelly protein 5‐like (LOC105675916)−1.371.39E−062.63E−04
LOC105672956Ribose‐phosphate pyrophosphokinase 1 (LOC105672956)−1.393.22E−077.68E−05
LOC105676485Uncharacterized LOC105676485 (LOC105676485)−1.402.24E−041.90E−02
LOC105672335Uncharacterized LOC105672335 (LOC105672335)−1.413.70E−042.85E−02
LOC105667549Vascular endothelial growth factor receptor 1‐like (LOC105667549)−1.425.42E−056.01E−03
LOC105676142Vascular endothelial growth factor receptor kdr‐like (LOC105676142)−1.451.59E−039.20E−02
LOC105669099Vascular endothelial growth factor B‐like (LOC105669099)−1.454.09E−042.99E−02
LOC105674346Neural‐cadherin (LOC105674346)−1.493.92E−081.29E−05
LOC105671703Facilitated trehalose transporter Tret1‐like (LOC105671703)−1.521.39E−038.15E−02
LOC105672628Esterase FE4‐like (LOC105672628)−1.535.18E−092.32E−06
LOC105670266Sodium/potassium/calcium exchanger 3‐like (LOC105670266)−1.541.72E−041.60E−02
LOC105679180Solute carrier family 2−1.593.18E−077.68E−05
LOC105671469 d‐arabinitol dehydrogenase 1‐like (LOC105671469)−1.661.69E−098.22E−07
LOC105675436Chymotrypsin inhibitor‐like (LOC105675436)−1.691.42E−109.16E−08
LOC105669509Arylsulfatase B‐like (LOC105669509)−1.714.52E−067.23E−04
LOC105669158Sorbitol dehydrogenase‐like (LOC105669158)−1.718.01E−093.21E−06
LOC105675717Defensing‐2 (LOC105675717)−1.801.05E−083.93E−06
LOC105679484Sorbitol dehydrogenase‐like (LOC105679484)−1.803.71E−042.85E−02
LOC105679620Uncharacterized LOC105679620 (LOC105679620)−1.881.68E−052.26E−03
LOC105679945Cytochrome P450 4C1‐like (LOC105679945)−1.951.30E−037.71E−02
LOC105679847Probable phytanoyl‐CoA dioxygenase (LOC105679847)−2.032.39E−111.92E−08
LOC105667920Phosphoenolpyruvate carboxykinase [GTP]‐like (LOC105667920)−2.081.30E−051.84E−03
LOC105675714Uncharacterized LOC105675714 (LOC105675714)−2.102.85E−042.27E−02
LOC105672537Alpha‐glucosidase‐like (LOC105672537)−2.154.98E−156.98E−12
LOC105672219Leucine‐rich repeat‐containing protein 4‐like (LOC105672219)−2.173.72E−112.78E−08
LOC105680018Uncharacterized LOC105680018 (LOC105680018)−2.202.77E−064.78E−04
LOC105675643Prismalin‐14‐like (LOC105675643)−2.292.95E−053.59E−03
LOC105678258Facilitated trehalose transporter Tret1‐like (LOC105678258)−2.351.24E−037.41E−02
LOC105668871Phenoloxidase 2‐like (LOC105668871)−2.368.57E−171.37E−13
LOC105676062Protein henna (LOC105676062)−2.373.44E−081.17E−05
LOC105679763Uncharacterized oxidoreductase C26H5.09c‐like (LOC105679763)−2.404.11E−134.60E−10
LOC105671889Synaptobrevin homolog YKT6‐like (LOC105671889)−2.447.03E−071.43E−04
LOC105667386Hexamerin‐like (LOC105667386)−2.634.83E−124.51E−09
LOC105675433Dynein beta chain, ciliary (LOC105675433)−2.971.07E−073.08E−05
LOC105674885Purine nucleoside phosphorylase‐like (LOC105674885)−3.035.32E−231.19E−19
LOC105674055Uncharacterized protein DDB_G0290685‐like (LOC105674055)−3.041.43E−274.00E−24
LOC105674482Aldehyde dehydrogenase family 1 member A3 (LOC105674482)−3.259.19E−343.43E−30
LOC105676600Arylphorin subunit alpha‐like (LOC105676600)−3.511.97E−041.78E−02
T8LOC105668186Uncharacterized LOC105668186 (LOC105668186)8.254.34E−048.24E−02
LOC105670097Spidroin‐1 (LOC105670097)6.795.27E−073.32E−04
LOC105672689Uncharacterized LOC105672689 (LOC105672689)2.283.82E−093.81E−06
LOC105675162Uncharacterized LOC105675162 (LOC105675162)1.971.12E−111.67E−08
LOC105670021Chymotrypsin‐2‐like (LOC105670021)1.788.18E−052.33E−02
LOC105667585Laccase‐1‐like (LOC105667585)1.662.68E−125.00E−09
LOC105671850Protein‐S‐isoprenylcysteine O‐methyltransferase (LOC105671850)1.562.02E−057.47E−03
LOC105669469Cytochrome b5‐like (LOC105669469)1.445.07E−062.33E−03
LOC105671337Putative fatty acyl‐CoA reductase CG5065 (LOC105671337)1.392.23E−061.21E−03
LOC105672439Alpha‐sarcoglycan (LOC105672439)1.373.77E−051.29E−02
LOC105671866Serine protease gd‐like (LOC105671866)1.292.23E−071.48E−04
LOC1056738742‐oxoisovalerate dehydrogenase subunit beta1.263.26E−046.90E−02
LOC105673821Vascular endothelial growth factor A‐like (LOC105673821)1.264.54E−051.43E−02
LOC105669027Putative nuclease HARBI1 (pseudo)1.193.03E−046.71E−02
LOC105673881Beta‐1,3‐glucan‐binding protein‐like (LOC105673881)1.181.43E−055.70E−03
LOC105674055Uncharacterized protein DDB_G0290685‐like (LOC105674055)1.102.83E−103.76E−07
LOC105677650Speckle targeted PIP5K1A‐regulated poly(A) polymerase‐like (LOC105677650)1.102.68E−046.04E−02
LOC105675725Serine protease snake‐like (LOC105675725)1.041.68E−044.19E−02
LOC105667656Uncharacterized LOC105667656 (LOC105667656)1.012.12E−057.47E−03
LOC105676251Uncharacterized LOC105676251 (LOC105676251)0.992.00E−044.89E−02
LOC105680007Protein toll (LOC105680007)0.983.45E−047.12E−02
LOC105672359Thiamine transporter 2‐like (LOC105672359)0.973.29E−046.90E−02
LOC105673986G‐protein coupled receptor moody (LOC105673986)0.965.07E−049.06E−02
LOC105669664Uncharacterized LOC105669664 (LOC105669664)0.923.78E−047.67E−02
LOC105674673Putative histone‐lysine N‐methyltransferase 1 (LOC105674673)0.895.02E−049.06E−02
LOC105676303N‐(5‐amino‐5‐carboxypentanoyl)‐l‐cysteinyl‐d‐valine synthase (LOC105676303)0.862.17E−045.18E−02
LOC105673707Kinesin‐like protein unc‐104 (LOC105673707)0.841.10E−042.99E−02
LOC105669176Organic cation transporter protein‐like (LOC105669176)0.845.60E−062.48E−03
LOC105672117ATP‐binding cassette sub‐family G member 4 (LOC105672117)0.831.35E−055.56E−03
LOC105678395Uncharacterized LOC105678395 (LOC105678395)0.824.07E−048.09E−02
LOC105671203Uncharacterized LOC105671203 (LOC105671203)0.761.31E−043.40E−02
LOC105671406Putative phosphatidate phosphatase (LOC105671406)0.724.17E−048.09E−02
LOC105676136Guanine nucleotide‐binding protein G(i) subunit alpha (LOC105676136)0.691.99E−057.47E−03
LOC105671687Plastin‐2 (LOC105671687)0.665.64E−049.93E−02
LOC105673509Ankyrin repeat and BTB/POZ domain‐containing protein BTBD11 (LOC105673509)0.582.40E−045.63E−02
LOC105679739Uncharacterized LOC105679739 (LOC105679739)−0.592.11E−057.47E−03
LOC105678332Pancreatic triacylglycerol lipase‐like (LOC105678332)−0.637.11E−052.16E−02
LOC105677611Uncharacterized LOC105677611 (LOC105677611)−0.684.30E−051.39E−02
LOC105671942Hexokinase‐2‐like (LOC105671942)−0.714.58E−048.56E−02
LOC105669509Arylsulfatase B‐like (LOC105669509)−0.742.60E−045.98E−02
LOC105667685Solute carrier organic anion transporter family member 2A1 (LOC105667685)−0.743.18E−046.90E−02
LOC105678768Lipoyltransferase 1−0.811.31E−043.40E−02
LOC105674040Apolipophorins (LOC105674040)−0.857.22E−052.16E−02
LOC105676627Uncharacterized LOC105676627 (LOC105676627)−0.974.82E−048.87E−02
LOC105667549Vascular endothelial growth factor receptor 1‐like (LOC105667549)−1.004.19E−048.09E−02
LOC105674437Aquaporin‐like (LOC105674437)−1.018.98E−075.37E−04
LOC105672704Receptor‐type tyrosine‐protein phosphatase epsilon‐like (LOC105672704)−1.039.68E−052.69E−02
LOC105675201Glycine N‐methyltransferase (LOC105675201)−1.032.68E−082.29E−05
LOC105676399Netrin receptor UNC5C‐like (LOC105676399)−1.042.23E−071.48E−04
LOC105675916Major royal jelly protein 5‐like (LOC105675916)−1.088.13E−052.33E−02
LOC105672628Esterase FE4‐like (LOC105672628)−1.134.28E−083.42E−05
LOC105669186Uncharacterized LOC105669186 (LOC105669186)−1.144.00E−051.33E−02
LOC105676405Fatty acid synthase (LOC105676405)−1.182.45E−092.67E−06
LOC105678833Acyl‐CoA Delta(11) desaturase‐like (LOC105678833)−1.192.75E−125.00E−09
LOC105678901High affinity nerve growth factor receptor‐like (LOC105678901)−1.253.89E−061.94E−03
LOC105675090Uncharacterized LOC105675090 (LOC105675090)−1.274.99E−062.33E−03
LOC105677615Alpha‐tocopherol transfer protein‐like (LOC105677615)−1.422.93E−125.00E−09
LOC105671862Uncharacterized LOC105671862 (LOC105671862)−1.531.52E−043.88E−02
LOC105679194Muscle segmentation homeobox‐like (LOC105679194)−1.542.47E−061.29E−03
LOC105680137Tryptophan 2,3‐dioxygenase (LOC105680137)−1.678.66E−132.59E−09
LOC105676142Vascular endothelial growth factor receptor kdr‐like (LOC105676142)−1.692.22E−071.48E−04
LOC105680118Cysteine proteinase 1‐like (LOC105680118)−2.037.00E−062.99E−03
LOC105677462Peroxisomal hydratase‐dehydrogenase‐epimerase‐like (LOC105677462)−2.071.32E−401.58E−36
LOC105680018Uncharacterized LOC105680018 (LOC105680018)−2.091.08E−091.29E−06
LOC105675840Uncharacterized protein K02A2.6‐like (LOC105675840)−3.231.08E−134.29E−10
LOC105678364Uncharacterized LOC105678364 (LOC105678364)−3.291.39E−067.92E−04
LOC105669037Uncharacterized LOC105669037 (LOC105669037)−4.306.30E−143.77E−10
LOC105670525Chondroadherin‐like (LOC105670525)−5.151.14E−081.05E−05
T12LOC105669627Uncharacterized LOC105669627 (LOC105669627)10.409.22E−061.27E−02
LOC105667928Uncharacterized LOC105667928 (pseudo)5.403.43E−102.13E−06
LOC105669318Kynurenine/alpha‐aminoadipate aminotransferase2.961.84E−062.86E−03
LOC105673362Limulus clotting factor C‐like (LOC105673362)2.741.11E−073.45E−04
LOC105676242Uncharacterized LOC105676242 (LOC105676242)2.371.68E−074.16E−04
LOC105670707Uncharacterized transmembrane protein DDB_G0289901‐like (LOC105670707)2.292.50E−075.16E−04
LOC105676540Uncharacterized LOC105676540 (LOC105676540)2.168.06E−071.43E−03
LOC105670591Uncharacterized LOC105670591 (LOC105670591)2.097.28E−056.94E−02
LOC105677207Gamma‐glutamyl transpeptidase 1‐like (LOC105677207)2.045.11E−055.28E−02
LOC105677194Glucose dehydrogenase1.822.74E−053.09E−02
LOC105674352Aromatic‐l‐amino acid decarboxylase (LOC105674352)1.781.43E−051.77E−02
LOC105677462Peroxisomal hydratase‐dehydrogenase‐epimerase‐like (LOC105677462)−3.042.10E−142.61E−10
LOC105671854Uncharacterized LOC105671854 (LOC105671854)−3.305.52E−082.28E−04

LFC: log2 fold change.

Table A4

Differentially expressed genes in bacteria‐injected isolated queens with false discovery rate <10%. T2, T4, T8, and T12 indicate the post‐injection time points

Time pointLocusDescriptionLFC p‐ValueAdjusted p‐value
T2LOC105672684Protein hairy (LOC105672684)1.753.31E−061.93E−03
LOC105672434Uncharacterized LOC105672434 (LOC105672434)1.532.39E−115.13E−08
LOC105670707Uncharacterized transmembrane protein DDB_G0289901‐like (LOC105670707)1.482.33E−072.27E−04
LOC105675132Uncharacterized LOC105675132 (LOC105675132)1.453.35E−044.66E−02
LOC105673362Limulus clotting factor C‐like (LOC105673362)1.454.68E−074.18E−04
LOC105669805Facilitated trehalose transporter Tret1‐2 homolog (LOC105669805)1.201.75E−056.19E−03
LOC105679763Uncharacterized oxidoreductase C26H5.09c‐like (LOC105679763)1.189.17E−048.86E−02
LOC105676470MAP/microtubule affinity‐regulating kinase 3‐like (LOC105676470)1.109.12E−101.40E−06
LOC105676540Uncharacterized LOC105676540 (LOC105676540)1.061.79E−056.19E−03
LOC105676242Uncharacterized LOC105676242 (LOC105676242)0.969.84E−081.17E−04
LOC105668293Chymotrypsin‐1‐like (LOC105668293)0.947.93E−063.81E−03
LOC105672325Calcium‐binding mitochondrial carrier protein SCaMC‐2‐like (LOC105672325)0.906.63E−047.04E−02
LOC105671678Collagen alpha‐2(I) chain‐like (LOC105671678)0.895.94E−051.35E−02
LOC105679973Fatty acid binding protein 1‐B.1‐like (LOC105679973)0.821.46E−042.56E−02
LOC105677611Uncharacterized LOC105677611 (LOC105677611)0.761.73E−042.86E−02
LOC105672337Protein fem‐1 homolog B (LOC105672337)0.674.27E−045.51E−02
LOC105674292Nose resistant to fluoxetine protein 6‐like (LOC105674292)0.585.93E−046.77E−02
LOC105668729Nuclear factor NF‐kappa‐B p100 subunit (LOC105668729) (Relish)0.541.01E−039.71E−02
LOC105677684E3 ubiquitin‐protein ligase TRIM71 (LOC105677684)−0.721.01E−042.03E−02
LOC105678648Protein toll‐like (LOC105678648)−0.723.01E−044.30E−02
LOC105667719Uncharacterized protein PFB0145c‐like (LOC105667719)−0.812.73E−044.01E−02
LOC105671848Putative exonuclease GOR (LOC105671848)−0.821.11E−042.12E−02
LOC105674378Uncharacterized LOC105674378 (LOC105674378)−0.826.36E−046.89E−02
LOC105676004Uncharacterized LOC105676004 (LOC105676004)−0.826.60E−047.04E−02
LOC105671329Insulin‐degrading enzyme‐like (LOC105671329)−0.837.00E−047.13E−02
LOC105672982Chromosome‐associated kinesin KIF4 (LOC105672982)−0.843.02E−058.75E−03
LOC105670214Tissue factor pathway inhibitor‐like (LOC105670214)−0.879.09E−048.86E−02
LOC105673464Venom carboxylesterase‐6‐like (pseudo)−0.886.57E−051.47E−02
LOC10566736846 kDa FK506‐binding nuclear protein‐like (LOC105667368)−0.885.38E−046.26E−02
LOC105667677Zinc carboxypeptidase‐like (LOC105667677)−0.886.17E−046.82E−02
LOC105670134Uncharacterized LOC105670134 (LOC105670134)−0.885.08E−046.19E−02
LOC105670241Uncharacterized LOC105670241 (LOC105670241)−0.893.70E−059.80E−03
LOC105670430Aminopeptidase N‐like (LOC105670430)−0.915.43E−051.27E−02
LOC105668482Espin (LOC105668482)−0.924.39E−045.60E−02
LOC105670871Uncharacterized LOC105670871 (LOC105670871)−0.926.72E−047.06E−02
LOC105677706Bipolar kinesin KRP‐130‐like (LOC105677706)−0.924.01E−045.24E−02
LOC105678817Protein toll‐like (LOC105678817)−0.944.06E−051.04E−02
LOC105674728Muscle M‐line assembly protein unc‐89‐like (LOC105674728)−0.941.14E−068.71E−04
LOC105678912Protein toll‐like (LOC105678912)−0.948.07E−048.09E−02
LOC105670239Uncharacterized LOC105670239 (LOC105670239)−0.984.27E−051.05E−02
LOC105678342Gephyrin‐like (LOC105678342)−0.993.59E−044.87E−02
LOC105678985Uncharacterized LOC105678985 (LOC105678985)−1.001.95E−056.35E−03
LOC105670219Uncharacterized LOC105670219 (LOC105670219)−1.007.05E−047.13E−02
LOC105674716Zinc carboxypeptidase A 1‐like (LOC105674716)−1.019.03E−051.90E−02
LOC105670899Uncharacterized LOC105670899 (LOC105670899)−1.013.63E−059.80E−03
LOC105678986Uncharacterized LOC105678986 (LOC105678986)−1.013.51E−044.83E−02
LOC105678984Uncharacterized LOC105678984 (LOC105678984)−1.026.48E−063.31E−03
LOC105667907Thyroid receptor‐interacting protein 11‐like (LOC105667907)−1.021.05E−039.99E−02
LOC105669733Venom carboxylesterase‐6‐like (LOC105669733)−1.021.16E−042.14E−02
LOC105678217Uncharacterized LOC105678217 (LOC105678217)−1.025.44E−051.27E−02
LOC105671625Uncharacterized LOC105671625 (LOC105671625)−1.063.10E−058.75E−03
LOC105676578Thyrotropin‐releasing hormone‐degrading ectoenzyme‐like (LOC105676578)−1.065.30E−046.25E−02
LOC105678934Uncharacterized LOC105678934 (LOC105678934)−1.065.13E−046.19E−02
LOC105678987Uncharacterized LOC105678987 (LOC105678987)−1.072.68E−043.99E−02
LOC105675620Aminopeptidase N‐like (LOC105675620)−1.072.58E−043.96E−02
LOC105674397Uncharacterized LOC105674397 (LOC105674397)−1.082.38E−057.32E−03
LOC105670244Uncharacterized LOC105670244 (LOC105670244)−1.102.22E−043.56E−02
LOC105670868Uncharacterized LOC105670868 (LOC105670868)−1.123.42E−061.93E−03
LOC105674484RCC1 and BTB domain‐containing protein 1‐like (LOC105674484)−1.142.31E−043.59E−02
LOC105676597Uncharacterized LOC105676597 (LOC105676597)−1.151.00E−042.03E−02
LOC105674665T‐box transcription factor TBX20‐like (LOC105674665)−1.176.35E−046.89E−02
LOC105674406Uncharacterized LOC105674406 (LOC105674406)−1.172.39E−057.32E−03
LOC105679050Transcription termination factor 2‐like (LOC105679050)−1.192.05E−072.20E−04
LOC105674677Uncharacterized LOC105674677 (LOC105674677)−1.201.10E−068.71E−04
LOC105679162Uncharacterized LOC105679162 (LOC105679162)−1.211.39E−042.48E−02
LOC105672421Uncharacterized LOC105672421 (LOC105672421)−1.221.02E−042.03E−02
LOC105679916Kinesin‐like protein KIF12 (LOC105679916)−1.248.97E−064.01E−03
LOC105675300Aminopeptidase N‐like (LOC105675300)−1.255.16E−046.19E−02
LOC105672131Uncharacterized LOC105672131 (LOC105672131)−1.268.11E−051.74E−02
LOC105678936Uncharacterized LOC105678936 (LOC105678936)−1.262.99E−044.30E−02
LOC105670915Probable salivary secreted peptide (LOC105670915)−1.297.81E−111.40E−07
LOC105676006Uncharacterized LOC105676006 (LOC105676006)−1.301.23E−055.08E−03
LOC105668490Uncharacterized LOC105668490 (LOC105668490)−1.336.14E−046.82E−02
LOC105678344Gephyrin‐like (LOC105678344)−1.331.92E−043.11E−02
LOC105671608Uncharacterized LOC105671608 (LOC105671608)−1.352.62E−043.96E−02
LOC105678353Aminopeptidase N‐like (LOC105678353)−1.432.18E−061.56E−03
LOC105677450Phosphotriesterase‐related protein‐like (LOC105677450)−1.441.15E−042.14E−02
LOC105670356Sodium‐dependent nutrient amino acid transporter 1‐like (LOC105670356)−1.451.64E−042.79E−02
LOC105679178Uncharacterized LOC105679178 (LOC105679178)−1.455.80E−046.69E−02
LOC105670873Uncharacterized LOC105670873 (LOC105670873)−1.454.31E−051.05E−02
LOC105668011Uncharacterized LOC105668011 (LOC105668011)−1.512.29E−043.59E−02
LOC105670875Uncharacterized LOC105670875 (LOC105670875)−1.536.10E−046.82E−02
LOC105676970A disintegrin and metalloproteinase with thrombospondin motifs 7‐like (LOC105676970)−1.538.34E−048.28E−02
LOC105679161A disintegrin and metalloproteinase with thrombospondin motifs 17‐like (LOC105679161)−1.543.75E−059.80E−03
LOC105674012Phosphotriesterase‐related protein‐like (LOC105674012)−1.551.04E−042.03E−02
LOC105676008Uncharacterized LOC105676008 (LOC105676008)−1.551.57E−056.03E−03
LOC105679027Uncharacterized LOC105679027 (LOC105679027)−1.584.64E−045.85E−02
LOC105674893Uncharacterized LOC105674893 (LOC105674893)−1.593.67E−044.89E−02
LOC105673254Thyrotropin‐releasing hormone‐degrading ectoenzyme‐like (LOC105673254)−1.603.12E−044.40E−02
LOC105674631Uncharacterized LOC105674631 (LOC105674631)−1.615.14E−046.19E−02
LOC105671207A disintegrin and metalloproteinase with thrombospondin motifs 7‐like (LOC105671207)−1.632.47E−057.36E−03
LOC105677676Aminopeptidase N‐like (LOC105677676)−1.673.69E−044.89E−02
LOC105674526Uncharacterized LOC105674526 (LOC105674526)−1.718.17E−063.81E−03
LOC105677348Uncharacterized LOC105677348 (LOC105677348)−1.732.80E−151.00E−11
LOC105674527Uncharacterized LOC105674527 (LOC105674527)−1.742.66E−061.78E−03
LOC105676143A disintegrin and metalloproteinase with thrombospondin motifs 8‐like (LOC105676143)−1.788.79E−048.65E−02
LOC105677480Uncharacterized LOC105677480 (LOC105677480)−1.806.99E−047.13E−02
LOC105678343Gephyrin‐like (LOC105678343)−1.865.09E−062.73E−03
LOC105668553A disintegrin and metalloproteinase with thrombospondin motifs 2‐like (LOC105668553)−1.931.66E−042.79E−02
LOC105673493Alpha‐tocopherol transfer protein‐like (LOC105673493)−1.946.81E−047.08E−02
LOC105679148Uncharacterized LOC105679148 (LOC105679148)−1.991.59E−082.13E−05
LOC105676228Glutamyl aminopeptidase‐like (LOC105676228)−2.023.17E−061.93E−03
LOC105677332Uncharacterized LOC105677332 (LOC105677332)−2.052.87E−171.54E−13
LOC105675423Uncharacterized LOC105675423 (LOC105675423)−2.081.51E−055.98E−03
LOC105674732Zinc carboxypeptidase‐like (LOC105674732)−2.101.60E−042.76E−02
LOC105674384Uncharacterized LOC105674384 (LOC105674384)−2.111.91E−056.35E−03
LOC105675063Alkaline phosphatase 4‐like (LOC105675063)−2.131.79E−056.19E−03
LOC105677347Uncharacterized LOC105677347 (LOC105677347)−2.169.71E−201.04E−15
LOC105671515A disintegrin and metalloproteinase with thrombospondin motifs 7‐like (LOC105671515)−2.219.59E−064.11E−03
LOC105677333Uncharacterized LOC105677333 (LOC105677333)−2.255.21E−141.40E−10
LOC105667394A disintegrin and metalloproteinase with thrombospondin motifs 12‐like (LOC105667394)−2.301.37E−042.48E−02
LOC105668554A disintegrin and metalloproteinase with thrombospondin motifs 2‐like (LOC105668554)−2.455.20E−046.19E−02
LOC105679017Uncharacterized LOC105679017 (LOC105679017)−2.776.92E−051.51E−02
T4LOC105679873Sequestosome‐1 (LOC105679873)3.083.32E−144.73E−11
LOC105674352Aromatic‐l‐amino acid decarboxylase (LOC105674352)3.033.71E−134.39E−10
LOC105667809Protein lethal(2)essential for life‐like (LOC105667809)3.021.13E−075.03E−05
LOC105676758Ninjurin‐1 (LOC105676758)2.822.79E−071.10E−04
LOC105678482NF‐kappa‐B inhibitor cactus‐like (LOC105678482)2.783.58E−092.12E−06
LOC105678050Uncharacterized LOC105678050 (LOC105678050)2.648.90E−062.48E−03
LOC105675162Uncharacterized LOC105675162 (LOC105675162)2.334.34E−061.40E−03
LOC105679973Fatty acid binding protein 1‐B.1‐like (LOC105679973)1.971.70E−054.33E−03
LOC105674105Beta‐hexosaminidase subunit beta‐like (LOC105674105)1.926.17E−051.19E−02
LOC105678395Uncharacterized LOC105678395 (LOC105678395)1.896.75E−062.09E−03
LOC105677178Alpha‐2‐macroglobulin‐like protein 1 (LOC105677178) (TepII)1.892.59E−069.12E−04
LOC105671337Putative fatty acyl‐CoA reductase CG5065 (LOC105671337)1.862.04E−043.46E−02
LOC105679392Vanin‐like protein 1 (LOC105679392)1.838.62E−062.48E−03
LOC105677051Protein Malvolio (LOC105677051)1.802.15E−043.56E−02
LOC105676443Uncharacterized LOC105676443 (LOC105676443)1.793.88E−058.35E−03
LOC105679998Heat shock 70 kDa protein cognate 4 (LOC105679998)1.423.74E−045.42E−02
LOC105669805Facilitated trehalose transporter Tret1‐2 homolog (LOC105669805)−1.567.81E−049.86E−02
LOC105675281Fibrillin‐1 (LOC105675281)−1.674.31E−046.13E−02
LOC105670714Alpha‐amylase A (LOC105670714)−1.784.73E−059.49E−03
LOC105675053Cytochrome P450 6a2‐like (LOC105675053)−1.794.80E−046.57E−02
LOC105667318Dentin sialophosphoprotein‐like (LOC105667318)−1.872.69E−056.21E−03
LOC105676465Facilitated trehalose transporter Tret1 (LOC105676465)−1.873.55E−045.26E−02
LOC105676200Short‐chain dehydrogenase/reductase family 16C member 6‐like (LOC105676200)−1.882.75E−044.45E−02
LOC105676829Stearoyl‐CoA desaturase 5‐like (LOC105676829)−1.906.18E−048.14E−02
LOC105669660Nose resistant to fluoxetine protein 6‐like (LOC105669660)−1.977.40E−049.57E−02
LOC105673315Pheromone‐binding protein Gp‐9‐like (LOC105673315)−2.042.93E−044.64E−02
LOC105677462Peroxisomal hydratase‐dehydrogenase‐epimerase‐like (LOC105677462)−2.133.14E−044.85E−02
LOC105679763Uncharacterized oxidoreductase C26H5.09c‐like (LOC105679763)−2.159.02E−051.67E−02
LOC105672608Facilitated trehalose transporter Tret1‐like (LOC105672608)−2.261.92E−043.32E−02
LOC105671746Probable cytochrome P450 304a1 (LOC105671746)−2.316.96E−072.61E−04
LOC105677950Elongation of very long chain fatty acids protein 4‐like (LOC105677950)−2.514.67E−046.52E−02
LOC105670857Leucine‐rich repeat‐containing protein egg‐6 (LOC105670857)−2.531.57E−054.14E−03
LOC105671912Vitellogenin‐1‐like (LOC105671912)−2.735.67E−047.62E−02
LOC105678691Scavenger receptor class B member 1‐like (LOC105678691)−2.755.51E−093.02E−06
LOC105676041Uncharacterized LOC105676041 (LOC105676041)−2.804.87E−113.85E−08
LOC105674885Purine nucleoside phosphorylase‐like (LOC105674885)−2.839.06E−062.48E−03
LOC105674435Serine protease inhibitor dipetalogastin‐like (LOC105674435)−2.842.69E−069.12E−04
LOC105677195Glucose dehydrogenase [FAD−2.852.71E−056.21E−03
LOC105669773Regucalcin‐like (LOC105669773)−2.851.81E−088.60E−06
LOC105668188Uncharacterized LOC105668188 (LOC105668188)−2.861.41E−087.16E−06
LOC105674040Apolipophorins (LOC105674040)−2.881.39E−075.80E−05
LOC105679486Acyl‐CoA Delta(11) desaturase‐like (LOC105679486)−2.927.97E−049.86E−02
LOC105669905Uncharacterized LOC105669905 (LOC105669905)−2.959.17E−051.67E−02
LOC105675057Uncharacterized LOC105675057 (LOC105675057)−2.953.30E−044.99E−02
LOC105672219Leucine‐rich repeat‐containing protein 4‐like (LOC105672219)−2.982.37E−055.82E−03
LOC105670441Uncharacterized LOC105670441 (LOC105670441)−3.071.75E−043.11E−02
LOC105672550Uncharacterized LOC105672550 (LOC105672550)−3.134.27E−124.34E−09
LOC105670856Negative regulator of reactive oxygen species‐like (LOC105670856)−3.212.74E−091.77E−06
LOC105675773Peptidoglycan‐recognition protein SC2‐like (LOC105675773)−3.243.51E−156.23E−12
LOC105678491Uncharacterized LOC105678491 (LOC105678491)−3.679.17E−128.16E−09
LOC105671873Uncharacterized LOC105671873 (LOC105671873)−3.691.17E−202.78E−17
LOC105677373Probable WRKY transcription factor protein 1 (LOC105677373)−4.042.11E−091.50E−06
LOC105667550Uncharacterized LOC105667550 (LOC105667550)−4.954.11E−058.60E−03
LOC105671872Vitellogenin‐2‐like (LOC105671872)−5.082.66E−361.89E−32
LOC105669522Glucose dehydrogenase [FAD−5.082.89E−056.42E−03
LOC105670022Chymotrypsin‐2‐like (LOC105670022)−5.181.02E−273.64E−24
LOC105668189Uncharacterized LOC105668189 (LOC105668189)−11.644.80E−059.49E−03
LOC105670097Spidroin‐1 (LOC105670097)−13.258.03E−049.86E−02
T8LOC105669806Cytochrome P450 307a1‐like (LOC105669806)1.361.15E−074.64E−04
LOC105676242Uncharacterized LOC105676242 (LOC105676242)1.311.03E−051.19E−02
LOC105671866Serine protease gd‐like (LOC105671866)1.315.74E−069.27E−03
LOC105672126Uncharacterized LOC105672126 (LOC105672126)1.097.45E−056.35E−02
LOC105671608Uncharacterized LOC105671608 (LOC105671608)1.061.72E−049.96E−02
LOC105674427Beta‐1,3‐glucan‐binding protein‐like (LOC105674427)1.027.86E−056.35E−02
LOC105668572Uncharacterized LOC105668572 (LOC105668572)0.914.88E−083.94E−04
LOC105668988Uncharacterized LOC105668988 (LOC105668988)0.901.43E−049.96E−02
LOC105677178Alpha‐2‐macroglobulin‐like protein 1 (LOC105677178) (TepII)0.731.63E−049.96E−02
LOC105675407Inhibin beta E chain (LOC105675407)−0.777.26E−056.35E−02
LOC105677462Peroxisomal hydratase‐dehydrogenase‐epimerase‐like (LOC105677462)−0.891.54E−049.96E−02
LOC105672608Facilitated trehalose transporter Tret1‐like (LOC105672608)−0.937.57E−061.02E−02
LOC105676062Protein henna (LOC105676062)−1.304.41E−068.90E−03
LOC105668757Uncharacterized LOC105668757 (LOC105668757)−2.034.17E−071.12E−03
T12LOC105668184Uncharacterized LOC105668184 (LOC105668184)8.581.64E−088.01E−06
LOC105675287Major royal jelly protein 1 (LOC105675287)5.051.72E−296.14E−26
LOC105670097Spidroin‐1 (LOC105670097)3.474.32E−045.14E−02
LOC105678813Uncharacterized LOC105678813 (LOC105678813)3.456.53E−433.50E−39
LOC105669245Ejaculatory bulb‐specific protein 3‐like (LOC105669245)2.925.39E−061.41E−03
LOC105676540Uncharacterized LOC105676540 (LOC105676540)2.867.75E−292.08E−25
LOC105676242Uncharacterized LOC105676242 (LOC105676242)2.633.00E−236.44E−20
LOC105670707Uncharacterized transmembrane protein DDB_G0289901‐like (LOC105670707)2.175.77E−456.19E−41
LOC105679181Facilitated trehalose transporter Tret1 (LOC105679181)1.871.22E−096.87E−07
LOC105672089Lipid storage droplets surface‐binding protein 2‐like (LOC105672089)1.871.94E−091.04E−06
LOC105671866Serine protease gd‐like (LOC105671866)1.704.82E−113.44E−08
LOC105672123Uncharacterized LOC105672123 (LOC105672123)1.633.02E−055.73E−03
LOC105674930Facilitated trehalose transporter Tret1‐like (LOC105674930)1.602.18E−078.67E−05
LOC105673362Limulus clotting factor C‐like (LOC105673362)1.556.18E−072.14E−04
LOC105669469Cytochrome b5‐like (LOC105669469)1.466.81E−137.30E−10
LOC105675162Uncharacterized LOC105675162 (LOC105675162)1.461.35E−162.41E−13
LOC105677051Protein Malvolio (LOC105677051)1.443.83E−123.42E−09
LOC105676758Ninjurin‐1 (LOC105676758)1.411.24E−075.10E−05
LOC105678482NF‐kappa‐B inhibitor cactus‐like (LOC105678482)1.408.63E−161.32E−12
LOC105678075Tyrosine 3‐monooxygenase (LOC105678075)1.401.51E−131.80E−10
LOC105673363Limulus clotting factor C‐like (LOC105673363)1.373.02E−091.54E−06
LOC105675429Cyclic GMP‐AMP synthase (LOC105675429)1.295.14E−082.29E−05
LOC105677645Cytochrome P450 6A1‐like (LOC105677645)1.249.63E−051.54E−02
LOC105677207Gamma‐glutamyl transpeptidase 1‐like (LOC105677207)1.214.40E−123.63E−09
LOC105679973Fatty acid binding protein 1‐B.1‐like (LOC105679973)1.213.53E−061.02E−03
LOC105676748Cysteine sulfinic acid decarboxylase (LOC105676748)1.191.21E−063.92E−04
LOC105671174Lipopolysaccharide‐induced tumor necrosis factor‐alpha factor homolog (LOC105671174)1.152.95E−068.78E−04
LOC105672439Alpha‐sarcoglycan (LOC105672439)1.156.89E−082.95E−05
LOC105679722Uncharacterized LOC105679722 (LOC105679722)1.125.34E−046.10E−02
LOC105678784Protein toll‐like (LOC105678784)1.113.29E−044.15E−02
LOC105671850Protein‐S‐isoprenylcysteine O‐methyltransferase (LOC105671850)1.101.57E−053.11E−03
LOC105677622Uncharacterized LOC105677622 (LOC105677622)1.082.16E−066.61E−04
LOC105677585Venom protease‐like (LOC105677585)1.061.20E−052.48E−03
LOC1056738742‐oxoisovalerate dehydrogenase subunit beta1.037.40E−051.24E−02
LOC105672119Glutamine:fructose‐6‐phosphate aminotransferase [isomerizing] 2‐like (LOC105672119)1.034.34E−071.55E−04
LOC105677178Alpha‐2‐macroglobulin‐like protein 1 (LOC105677178) (TepII)1.022.65E−071.02E−04
LOC105672744Probable phospholipid‐transporting ATPase VD (LOC105672744)0.993.88E−061.09E−03
LOC105667656Uncharacterized LOC105667656 (LOC105667656)0.981.82E−053.54E−03
LOC105678551Uncharacterized LOC105678551 (LOC105678551)0.964.23E−045.12E−02
LOC105676247Uncharacterized LOC105676247 (LOC105676247)0.958.77E−062.09E−03
LOC105671291Putative inorganic phosphate cotransporter (LOC105671291)0.928.11E−048.44E−02
LOC105673744Uncharacterized LOC105673744 (LOC105673744) (Serpin‐27A‐like)0.911.01E−041.60E−02
LOC105672065Uncharacterized LOC105672065 (LOC105672065)0.913.06E−044.05E−02
LOC105677172Protein dimmed‐like (LOC105677172)0.909.81E−062.19E−03
LOC105675116Sterol 24‐C‐methyltransferase‐like (LOC105675116)0.895.33E−059.08E−03
LOC105668572Uncharacterized LOC105668572 (LOC105668572)0.891.39E−042.09E−02
LOC105672359Thiamine transporter 2‐like (LOC105672359)0.887.74E−051.28E−02
LOC105673919ATP‐binding cassette sub‐family C member 9 (LOC105673919)0.883.12E−055.78E−03
LOC105668941Probable citrate synthase 2, mitochondrial (LOC105668941)0.863.49E−056.23E−03
LOC105669588Apoptosis‐inducing factor 3 (LOC105669588)0.852.78E−071.03E−04
LOC105674532ETS homologous factor‐like (LOC105674532)0.843.01E−044.05E−02
LOC105678679AN1‐type zinc finger protein 2A‐like (LOC105678679)0.845.66E−046.38E−02
LOC105677494Annexin B9 (LOC105677494)0.837.92E−061.97E−03
LOC105670266Sodium/potassium/calcium exchanger 3‐like (LOC105670266)0.819.60E−062.19E−03
LOC105679962Thioredoxin reductase 1, mitochondrial (LOC105679962)0.815.39E−061.41E−03
LOC105668729Nuclear factor NF‐kappa‐B p100 subunit (LOC105668729) (Relish)0.783.01E−044.05E−02
LOC105678483NF‐kappa‐B inhibitor cactus‐like (LOC105678483)0.734.25E−045.12E−02
LOC105675225Kelch‐like ECH‐associated protein 1 (LOC105675225)0.711.28E−041.96E−02
LOC105678890Sodium‐independent sulfate anion transporter (LOC105678890)0.717.95E−048.44E−02
LOC105673596Putative inorganic phosphate cotransporter (LOC105673596)0.624.03E−045.03E−02
LOC105675851Sphingosine kinase 2 (LOC105675851)0.627.01E−047.66E−02
LOC105677558Kinectin‐like (LOC105677558)0.611.64E−042.40E−02
LOC105668823Uncharacterized LOC105668823 (LOC105668823)0.619.88E−049.77E−02
LOC105674043Uncharacterized LOC105674043 (LOC105674043)0.602.51E−043.54E−02
LOC105671136Serine protease 52‐like (LOC105671136)0.538.59E−048.85E−02
LOC105678761Serine protease inhibitor 3/4‐like (LOC105678761)−0.519.14E−049.33E−02
LOC105672958Cytochrome P450 9e2‐like (LOC105672958)−0.671.01E−039.87E−02
LOC105668778Leucine‐rich repeats and immunoglobulin‐like domains protein 2 (LOC105668778)−0.679.81E−049.77E−02
LOC105671541Protein croquemort‐like (LOC105671541)−0.689.94E−049.77E−02
LOC105676100Tubulin‐specific chaperone cofactor E‐like protein (LOC105676100)−0.715.35E−046.10E−02
LOC105667678Monocarboxylate transporter 12‐B (LOC105667678)−0.756.13E−046.85E−02
LOC105672522Rho‐related BTB domain‐containing protein 1 (LOC105672522)−0.766.84E−047.56E−02
LOC105677283Alpha‐aminoadipic semialdehyde synthase (LOC105677283)−0.771.62E−042.40E−02
LOC105673034PI‐PLC × domain‐containing protein 1‐like (LOC105673034)−0.788.02E−048.44E−02
LOC105677249Glycogen‐binding subunit 76A (LOC105677249)−0.799.57E−051.54E−02
LOC105667709Uncharacterized LOC105667709 (LOC105667709)−0.794.18E−045.12E−02
LOC105680137Tryptophan 2−0.794.02E−057.07E−03
LOC105674346Neural‐cadherin (LOC105674346)−0.833.04E−044.05E−02
LOC105670852Steroid receptor seven‐up, isoforms B/C (LOC105670852)−0.841.99E−042.84E−02
LOC105678750Uncharacterized LOC105678750 (LOC105678750)−0.854.64E−045.41E−02
LOC105669560Inositol oxygenase (LOC105669560)−0.858.16E−061.99E−03
LOC105668188Uncharacterized LOC105668188 (LOC105668188)−0.858.11E−048.44E−02
LOC105669693Aryl hydrocarbon receptor nuclear translocator‐like protein 1 (LOC105669693)−0.871.70E−042.46E−02
LOC105669509Arylsulfatase B‐like (LOC105669509)−0.924.77E−058.24E−03
LOC105679739Uncharacterized LOC105679739 (LOC105679739)−0.965.10E−082.29E−05
LOC105672956Ribose‐phosphate pyrophosphokinase 1 (LOC105672956)−0.987.94E−048.44E−02
LOC105680118Cysteine proteinase 1‐like (LOC105680118)−0.993.23E−044.12E−02
LOC105677063Organic cation transporter protein (LOC105677063)−1.011.51E−053.06E−03
LOC105674681Cytochrome P450 6j1‐like (LOC105674681)−1.033.11E−044.05E−02
LOC105672502Alpha‐tocopherol transfer protein‐like (LOC105672502)−1.033.13E−044.05E−02
LOC105671942Hexokinase‐2‐like (LOC105671942)−1.041.48E−109.89E−08
LOC105667318Dentin sialophosphoprotein‐like (LOC105667318)−1.043.05E−055.73E−03
LOC105680018Uncharacterized LOC105680018 (LOC105680018)−1.111.16E−052.43E−03
LOC105667320Homeobox protein Nkx‐2.2a‐like (LOC105667320)−1.169.78E−049.77E−02
LOC105671469 d‐arabinitol dehydrogenase 1‐like (LOC105671469)−1.172.77E−043.86E−02
LOC105671862Uncharacterized LOC105671862 (LOC105671862)−1.173.35E−056.08E−03
LOC105677265Tachykinin‐like peptides receptor 99D (LOC105677265)−1.256.72E−072.25E−04
LOC105671615Zinc finger protein 76‐like (LOC105671615)−1.261.12E−052.43E−03
LOC105670688Uncharacterized LOC105670688 (LOC105670688)−1.324.53E−045.33E−02
LOC105678416Pancreatic lipase‐related protein 2‐like (LOC105678416)−1.361.73E−111.32E−08
LOC105676634Carboxypeptidase B‐like (LOC105676634)−1.391.55E−064.88E−04
LOC105668871Phenoloxidase 2‐like (LOC105668871)−1.424.69E−061.29E−03
LOC105679484Sorbitol dehydrogenase‐like (LOC105679484)−1.451.09E−041.70E−02
LOC105675407Inhibin beta E chain (LOC105675407)−1.571.85E−152.47E−12
LOC105670471Trypsin epsilon‐like (LOC105670471)−1.641.15E−052.43E−03
LOC105678258Facilitated trehalose transporter Tret1‐like (LOC105678258)−1.876.36E−061.62E−03
LOC105672897Cytochrome P450 4C1‐like (pseudo)−1.971.08E−096.45E−07
LOC105672608Facilitated trehalose transporter Tret1‐like (LOC105672608)−2.181.63E−101.03E−07
LOC105672083Cytochrome P450 4c21‐like (LOC105672083)−2.429.57E−062.19E−03
LOC105677462Peroxisomal hydratase‐dehydrogenase‐epimerase‐like (LOC105677462)−2.452.17E−122.11E−09

LFC: log2 fold change.

Table 4

Differentially expressed core immune genes induced by bacterial injection in the queens. T2, T4, T8, and T12 indicate post‐injection time points

LocusAnnotationSocialIsolated
T2T4T8T12T2T4T8T12
TollLOC105673881BGBP, recognition of microbes1.18
LOC105673362Serine protease, activation of the pathway2.741.451.55
LOC105675725Serine protease, activation of the pathway1.04
LOC105671866Serine protease, activation of the pathway1.311.70
LOC105673363Serine protease, activation of the pathway1.37
LOC105678817Protein toll‐like1.69−0.94
LOC105678912Protein toll‐like−0.94
LOC105678648Protein toll‐like1.50
LOC105678784Protein toll‐like1.11
LOC105678482Cactus‐1a, Toll signaling2.781.40
LOC105678483Cactus‐1b, Toll signaling0.73
LOC105676758Ninjurin, up‐regulated by the Toll pathway2.821.41
ImdLOC105668729Relish, Imd signaling0.540.78
LOC105675773PGRP‐S2a, negative regulator of Imd pathway−1.20−3.24
LOC105678813Pirk, negative regulator of Imd pathway3.45
AMPsLOC105670591Hymenoptaecin2.09
LOC105675436Ixodidin−1.69
LOC105675717Defensin−1.80
MelanizationLOC105676303Ebony1.81
LOC105667585Laccase1.481.66
LOC105668871Prophenoloxidase (PPO)−2.36−1.42
LOC105674352Dopa decarboxylase1.783.03
LOC105675407inhibin beta E chain, limits infection induced melanization−0.77−1.57
LOC105677585Serine protease, activation of PPO1.06
LOC105671136Serine protease, activation of PPO0.53
LOC105678075Pale, involved in melanization1.40
LOC105673744serpin, inhibition of PPO activation0.91
PhagocytosisLOC105678691SCR‐B‐like, phagocytosis−2.28−2.75
LOC105677178TepII, phagocytosis1.890.731.02
LOC105675281Nim‐C, mediates phagocytosis−1.67
LOC105671541Croquemort, phagocytosis−0.68
Differentially expressed core immune genes induced by bacterial injection in the queens. T2, T4, T8, and T12 indicate post‐injection time points The majority of the DEGs were not directly related to immune response, the core immune genes representing only 5% and 9% of the regulated genes in social and isolated queens, respectively. To get insight on the affected biological processes and molecular functions, GO enrichment analysis was carried out for treatment contrasts with at least 10 DEGs. The up‐regulated genes of social queens at 4 hpi showed enrichment of proteolysis and serine‐type endopeptidase inhibitor activity (Appendix: Table A2). In the isolated queens, down‐regulated genes at 2 hpi showed enrichment of proteolysis, molybdopterin cofactor biosynthetic process, and serine protease inhibitor activity (Appendix: Table A2). The genes categorized as being involved in proteolysis and having serine protease inhibitor activity were largely the same genes as in the social queens. Oxidation‐reduction process was enriched in the down‐regulated genes of isolated queens at 12 hpi including gene encoding for phenoloxidase (LOC105668871) and several cytochrome P450 protein‐coding genes.

Activation of Toll signaling pathway

The expression of immune genes indicated activation of the signaling pathway Toll (Table 4). In social queens, five Toll pathway genes were up‐regulated. These included beta‐1,3‐glucan‐binding protein (BGBP, LOC105673881), based on BLASTP search similar to Drosophila microbial recognition protein GNBP1 (GenBank Accession number NP_524142, 34% identity, 92% coverage) involved in recognition of gram‐positive bacteria (Pili‐Floury et al., 2004). Up‐regulated were also two genes encoding serine proteases: limulus clotting factor C‐like (LOC105673362) similar to Drosophila modular serine protease, modSP (NP_536776, 27% identity, 97% coverage), and serine protease snake‐like (LOC105675725) similar to Drosophila snake (NP_524338, 39% identity, 56% coverage). Both modSP and snake are involved in activation of the Toll receptor by transmitting microbial recognition signals from pattern‐recognition proteins GNBP1 and PGRP‐SA to Spätzle, which functions just upstream of Toll (Buchon et al., 2009). Two genes encoding Toll receptors were up‐regulated, LOC105678817 and LOC105678648, both similar to Drosophila Toll (NP_524518, 29% identity, 70% coverage and 30% identity, 48% coverage, respectively). In the isolated queens, seven Toll pathway genes were up‐regulated and two down‐regulated (Table 4). Three genes encoding for serine proteases, all involved in the activation of the Toll pathway in a similar way described above for modSP and snake, were up‐regulated: two limulus clotting factor C‐like (LOC105673362 and LOC105673363) similar to Drosophila modSP (NP_536776, 27% identity, 97% coverage and 31% identity, 94% coverage, respectively) and additionally, serine protease gd‐like (LOC105671866) similar to gastrulation‐defective in Drosophila (NP_001303552, 29% identity, 84% coverage) that presumably activates serine protease snake (Rose et al., 2003). One gene encoding Toll‐like protein (LOC105678784) similar to Drosophila Toll (NP_524518, 36% identity, 90% coverage), which is a transmembrane receptor, was up‐regulated, and two Toll‐like protein‐coding genes were down‐regulated (LOC105678817 and LOC105678912). Two genes downstream of Toll receptor were up‐regulated, cactus‐1a (LOC105678482) and cactus‐1b (LOC105678483), both similar to Drosophila cactus (NP_476943, 43% identity, 50% coverage and 38% identity, 76% coverage, respectively) which is an inhibitor of NF‐κB transcription factor Dorsal that positively regulates the transcription of antimicrobial peptides (AMPs; Ferrandon et al., 2007). Notably, our analysis only revealed two Toll pathway genes overlapping between the social and isolated queens, limulus clotting factor C‐like (LOC105673362) and protein Toll‐like (LOC105678817), of which the latter was significantly up‐regulated in the social queens while down‐regulated in the isolated queens.

Activation of Imd signaling pathway

Genes along the Imd pathway were not as widely represented among the DEGs as the Toll pathway genes (Table 4). Down‐regulated in both social and isolated queens was a gene encoding for peptidoglycan‐recognition protein SC2 (PGRP‐SC2, LOC105675773), which is a negative regulator of the Imd pathway (Bischoff et al., 2006). In addition, isolated queens showed up‐regulation of a gene encoding for the NF‐κB‐like transcription factor Relish (LOC105668729) (Ferrandon et al., 2007) and for uncharacterized protein (LOC105678813) similar to Drosophila poor Imd response upon knock‐in (NP_001286686, 39% identity, 24% coverage), which, again, is a negative regulator of the Imd pathway (Kleino et al., 2008).

Expression of antimicrobial peptides

The Toll and Imd signaling cascades culminate in the expression of AMPs (Ferrandon et al., 2007), which are immune effectors attacking fungal and bacterial pathogens in the host. In social queens, one AMP encoding gene, hymenoptaecin (LOC105670591) (Casteels, Ampe, Jacobs, & Tempst, 1993), was up‐regulated at 12 hpi, and two AMP genes were down‐regulated at 4 hpi: defensin‐2 (LOC105675717) and chymotrypsin inhibitor‐like (LOC105675436) similar (41% identity, 71% coverage) to ixodidin (P83516), which has been characterized in the Cattle tick Rhipicephalus microplus (Fogaça et al., 2006).

Melanization

Melanization—an active mechanism to encapsulate pathogens within the host—was induced in both social and isolated queens indicated by a number of up‐regulated genes (Table 4), for example, venom protease‐like (LOC105677585) similar to venom serine protease (B5U2W0, 50% identity, 96% coverage) from Bombus ignitus, which is shown to activate the phenoloxidase cascade (Choo et al., 2010). Once activated, phenoloxidase catalyzes the production of quinones, which are polymerized to microbicidal melanin (De Gregorio et al., 2002). Up‐regulated were also N‐(5‐amino‐5‐carboxypentanoyl)‐ (LOC105676303) similar to ebony from Drosophila (NP_524431, 47% identity, 98% coverage) and aromatic‐ (LOC105674352), similar to Drosophila dopa decarboxylase (NP_724164, 74% identity, 90% coverage), both involved in melanization (Riedel, Vorkel, & Eaton, 2011).

Phagocytosis

Three genes involved in phagocytosis were down‐regulated (Table 4). These involved a gene encoding for scavenger receptor class B member 1‐like (LOC105678691) and protein croquemort‐like (LOC105671541), both similar to Drosophila croquemort (Q27367, 28% identity, 75% coverage and 37% identity, 90% coverage, respectively) required in the uptake of bacteria by phagocytes (Guillou, Troha, Wang, Franc, & Buchon, 2016), and fibrillin‐1 (LOC105675281) similar to Drosophila eater (NP_651533, 37% identity, 49% coverage) that is also a phagocytic receptor promoting engulfment of bacteria (Kocks et al., 2005). Up‐regulated was a gene encoding for alpha‐2‐macroglobulin‐like protein 1 (LOC105677178) similar to Drosophila TepII (NP_723300, 34% identity, 37% coverage) that recognizes surface structures of bacteria leading to phagocytosis (Shokal, Kopydlowski, & Eleftherianos, 2017). Here, only the gene encoding for scavenger receptor class B member 1‐like (LOC105678691) was regulated in both social and isolated queens.

Interaction effect of social isolation and bacterial injection

An interaction analysis of social isolation and bacterial injection at all the four time points showed regulation of 20 genes across all time points in the bacteria‐injected isolated queens (Tables 3 and 5). These included down‐regulation at 4 hpi of the Toll receptor activator‐gene spätzle (LOC105678357), up‐regulation at 12 hpi of the Imd pathway signaling gene imd (LOC105672003) and down‐regulation, also at 12 hpi, of hemocyte protein–glutamine gamma‐glutamyl transferase‐like (LOC105670674) similar to transglutaminase (NP_609174, 37% identity, 90% coverage) in Drosophila that inhibits the Imd pathway transcription factor Relish (Maki, Shibata, & Kawabata, 2017).
Table 5

Differentially expressed genes in bacteria‐injected isolated queens in interaction analysis of social environment and bacterial treatment with false discovery rate <10%. T2, T4, T8, and T12 indicate the post‐injection time points

Time pointLocusDescriptionLFC p‐ValueAdjusted p‐value
T2LOC105672931Uncharacterized protein LOC1056729311.415.31E−066.69E−02
T4LOC105678357Protein spätzle−1.402.61E−103.28E−06
LOC105668988Uncharacterized LOC105668988−7.825.81E−083.64E−04
LOC105667488Uncharacterized LOC105667488−2.501.71E−056.36E−02
LOC105668757Non‐coding RNA−1.742.03E−056.36E−02
LOC105668733Lambda‐crystallin homolog−0.553.13E−056.55E−02
LOC105678842Acyl‐CoA Delta(11) desaturase‐like−1.713.13E−056.55E−02
LOC105676303N‐(5‐amino‐5‐carboxypentanoyl)‐l‐cysteinyl‐d‐valine synthase−1.405.04E−059.03E−02
T8LOC105675386Sodium‐coupled monocarboxylate transporter 1−0.653.45E−064.35E−02
T12LOC105677280Uncharacterized LOC1056772802.018.53E−119.68E−07
LOC105674672Cholesterol desaturase daf‐361.496.29E−083.57E−04
LOC105675029Uncharacterized LOC105675029−0.831.20E−064.54E−03
LOC105677088Cytochrome P450 9e2‐like0.992.24E−066.36E−03
LOC105670674Hemocyte protein–glutamine gamma‐glutamyl transferase‐like−0.599.36E−061.77E−02
LOC105672003Uncharacterized (imd)0.819.08E−061.77E−02
LOC105673930MLX‐interacting protein0.472.47E−054.01E−02
LOC105669664Uncharacterized LOC1056696641.178.56E−059.87E−02
LOC105671661Inositol polyphosphate multikinase0.479.57E−059.87E−02
LOC105675400Uncharacterized LOC1056754000.508.01E−059.87E−02
LOC105676429Protein embryonic gonad‐like0.739.19E−059.87E−02

LFC: log2 fold change.

Differentially expressed genes in bacteria‐injected isolated queens in interaction analysis of social environment and bacterial treatment with false discovery rate <10%. T2, T4, T8, and T12 indicate the post‐injection time points LFC: log2 fold change. Hence, in both presence and absence of workers, all important immune defense pathways were triggered in the queens, with the highest number in the Toll pathway.

DISCUSSION

In this study, we tested how the presence or absence of workers affects ant queen immune response after bacterial infection. When testing for the effect of our experimentally induced bacterial infections, we found that existing viral load had an effect on differential gene expression analyses and that virus presence and load should be taken into account in these types of analysis, as previously reported (Gerth & Hurst, 2017). To further control for the effect of social worker presence or absence per se in the absence of an infection, we first analyzed differential gene expression between Ringer‐injected queens reared in the social environment or alone. Despite our sample size being large enough to detect significant effects of rearing on queen metabolism, we could not detect any general effect on queen immune gene expression. We then tested whether worker presence or absence interfered with the queens’ individual immune response to bacterial infection over the course of infection. Overall, we found that injection of bacteria, over the four time points studied, affected the expression of similar numbers of genes in both social and isolated queens but interestingly, the social queens up‐regulated the majority of the genes, whereas in the isolated queens, down‐regulation was prevailing. This general down‐regulation might be a consequence of social isolation, which has been shown to affect life‐history traits by reducing longevity in workers of the ant Camponotus fellah (Boulay et al., 1999; Koto et al., 2015), yet did not compromise the innate immune response of bumblebees after pathogen challenge (Richter, Helbing, Erler, & Lattorff, 2012). In the group‐living earwig Forficula auricularia, rearing individuals alone also lead to a transiently increased susceptibility after pathogen exposure shortly after isolation, yet an indistinguishable survival of individuals living isolated or in groups for longer periods (Kohlmeier et al., 2016), hence the effects of social isolation may be plastic, both varying over time and across species. The isolated queens regulated slightly, but not significantly, higher number of the core immune genes than social queens (23 vs. 14, χ2 = 3.38, df = 1, p = 0.07) and the immune gene expression in the isolated queens did not show the overall pattern of down‐regulation observed in all of their DEGs: 65% of immune genes were up‐regulated as opposed to 37% of all DEGs (χ2 = 8.11, df = 1, p = 0.004). Therefore, even though gene expression in the isolated queens showed a trend of down‐regulation, the activation of cellular and humoral immune cascades was comparable to the social queens. An interesting observation was two enriched GO terms, serine protease inhibitor activity and proteolysis, both categories including approximately 20 genes, which were up‐regulated at 4 hpi in the bacteria‐injected social queens and down‐regulated at 2 hpi in the bacteria‐injected isolated queens. All except one of the genes in the serine protease inhibitor‐category were long non‐coding RNAs (lncRNA) which Blast2Go annotation found to contain a protease inhibitor domain suggesting they might regulate serine protease inhibitors (serpins). In insects, serpins are known to be involved in the regulation of immune signaling cascades, phagocytosis, and digestion (Gubb, Sanz‐Parra, Barcena, Troxler, & Fullaondo, 2010), and the expression of serpin‐related lncRNAs could be involved in the fine‐tuning of various arms of immune response. It is striking that the gene expression patterns of these genes showed opposite directions in the two rearing conditions, highlighting the strong effect of social environment on the general response to bacterial injection. As a conclusion, this study shows that ant queens were equally able to activate innate immune signaling cascades after bacterial injection when kept together with workers or when reared alone. This reveals that pathogen‐injected queens raise an induced immune response even in the presence of rearing workers, yet that worker presence interferes with which exact set of genes is regulated. Hence, we could show that individual queen responses are not compromised, but modulated by their social context.

AUTHOR CONTRIBUTIONS

LV and SC designed the research, LV performed the experimental work, LV carried out the bioinformatics analyses of RNA‐seq data, LV and JJ carried out the virus‐related bioinformatics analyses, LV and IH performed the statistical analyses, TB and SE helped LV to interpret the results related to differentially expressed genes, and LV and SC wrote the manuscript with contributions from all authors.

DATA ACCESSIBILITY

The short read sequence data are deposited at NCBI, BioProject PRJNA279338.
  57 in total

Review 1.  Social immunity.

Authors:  Sylvia Cremer; Sophie A O Armitage; Paul Schmid-Hempel
Journal:  Curr Biol       Date:  2007-08-21       Impact factor: 10.834

2.  Survival after pathogen exposure in group-living insects: don't forget the stress of social isolation!

Authors:  P Kohlmeier; K Holländer; J Meunier
Journal:  J Evol Biol       Date:  2016-06-23       Impact factor: 2.411

3.  Opposing effects of allogrooming on disease transmission in ant societies.

Authors:  Fabian J Theis; Line V Ugelvig; Carsten Marr; Sylvia Cremer
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-05-26       Impact factor: 6.237

4.  Redefining the invertebrate RNA virosphere.

Authors:  Mang Shi; Xian-Dan Lin; Jun-Hua Tian; Liang-Jun Chen; Xiao Chen; Ci-Xiu Li; Xin-Cheng Qin; Jun Li; Jian-Ping Cao; John-Sebastian Eden; Jan Buchmann; Wen Wang; Jianguo Xu; Edward C Holmes; Yong-Zhen Zhang
Journal:  Nature       Date:  2016-11-23       Impact factor: 49.962

5.  Transglutaminase-catalyzed incorporation of polyamines masks the DNA-binding region of the transcription factor Relish.

Authors:  Kouki Maki; Toshio Shibata; Shun-Ichiro Kawabata
Journal:  J Biol Chem       Date:  2017-03-03       Impact factor: 5.157

6.  Pirk is a negative regulator of the Drosophila Imd pathway.

Authors:  Anni Kleino; Henna Myllymäki; Jenni Kallio; Leena-Maija Vanha-aho; Kaisa Oksanen; Johanna Ulvila; Dan Hultmark; Susanna Valanne; Mika Rämet
Journal:  J Immunol       Date:  2008-04-15       Impact factor: 5.422

7.  HTSeq--a Python framework to work with high-throughput sequencing data.

Authors:  Simon Anders; Paul Theodor Pyl; Wolfgang Huber
Journal:  Bioinformatics       Date:  2014-09-25       Impact factor: 6.937

8.  Destructive disinfection of infected brood prevents systemic disease spread in ant colonies.

Authors:  Christopher D Pull; Line V Ugelvig; Florian Wiesenhofer; Anna V Grasse; Simon Tragust; Thomas Schmitt; Mark Jf Brown; Sylvia Cremer
Journal:  Elife       Date:  2018-01-09       Impact factor: 8.140

9.  Short reads from honey bee (Apis sp.) sequencing projects reflect microbial associate diversity.

Authors:  Michael Gerth; Gregory D D Hurst
Journal:  PeerJ       Date:  2017-07-12       Impact factor: 2.984

10.  Single-stranded RNA viruses infecting the invasive Argentine ant, Linepithema humile.

Authors:  Monica A M Gruber; Meghan Cooling; James W Baty; Kevin Buckley; Anna Friedlander; Oliver Quinn; Jessica F E J Russell; Alexandra Sébastien; Philip J Lester
Journal:  Sci Rep       Date:  2017-06-12       Impact factor: 4.379
View more
  1 in total

1.  Different bacterial and viral pathogens trigger distinct immune responses in a globally invasive ant.

Authors:  Philip J Lester; Kaitlin H Buick; James W Baty; Antoine Felden; John Haywood
Journal:  Sci Rep       Date:  2019-04-08       Impact factor: 4.379
  1 in total

北京卡尤迪生物科技股份有限公司 © 2022-2023.