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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

Sting response time of individuals. Individual bees (573 total) were given an electrical shock from a constant current stimulator and the time in seconds for them to sting a suede patch was recorded. Genotypes of reciprocal hybrids are given on the X-axis: Africanized maternity hybrids AC (Apis mellifera carnica father) and AL (A.m. ligustica father), and Africanized paternity hybrids CA (A.m. carnica mother) and LA (A.m. ligustica mother). Data presented is untransformed, letters designate significant differences.
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Figure 2: Sting response time of individuals. Individual bees (573 total) were given an electrical shock from a constant current stimulator and the time in seconds for them to sting a suede patch was recorded. Genotypes of reciprocal hybrids are given on the X-axis: Africanized maternity hybrids AC (Apis mellifera carnica father) and AL (A.m. ligustica father), and Africanized paternity hybrids CA (A.m. carnica mother) and LA (A.m. ligustica mother). Data presented is untransformed, letters designate significant differences.

Mentions: We tested the stinging behavior of individual bees from our crosses by measuring the time that each bee took to sting a black suede patch after being stimulated with electrical current (assay described in Shorter et al., 2012). In total 573 bees were tested from the four F1 reciprocal colonies. These colonies are designated AL (AHB queen × A.m. ligustica drone), LA (A.m. ligustica queen × AHB drone), AC (AHB queen × A.m. carnica drone), and CA (A.m. carnica queen × AHB drone) in Figure 2. Data was transformed using the natural log function to fit a normal distribution and was analyzed under a one way analysis of variance to test for differences in the stinging behavior of the four F1 reciprocal crosses. Least squares means t-tests were performed to compare the means of the four groups.


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)

Sting response time of individuals. Individual bees (573 total) were given an electrical shock from a constant current stimulator and the time in seconds for them to sting a suede patch was recorded. Genotypes of reciprocal hybrids are given on the X-axis: Africanized maternity hybrids AC (Apis mellifera carnica father) and AL (A.m. ligustica father), and Africanized paternity hybrids CA (A.m. carnica mother) and LA (A.m. ligustica mother). Data presented is untransformed, letters designate significant differences.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 2: Sting response time of individuals. Individual bees (573 total) were given an electrical shock from a constant current stimulator and the time in seconds for them to sting a suede patch was recorded. Genotypes of reciprocal hybrids are given on the X-axis: Africanized maternity hybrids AC (Apis mellifera carnica father) and AL (A.m. ligustica father), and Africanized paternity hybrids CA (A.m. carnica mother) and LA (A.m. ligustica mother). Data presented is untransformed, letters designate significant differences.
Mentions: We tested the stinging behavior of individual bees from our crosses by measuring the time that each bee took to sting a black suede patch after being stimulated with electrical current (assay described in Shorter et al., 2012). In total 573 bees were tested from the four F1 reciprocal colonies. These colonies are designated AL (AHB queen × A.m. ligustica drone), LA (A.m. ligustica queen × AHB drone), AC (AHB queen × A.m. carnica drone), and CA (A.m. carnica queen × AHB drone) in Figure 2. Data was transformed using the natural log function to fit a normal distribution and was analyzed under a one way analysis of variance to test for differences in the stinging behavior of the four F1 reciprocal crosses. Least squares means t-tests were performed to compare the means of the four groups.

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