Genomic signatures of eusocial evolution in insects

Mikhailova, Alina A; Rinke, Sarah; Harrison, Mark C

doi:10.1016/j.cois.2023.101136

Cited by 6 publications

(1 citation statement)

References 61 publications

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“…In this meta-analysis, dN/dS scales negatively with genome size in insects, but never with TE content. As eusociality appears to bring about selection relaxation (Imrit et al 2020; Kapheim et al 2015; Weyna and Romiguier 2021), several studies explored the link between N e and genome size in this taxon by focussing on social complexity as a proxy, but with contrasting outcomes: Mikhailova et al (2023) find bigger genome size associated with eusociality in Hymenoptera, but the opposite trend in Blattodea; in contrast and partially in accordance with our findings, Kapheim et al (2015) and Koshikawa et al (2008) report less abundant TEs in eusocial hymenopters and smaller genomes in eusocial termites, respectively. While the approximation of N e based on dN/dS should allow for a quantification of selection efficacy in wider terms than sociality traits, the investigated evolutionary scale might hold an important role in the outcome of such analyses.…”

Section: Discussionmentioning

confidence: 99%

Effective population size does not explain long-term variation in genome size and transposable element content in animals

Marino,

Debaecker,

Fiston-Lavier

et al. 2024

Preprint

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Animal genomes exhibit a remarkable variation in size, but the evolutionary forces responsible for such variation are still debated. As the effective population size (Ne) reflects the intensity of genetic drift, it is expected to be a key determinant of the fixation rate of nearly-neutral mutations. Accordingly, the Mutational Hazard Hypothesis postulates lineages with low Ne to have bigger genome sizes due to the accumulation of slightly deleterious transposable elements (TEs), and those with high Ne to maintain streamlined genomes as a consequence of a more effective selection against TEs. However, the existence of both empirical confirmation and refutation using different methods and different scales precludes its general validation. Using high-quality public data, we estimated genome size, TE content and rate of non-synonymous to synonymous substitutions (dN/dS) as Ne proxy for 807 species including vertebrates, molluscs and insects. After collecting available life-history traits, we tested the associations among population size proxies, TE content and genome size, while accounting for phylogenetic non-independence. Our results confirm TEs as major drivers of genome size variation, and endorse life-history traits and dN/dS as reliable proxies for Ne. However, we do not find any evidence for increased drift to result in an accumulation of TEs across animals. Within more closely related clades, only a few isolated and weak associations emerge in fishes and birds. Our results outline a scenario where TE dynamics vary according to lineage-specific patterns, lending no support for genetic drift as the predominant force driving long-term genome size evolution in animals.

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Section: Discussionmentioning

confidence: 99%

Effective population size does not explain long-term variation in genome size and transposable element content in animals

Marino,

Debaecker,

Fiston-Lavier

et al. 2024

Preprint

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Genomic analyses of the southern and eastern yellowjacket wasps (Hymenoptera: Vespidae) reveal evolutionary signatures of social life

Catto,

Caine,

Orr

et al. 2024

Annals of the Entomological Society of America

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Insects have evolved remarkably complex social systems. Social wasps are particularly noteworthy because they display gradations in social behaviors. Here, we sequence the genomes of two highly diverged Vespula wasps, V. squamosa and V. maculifrons Buysson (Hymenoptera: Vespidae), to gain greater insight into the evolution of sociality. Both V. squamosa and V. maculifrons are social wasps that live in large colonies characterized by distinct queen and worker castes. However, V. squamosa is a facultative social parasite, and V. maculifrons is its frequent host. We found that the genomes of both species were ~200 Mbp in size, similar to the genome sizes of congeneric species. Analyses of gene expression from members of different castes and developmental stages revealed similarities in expression patterns among immature life stages. We also found evidence of DNA methylation within the genome of both species by directly analyzing DNA sequence reads. Moreover, genes that were highly and uniformly expressed were also relatively highly methylated. We further uncovered evidence of differences in patterns of molecular evolution in the two taxa, consistent with V. squamosa exhibiting alterations in evolutionary pressures associated with its facultatively parasitic or polygyne life history. Finally, rates of gene evolution were correlated with variation in gene expression between castes and developmental stages, as expected if more highly expressed genes were subject to stronger levels of selection. Overall, this study expands our understanding of how social behavior relates to genome evolution in insects.

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Genomic architecture in social insects is more strongly associated with phylogeny than social behavior

Behrends,

Hagan,

Kuinkel

et al. 2024

Annals of the Entomological Society of America

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The evolution of sociality in insects has been predicted to reduce effective population sizes, in turn leading to changes in genome architecture, including higher recombination rates, larger genomes, increased GC-biased gene conversion (gBGC), and greater intragenomic variation in GC content to maintain castes through differential methylation. As the number of sequenced insect genomes continues to grow, it remains an open question which, if any, of these genomic features are consistent across social insect genomes. A major challenge to determining such commonalities has been the lack of phylogenetically controlled analyses across independent origins of sociality. Of the 15 Hymenoptera species for which recombination rate was available, social species had higher rates of recombination. Next, we conducted a broader analysis of genome architecture by analyzing genome assemblies for 435 species of Hymenoptera and 8 species of Blattodea to test if GC content, genome size, distribution of CpG sites or codon bias repeatedly differed between social and nonsocial species. Overall, there was little support for predictable changes in genome architecture associated with sociality across Hymenoptera, after accounting for phylogenetic relationships. However, we found a significant negative relationship between sociality and GC content within the family Apidae and a significant negative relationship between sociality and genome size within the family Halictidae. In all, these results suggest that unique origins of social behavior may produce unique trends in genomic architecture. Our study highlights the need to examine genome architecture across independent origins of social behavior.

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Genomic signatures of eusocial evolution in insects

Cited by 6 publications

References 61 publications

Effective population size does not explain long-term variation in genome size and transposable element content in animals

Effective population size does not explain long-term variation in genome size and transposable element content in animals

Genomic analyses of the southern and eastern yellowjacket wasps (Hymenoptera: Vespidae) reveal evolutionary signatures of social life

Genomic architecture in social insects is more strongly associated with phylogeny than social behavior

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