Biased social chromosome transmission in males of the fire ant <i>Solenopsis invicta</i>

Selfish genetic elements subvert the normal rules of inheritance to unfairly propagate themselves, often at the expense of other genomic elements and the fitness of individuals carrying them. Social life provides diverse avenues for the propagation of such elements. In the fire ant Solenopsis invicta, polymorphic social organization is controlled by a social chromosome, one variant of which (Sb) enhances its own transmission in polygyne colonies through effects on caste development and queen acceptance by workers. Whether the selfish effects of Sb extend to haploid (reproductive) males in this system is less clear. Here, we demonstrate a strong overrepresentation of the Sb social chromosome haplotype in reproductive males, relative to Mendelian expectations, in both the pupal and adult stages. We tested for the presence of selective execution of adult SB males by workers but did not detect such behavior. Combined with the presence of a strong imbalance in the haplotype frequencies already early in the pupal stage, these results indicate that the Sb supergene may distort male haplotype frequencies during larval or embryonic development. These findings are significant because they demonstrate yet another mode by which the selfish tendencies of the Sb supergene are manifested, illuminate complex interactions between Sb and the fire ant breeding system, inform the development of models of the population dynamics of Sb, and illustrate how a selfish supergene can increase in frequency in a population despite harboring deleterious mutations.

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Publication Details

Journal
G3 Genes Genomes Genetics
Published
2024-12-06
DOI
https://doi.org/10.1093/g3journal/jkae289
Citations
6
Primary Topic
Insect and Arachnid Ecology and Behavior
Type
article
Field-Weighted Citation Impact
3.30

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article

Biased social chromosome transmission in males of the fire ant Solenopsis invicta

Brendan G. Hunt, Haolin Zeng, Kenneth G. Ross, Daniel R Hettesheimer
6 citations
G3 Genes Genomes Genetics
Insect and Arachnid Ecology and Behavior
3.30
article

Biased social chromosome transmission in males of the fire ant Solenopsis invicta

Brendan G. Hunt, Haolin Zeng, Kenneth G. Ross, Daniel R Hettesheimer
article en
6 citations

Abstract

Selfish genetic elements subvert the normal rules of inheritance to unfairly propagate themselves, often at the expense of other genomic elements and the fitness of individuals carrying them. Social life provides diverse avenues for the propagation of such elements. In the fire ant Solenopsis invicta, polymorphic social organization is controlled by a social chromosome, one variant of which (Sb) enhances its own transmission in polygyne colonies through effects on caste development and queen acceptance by workers. Whether the selfish effects of Sb extend to haploid (reproductive) males in this system is less clear. Here, we demonstrate a strong overrepresentation of the Sb social chromosome haplotype in reproductive males, relative to Mendelian expectations, in both the pupal and adult stages. We tested for the presence of selective execution of adult SB males by workers but did not detect such behavior. Combined with the presence of a strong imbalance in the haplotype frequencies already early in the pupal stage, these results indicate that the Sb supergene may distort male haplotype frequencies during larval or embryonic development. These findings are significant because they demonstrate yet another mode by which the selfish tendencies of the Sb supergene are manifested, illuminate complex interactions between Sb and the fire ant breeding system, inform the development of models of the population dynamics of Sb, and illustrate how a selfish supergene can increase in frequency in a population despite harboring deleterious mutations.

G3 Genes Genomes GeneticsVol. 15(2)
University of Georgia (US)
National Science Foundation
Openalex Percentile: Top 7%
Insect and Arachnid Ecology and Behavior
3.30
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Biased social chromosome transmission in males of the fire ant <i>Solenopsis invicta</i> — Brendan G. Hunt, Haolin Zeng, et al. · G3 Genes Genomes Genetics (2024) | TGRS Research Map | TGRS