Trends in Genetics
ReviewThe genomic impact of 100 million years of social evolution in seven ant species
Section snippets
Ant genomes: tools to study biological and social complexity
Ants (Hymenoptera, Formicidae; see Glossary) comprise a dominant component of most terrestrial habitats. The more than 14000 described species (http://www.antweb.org) show an enormous diversity in life-history features, ecological and behavioral adaptations and social organization, and are a prime example of a complex adaptive system 1, 2, 3, 4, 5. Current evidence suggests that the last common ancestor of the ants lived during the Jurassic and Cretaceous periods, 140–168 million years ago
Genomic and genetic features of the seven sequenced ant species
The use of different sequencing technologies and depth of coverage across the sequenced ant species (10.5–123×) has yielded genome assemblies with a ten-fold range of median scaffold sizes (N50 from 598 kb to 5154 kb; Table 2). The overall size of these genomes ranges from 250 Mb to 753 Mb, and most of the variation in genome size is attributable to differences in repetitive element content (Table 2). Solenopsis invicta is the largest ant genome sequenced (353 Mb assembled) [17] and, although no
Epigenetic control of caste determination
DNA methylation and histone modifications contribute to gene expression regulation and can be stably transmitted between cell division events [39]. Unlike genetic information, which changes slowly over the course of multiple generations, such epigenetic information can change quickly within an individual in response to changing environmental conditions (e.g. temperature, diet, and stress). Although an individual is only endowed with one nuclear genome, it can have multiple epigenomes that
Genetic control of caste programs
Pogonomyrmex barbatus promises the most insight into the genetic and epigenetic factors influencing caste determination because it is the only sequenced ant species known to use both environmental (ECD) and genetic forms of caste determination (GCD). Hence, genetic markers allow queen- or worker-destined individuals to be distinguished regardless of developmental stage 45, 46. This makes it possible to analyze stage-specific expression data, allowing for the identification of the developmental
Concluding remarks and future perspectives
The release of seven sequenced ant genomes and the development of new genomic tools for ants has laid the groundwork for an exciting new era of socio- and ant genomics 13, 14. It is now possible to study the molecular basis of social behavior in a second taxon that evolved eusociality independently from the honeybee lineage. The first analysis of the seven ant genomes revealed that ants have a different sociogenome compared with that of the honeybee and that there is also significant variation
Acknowledgments
The authors would like to thank Alex Wild and Myrmecos.net for providing images of the sequenced ant species used in Figure 1. JG and CRS were supported by a grant from the NSF (IOS-0920732). CDS was supported by a grant from the NIMH (5SC2MH086071). DS is supported by a Howard Hughes Medical Institute Collaborative Innovation Award #200900 to D. Reinberg, S. Berger, and J. Liebig. YW was supported by a European Research Council grant to Laurent Keller and JR was supported by a Swiss NSF grant
Glossary
- Caste
- a subset of individuals in an insect colony that are characterized either behaviorally or morphologically.
- Environmental caste determination (ECD)
- the differentiation between queens and worker castes is determined by environmental factors, such as exposure to hormones, temperature, or alternate food sources. This is thought to be the main mechanism of caste determination across eusocial species.
- Epigenetics
- the study of heritable molecular differences resulting in a measurable phenotype that
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2022, Current Topics in Developmental BiologyCitation Excerpt :The social Hymenoptera—ants, bees, and wasps—are emerging as valuable models for the study of molecular processes … Abouheif and Wray now formally welcome ants into the vigorous field of “evo-devo” with a fascinating description of changes in gene expression that are associated with the evolution of the wingless worker caste … The heightened interest in social insects reflects the sense that the time has come to develop a comprehensive understanding in molecular terms of social life: how it evolved, how it is governed, and how it influences all aspects of genome structure, gene expression and organismal development, physiology and behavior.” Fast forward 20 years, ant researchers have now sequenced over 100 ant genomes from almost every major subfamily (Boomsma et al., 2017; Gadau et al., 2012), they have developed cutting edge tools to manipulate gene expression during development (reviewed in Sieriebriennikov, Reinberg, and Desplan (2021), including CRISPR (Chiu, Hsu, Chang, Huang, & Wang, 2020; Trible et al., 2017; Yan et al., 2017), RNAi (Rajakumar et al., 2018; Ratzka, Gross, & Feldhaar, 2013), transgenics (Sieriebriennikov et al., 2021) and pharmacological inhibitors (Alvarado, Rajakumar, Abouheif, & Szyf, 2015; Fetter-Pruneda et al., 2021)). Researchers are increasingly combining these molecular tools with colony-level manipulations––what E.O. Wilson has called the “pseudo-mutant” approach (Wilson, 1985).
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