Eusociality in Termites Reduces the Efficiency of Natural Selection

Konsep Inti

Eusociality in termites is associated with a genome-wide reduction in the efficiency of natural selection, as evidenced by an elevated ratio of non-synonymous to synonymous mutations (dN/dS).

Abstrak

The study investigates the genomic consequences of eusociality in termites (Isoptera) on two different timescales.
First, by analyzing transcriptome data from 66 Blattodea species, the authors focus on the ratio of non-synonymous to synonymous mutations (dN/dS) as a marker of natural selection efficiency and effective population size. The results demonstrate an elevated dN/dS ratio in termites compared to other members of Blattodea, suggesting that the convergent evolution toward eusociality strongly reduces the effective population size and the genome-wide efficiency of natural selection.
Then, by comparing 68 termite transcriptomes, the authors show that this decrease in natural selection efficiency is even more pronounced in termites displaying high levels of social complexity. Termite species with the highest levels of social organization, characterized by large colonies and high caste specialization, exhibit the highest dN/dS ratios.
These findings contribute to understanding the complex interplay between social structures and natural selection patterns, highlighting the genetic footprint of eusociality in shaping the evolution of termites. The results suggest that eusociality is associated with a genome-wide reduction in the efficiency of natural selection, similar to the patterns observed in large vertebrates.

Statistik

"Termites (i.e. eusocial Blattodea) exhibit higher dN /dS ratios than solitary Blattodea species."
"Among termites, species displaying the highest levels of social complexity tend to exhibit higher dN /dS ratio in comparison to those considered to exhibit simpler social organization."

Kutipan

"Our results demonstrate an elevated dN /dS ratio in termites compared to other members of Blattodea, further generalizing the idea that convergent evolution toward eusociality strongly reduces the effective population size and the genome-wide efficiency of natural selection."
"Furthermore, among termites, species displaying the highest levels of social complexity tend to exhibit higher dN /dS ratio in comparison to those considered to exhibit simpler social organization."

Wawasan Utama Disaring Dari

The impact of social complexity on the efficacy of natural selection in termites

by Roux,C., Wey... pada www.biorxiv.org 04-29-2024

https://www.biorxiv.org/content/10.1101/2024.04.26.591327v2

Pertanyaan yang Lebih Dalam

How do demographic inferences using PSMC-like approaches in non-social species with high dN/dS ratios, such as Cryptocercus, and closely related eusocial groups compare, and could this provide insights into the timing of effective population size variations associated with the emergence of eusociality?

Demographic inferences using PSMC-like (Pairwise Sequential Markovian Coalescent) approaches can provide valuable insights into the historical population dynamics of both non-social species, such as Cryptocercus, and closely related eusocial groups like termites. In non-social species with high dN/dS ratios, such as Cryptocercus wrighti, the elevated dN/dS suggests a relaxation of purifying selection, which may indicate a smaller effective population size (Ne) and a higher accumulation of slightly deleterious mutations. By applying PSMC-like methods, researchers can estimate historical fluctuations in Ne, revealing whether the observed high dN/dS ratios are a result of long-term low Ne or recent demographic changes.
In contrast, closely related eusocial groups, such as termites, may exhibit different demographic patterns due to their complex social structures. The emergence of eusociality is often associated with a significant reduction in Ne, as reproduction is limited to a few individuals within a colony. By comparing the demographic histories of these groups, researchers can gain insights into the timing of Ne variations that coincide with the evolution of eusociality. For instance, if PSMC analyses reveal a historical decline in Ne in both Cryptocercus and eusocial termites, it could suggest that low Ne predates the evolution of eusociality, supporting the hypothesis that high parental care and low Ne facilitate the transition to eusocial structures. Conversely, if eusocial groups show a more pronounced decline in Ne following the emergence of eusociality, it may indicate that social complexity exacerbates the effects of genetic drift, further reducing the efficacy of natural selection.

What are the potential mechanisms by which worker reproduction and indirect selection on worker-specific genes could further contribute to the elevated dN/dS ratios observed in termites with highly specialized worker castes?

Worker reproduction and indirect selection on worker-specific genes can significantly contribute to the elevated dN/dS ratios observed in termites with highly specialized worker castes. In eusocial insects, such as termites, the presence of sterile workers (true workers) limits direct selection on worker-specific genes, as these individuals do not reproduce. Instead, the fitness of these genes is influenced by kin selection, where the reproductive success of related individuals (e.g., the queen and her offspring) indirectly benefits the workers. This indirect selection is generally less effective than direct selection, leading to a higher accumulation of deleterious mutations in worker-specific genes, which can manifest as elevated dN/dS ratios.
Moreover, the specialization of worker castes can create a scenario where certain genes are under relaxed purifying selection due to their limited role in reproduction. As a result, the genetic variation within these worker-specific genes may increase, leading to a higher dN/dS ratio. Additionally, the evolutionary pressures faced by these specialized workers may differ from those acting on reproductive individuals, further contributing to the divergence in selection patterns. The combination of these factors—reduced direct selection, increased genetic drift due to low Ne, and the unique evolutionary pressures on worker castes—can collectively elevate dN/dS ratios in termites with highly specialized worker castes.

Could the patterns observed in termites and other eusocial insects be extended to other forms of complex social organization, such as in social mammals, and what insights could this provide into the general relationship between sociality and genome evolution?

The patterns observed in termites and other eusocial insects may indeed be extended to other forms of complex social organization, including social mammals. In both cases, the evolution of sociality often involves a division of reproductive labor and cooperative care of offspring, which can lead to a reduction in effective population size (Ne) and a corresponding decrease in the efficacy of natural selection. For instance, in social mammals like elephants and certain primates, where social structures are complex and involve cooperative breeding, similar dynamics may be at play. The limited number of breeding individuals within these social groups can result in elevated dN/dS ratios, reflecting a relaxation of purifying selection akin to that observed in eusocial insects.
By examining the genomic consequences of sociality across different taxa, researchers can gain insights into the general relationship between sociality and genome evolution. For example, the presence of high dN/dS ratios in both eusocial insects and social mammals may suggest that complex social structures impose similar evolutionary constraints, leading to analogous patterns of genetic drift and selection. Furthermore, understanding these patterns can illuminate the evolutionary pathways that facilitate the emergence of sociality, highlighting the potential role of kin selection and cooperative behaviors in shaping genomic architectures.
In summary, the comparative analysis of sociality across diverse taxa can enhance our understanding of how complex social structures influence genome evolution, providing a broader context for the observed patterns in termites and other eusocial insects. This perspective underscores the importance of considering sociality as a significant factor in evolutionary biology, with implications for the study of genetic diversity, adaptation, and the evolutionary dynamics of social organisms.