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Biased Allele Expression and Aggression in Hybrid Honeybees may be Influenced by Inappropriate Nuclear-Cytoplasmic Signaling.

Gibson JD, Arechavaleta-Velasco ME, Tsuruda JM, Hunt GJ - Front Genet (2015)

Bottom Line: This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins.It contains many genes that play important roles in metabolic regulation.Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Purdue University, West Lafayette IN, USA.

ABSTRACT
Hybrid effects are often exhibited asymmetrically between reciprocal families. One way this could happen is if silencing of one parent's allele occurs in one lineage but not the other, which could affect the phenotypes of the hybrids asymmetrically by silencing that allele in only one of the hybrid families. We have previously tested for allele-specific expression biases in hybrids of European and Africanized honeybees and we found that there was an asymmetric overabundance of genes showing a maternal bias in the family with a European mother. Here, we further analyze allelic bias in these hybrids to ascertain whether they may underlie previously described asymmetries in metabolism and aggression in similar hybrid families and we speculate on what mechanisms may produce this biased allele usage. We find that there are over 500 genes that have some form of biased allele usage and over 200 of these are biased toward the maternal allele but only in the family with European maternity, mirroring the pattern observed for aggression and metabolic rate. This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins. It contains many genes that play important roles in metabolic regulation. Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use. Based on these findings and previous work investigating aggression and metabolism in bees, we propose a novel hypothesis; that the asymmetric pattern of biased allele usage in these hybrids is a result of inappropriate use of piRNA-mediated nuclear-cytoplasmic signaling that is normally used to modulate aggression in honeybees. This is the first report of widespread asymmetric effects on allelic expression in hybrids and may represent a novel mechanism for gene regulation.

No MeSH data available.


Related in: MedlinePlus

Gene counts in bias categories. Average maternal/paternal bias of all genes in each bias category in each hybrid family (EA, European maternity; AE, Africanized maternity). Gray columns = European allele, Black = Africanized allele. The total number of genes in each category and the number falling in each QTL type are given in the columns on the right. Only genes falling into a single bias category across samples are included in counts for QTL types. ∗Significantly more genes in this category are present within these QTL than expected by chance (Bonferroni corrected p-value = 0.005).
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Figure 1: Gene counts in bias categories. Average maternal/paternal bias of all genes in each bias category in each hybrid family (EA, European maternity; AE, Africanized maternity). Gray columns = European allele, Black = Africanized allele. The total number of genes in each category and the number falling in each QTL type are given in the columns on the right. Only genes falling into a single bias category across samples are included in counts for QTL types. ∗Significantly more genes in this category are present within these QTL than expected by chance (Bonferroni corrected p-value = 0.005).

Mentions: Expression levels of the alleles in the two reciprocal crosses are from Kocher et al. (2015). Briefly, all transcriptome data is derived from the two reciprocal crosses utilizing the A.m. carnica queen (designated EA and AE for those with EHB and AHB maternity, respectively). Transcriptomes were sequenced from cDNA libraries of pooled first instar larvae (two libraries per family), pooled adults (guard bees, two libraries per family), and individual adult brains (three libraries per family). Single nucleotide polymorphisms (SNPs) differentiating European and Africanized alleles were identified by sequencing genomic DNA of the queen and drone parents of these two crosses to ensure the European and Africanized alleles were homozygous and different, resulting in F1 offspring that are heterozygous at all tested SNPs. All reads were mapped to the honeybee reference genome (Amel4.0; The Honeybee Genome Sequencing Consortium, 2006). Using counts of reads at each SNP, a general linear interactive mixed model (SAS, Cary, NC, USA) was utilized to assess expression of each allele for all transcripts containing diagnostic SNPs. The analysis in Kocher et al. (2015) required the bias to be in the same direction (maternal or paternal) in both directions of the cross (EA and AE hybrids) based on significant parent FDR < 0.05, and a bias of at least 0.6 (maternal or paternal reads/total reads; Wang and Clark, 2014) in order to search for consistent parent-of-origin effects. For the current analysis, we relaxed this criteria and only required that the bias be present in one direction of the cross. These genes were then placed into bias categories based on the expression levels of their alleles in each family relative to the parent-of-origin of that allele (e.g., Maternal bias, EA maternal/AE maternal; European bias, EA maternal/AE paternal, etc.; see Figure 1).


Biased Allele Expression and Aggression in Hybrid Honeybees may be Influenced by Inappropriate Nuclear-Cytoplasmic Signaling.

Gibson JD, Arechavaleta-Velasco ME, Tsuruda JM, Hunt GJ - Front Genet (2015)

Gene counts in bias categories. Average maternal/paternal bias of all genes in each bias category in each hybrid family (EA, European maternity; AE, Africanized maternity). Gray columns = European allele, Black = Africanized allele. The total number of genes in each category and the number falling in each QTL type are given in the columns on the right. Only genes falling into a single bias category across samples are included in counts for QTL types. ∗Significantly more genes in this category are present within these QTL than expected by chance (Bonferroni corrected p-value = 0.005).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664729&req=5

Figure 1: Gene counts in bias categories. Average maternal/paternal bias of all genes in each bias category in each hybrid family (EA, European maternity; AE, Africanized maternity). Gray columns = European allele, Black = Africanized allele. The total number of genes in each category and the number falling in each QTL type are given in the columns on the right. Only genes falling into a single bias category across samples are included in counts for QTL types. ∗Significantly more genes in this category are present within these QTL than expected by chance (Bonferroni corrected p-value = 0.005).
Mentions: Expression levels of the alleles in the two reciprocal crosses are from Kocher et al. (2015). Briefly, all transcriptome data is derived from the two reciprocal crosses utilizing the A.m. carnica queen (designated EA and AE for those with EHB and AHB maternity, respectively). Transcriptomes were sequenced from cDNA libraries of pooled first instar larvae (two libraries per family), pooled adults (guard bees, two libraries per family), and individual adult brains (three libraries per family). Single nucleotide polymorphisms (SNPs) differentiating European and Africanized alleles were identified by sequencing genomic DNA of the queen and drone parents of these two crosses to ensure the European and Africanized alleles were homozygous and different, resulting in F1 offspring that are heterozygous at all tested SNPs. All reads were mapped to the honeybee reference genome (Amel4.0; The Honeybee Genome Sequencing Consortium, 2006). Using counts of reads at each SNP, a general linear interactive mixed model (SAS, Cary, NC, USA) was utilized to assess expression of each allele for all transcripts containing diagnostic SNPs. The analysis in Kocher et al. (2015) required the bias to be in the same direction (maternal or paternal) in both directions of the cross (EA and AE hybrids) based on significant parent FDR < 0.05, and a bias of at least 0.6 (maternal or paternal reads/total reads; Wang and Clark, 2014) in order to search for consistent parent-of-origin effects. For the current analysis, we relaxed this criteria and only required that the bias be present in one direction of the cross. These genes were then placed into bias categories based on the expression levels of their alleles in each family relative to the parent-of-origin of that allele (e.g., Maternal bias, EA maternal/AE maternal; European bias, EA maternal/AE paternal, etc.; see Figure 1).

Bottom Line: This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins.It contains many genes that play important roles in metabolic regulation.Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Purdue University, West Lafayette IN, USA.

ABSTRACT
Hybrid effects are often exhibited asymmetrically between reciprocal families. One way this could happen is if silencing of one parent's allele occurs in one lineage but not the other, which could affect the phenotypes of the hybrids asymmetrically by silencing that allele in only one of the hybrid families. We have previously tested for allele-specific expression biases in hybrids of European and Africanized honeybees and we found that there was an asymmetric overabundance of genes showing a maternal bias in the family with a European mother. Here, we further analyze allelic bias in these hybrids to ascertain whether they may underlie previously described asymmetries in metabolism and aggression in similar hybrid families and we speculate on what mechanisms may produce this biased allele usage. We find that there are over 500 genes that have some form of biased allele usage and over 200 of these are biased toward the maternal allele but only in the family with European maternity, mirroring the pattern observed for aggression and metabolic rate. This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins. It contains many genes that play important roles in metabolic regulation. Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use. Based on these findings and previous work investigating aggression and metabolism in bees, we propose a novel hypothesis; that the asymmetric pattern of biased allele usage in these hybrids is a result of inappropriate use of piRNA-mediated nuclear-cytoplasmic signaling that is normally used to modulate aggression in honeybees. This is the first report of widespread asymmetric effects on allelic expression in hybrids and may represent a novel mechanism for gene regulation.

No MeSH data available.


Related in: MedlinePlus