Limits...
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

Proposed model of epigenetic regulation of aggression through piRNAs. (A) Divergent selective pressure for aggressive reproductive offspring on males and females creates genomic conflict, but this conflict is balanced by the need for appropriate colony-level aggression. Fathers attempt to increase aggression (through a shift toward aerobic glycolysis, AG) by silencing genes using sperm-loaded piRNAs. Mothers negate this silencing through genomic licensing using oocyte-loaded piRNAs. (B) AHB and EHB differ in aggression due to both genetic effects and a greater epigenetic potential for aggression in AHB, selected for in either their native or introduced range.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4664729&req=5

Figure 4: Proposed model of epigenetic regulation of aggression through piRNAs. (A) Divergent selective pressure for aggressive reproductive offspring on males and females creates genomic conflict, but this conflict is balanced by the need for appropriate colony-level aggression. Fathers attempt to increase aggression (through a shift toward aerobic glycolysis, AG) by silencing genes using sperm-loaded piRNAs. Mothers negate this silencing through genomic licensing using oocyte-loaded piRNAs. (B) AHB and EHB differ in aggression due to both genetic effects and a greater epigenetic potential for aggression in AHB, selected for in either their native or introduced range.

Mentions: We speculate that the metabolic switch toward AG in honeybee brains and the associated aggression is a phenotypic trait that has a partially epigenetic basis, mediated through the piwi/piRNA pathway. An epigenetic switch to aggression is at least implied by theory regarding genomic imprinting in honeybees, as honeybees exhibit extreme polyandry and drones should have an evolutionary drive to produce daughters that are more selfish in regards to producing their own offspring, including more aggressive daughter queens that may be successful in queen duels, therefore inheriting the nest including the worker bees and other resources. In a population there should also be simultaneous selective pressure on the queens to suppress this selfish and aggressive behavior, resulting in intragenomic conflict similar to the Peromyscus mouse example given earlier (Queller, 2003). This level of intracolonial aggression also needs to be balanced with the need for appropriate extra-colonial aggression (i.e., colony defense). The genomic conflict could occur through paternal piRNA silencing to increase aggression and maternal piRNA licensing to mitigate the paternal silencing and reduce aggression. Similar to the WTT and ELBOs discussed above this is a phenotype that would normally be suppressed (or canalized) but which would vary in extent between populations due to differing selective pressures (e.g., within AHB and EHB lineages; Figure 4).


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)

Proposed model of epigenetic regulation of aggression through piRNAs. (A) Divergent selective pressure for aggressive reproductive offspring on males and females creates genomic conflict, but this conflict is balanced by the need for appropriate colony-level aggression. Fathers attempt to increase aggression (through a shift toward aerobic glycolysis, AG) by silencing genes using sperm-loaded piRNAs. Mothers negate this silencing through genomic licensing using oocyte-loaded piRNAs. (B) AHB and EHB differ in aggression due to both genetic effects and a greater epigenetic potential for aggression in AHB, selected for in either their native or introduced range.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 4: Proposed model of epigenetic regulation of aggression through piRNAs. (A) Divergent selective pressure for aggressive reproductive offspring on males and females creates genomic conflict, but this conflict is balanced by the need for appropriate colony-level aggression. Fathers attempt to increase aggression (through a shift toward aerobic glycolysis, AG) by silencing genes using sperm-loaded piRNAs. Mothers negate this silencing through genomic licensing using oocyte-loaded piRNAs. (B) AHB and EHB differ in aggression due to both genetic effects and a greater epigenetic potential for aggression in AHB, selected for in either their native or introduced range.
Mentions: We speculate that the metabolic switch toward AG in honeybee brains and the associated aggression is a phenotypic trait that has a partially epigenetic basis, mediated through the piwi/piRNA pathway. An epigenetic switch to aggression is at least implied by theory regarding genomic imprinting in honeybees, as honeybees exhibit extreme polyandry and drones should have an evolutionary drive to produce daughters that are more selfish in regards to producing their own offspring, including more aggressive daughter queens that may be successful in queen duels, therefore inheriting the nest including the worker bees and other resources. In a population there should also be simultaneous selective pressure on the queens to suppress this selfish and aggressive behavior, resulting in intragenomic conflict similar to the Peromyscus mouse example given earlier (Queller, 2003). This level of intracolonial aggression also needs to be balanced with the need for appropriate extra-colonial aggression (i.e., colony defense). The genomic conflict could occur through paternal piRNA silencing to increase aggression and maternal piRNA licensing to mitigate the paternal silencing and reduce aggression. Similar to the WTT and ELBOs discussed above this is a phenotype that would normally be suppressed (or canalized) but which would vary in extent between populations due to differing selective pressures (e.g., within AHB and EHB lineages; Figure 4).

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