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1. Worker Reproduction and Caste Polymorphism Impact Genome Evolution and Social Genes Across the Ants

   https://doi.org/10.1093/gbe/evad095  

   Barkdull, Megan ; Moreau, Corrie S. ; Webster, ed., Matthew ( May 2023 , Genome Biology and Evolution)

   Eusocial insects are characterized by several traits, including reproductive division of labor and caste polymorphisms, which likely modulate genome evolution. Concomitantly, evolution may act on specific genes and pathways underlying these novel, sociality-associated phenotypes. Reproductive division of labor should increase the magnitude of genetic drift and reduce the efficacy of selection by reducing effective population size. Caste polymorphism has been associated with relaxed selection and may facilitate directional selection on caste-specific genes. Here, we use comparative analyses of 22 ant genomes to test how reproductive division of labor and worker polymorphism influence positive selection and selection intensity across the genome. Our results demonstrate that worker reproductive capacity is associated with a reduction in the degree of relaxed selection but is not associated with any significant change to positive selection. We find decreases in positive selection in species with polymorphic workers, but no increase in the degree of relaxed selection. Finally, we explore evolutionary patterns in specific candidate genes associated with our focal traits in eusocial insects. Two oocyte patterning genes previously implicated in worker sterility evolve under intensified selection in species with reproductive workers. Behavioral caste genes generally experience relaxed selection associated with worker polymorphism, whereas vestigial and spalt, both associated with soldier development in Pheidole ants, experience intensified selection in worker polymorphic species. These findings expand our understanding of the genetic mechanisms underlying elaborations of sociality. The impacts of reproductive division of labor and caste polymorphisms on specific genes illuminate those genes’ roles in generating complex eusocial phenotypes.

    

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2. Decoupled evolution of mating biology and social structure in Acromyrmex leaf-cutting ants

   https://doi.org/10.1007/s00265-021-03113-1  

   Dahan, Romain A. ; Grove, Nathan K. ; Bollazzi, Martin ; Gerstner, Benjamin P. ; Rabeling, Christian ( December 2021 , Behavioral Ecology and Sociobiology)

   Insect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants.Acromyrmexleaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South AmericanAcromyrmexspecies to study how different selective pressures influence the evolution of polygyny and polyandry. We show thatAcromyrmexspecies exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species,Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species,A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution inAcromyrmexleaf-cutting ants.

   Many species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.

    

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3. Genome, transcriptome and methylome sequencing of a primitively eusocial wasp reveal a greatly reduced DNA methylation system in a social insect

   https://doi.org/10.1111/mec.13578  

   Standage, Daniel S. ; Berens, Ali J. ; Glastad, Karl M. ; Severin, Andrew J. ; Brendel, Volker P. ; Toth, Amy L. ( March 2016 , Molecular Ecology)

   Comparative genomics of social insects has been intensely pursued in recent years with the goal of providing insights into the evolution of social behaviour and its underlying genomic and epigenomic basis. However, the comparative approach has been hampered by a paucity of data on some of the most informative social forms (e.g. incipiently and primitively social) and taxa (especially members of the wasp family Vespidae) for studying social evolution. Here, we provide a draft genome of the primitively eusocial model insectPolistes dominula, accompanied by analysis of caste‐related transcriptome and methylome sequence data for adult queens and workers.Polistes dominulapossesses a fairly typical hymenopteran genome, but shows very low genomewideGCcontent and some evidence of reduced genome size. We found numerous caste‐related differences in gene expression, with evidence that both conserved and novel genes are related to caste differences. Most strikingly, these –omics data reveal a major reduction in one of the major epigenetic mechanisms that has been previously suggested to be important for caste differences in social insects:DNAmethylation. Along with a conspicuous loss of a key gene associated with environmentally responsiveDNAmethylation (the de novoDNAmethyltransferaseDnmt3), these wasps have greatly reduced genomewide methylation to almost zero. In addition to providing a valuable resource for comparative analysis of social insect evolution, our integrative –omics data for this important behavioural and evolutionary model system call into question the general importance ofDNAmethylation in caste differences and evolution in social insects.

    

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4. Biogeography and evolution of social parasitism in Australian Myrmecia bulldog ants revealed by phylogenomics

   Mera-Rodríguez LD, Jourdan H ( May 2023 , Molecular phylogenetics and evolution)

   Studying the historical biogeography and life history transitions from eusocial colony life to social parasitism contributes to our understanding of the evolutionary mechanisms generating biodiversity in eusocial insects. The ants in the genus Myrmecia are a well-suited system for testing evolutionary hypotheses about how their species diversity was assembled through time because the genus is endemic to Australia with the single exception of the species M. apicalis inhabiting the Pacific Island of New Caledonia, and because at least one social parasite species exists in the genus. However, the evolutionary mechanisms underlying the disjunct biogeographic distribution of M. apicalis and the life history transition(s) to social parasitism remain unexplored. To study the biogeographic origin of the isolated, oceanic species M. apicalis and to reveal the origin and evolution of social parasitism in the genus, we reconstructed a comprehensive phylogeny of the ant subfamily Myrmeciinae. We utilized Ultra Conserved Elements (UCEs) as molecular markers to generate a molecular genetic dataset consisting of 2,287 loci per taxon on average for 66 out of the 93 known Myrmecia species as well as for the sister lineage Nothomyrmecia macrops and selected outgroups. Our time-calibrated phylogeny inferred that: (i) stem Myrmeciinae originated during the Paleocene ~ 58 Ma ago; (ii) the current disjunct biogeographic distribution of M. apicalis was driven by long-distance dispersal from Australia to New Caledonia during the Miocene ~ 14 Ma ago; (iii) the single social parasite species, M. inquilina, evolved directly from one of the two known host species, M. nigriceps, in sympatry via the intraspecific route of social parasite evolution; and (iv) 5 of the 9 previously established taxonomic species groups are non-monophyletic. We suggest minor changes to reconcile the molecular phylogenetic results with the taxonomic classification. Our study enhances our understanding of the evolution and biogeography of Australian bulldog ants, contributes to our knowledge about the evolution of social parasitism in ants, and provides a solid phylogenetic foundation for future inquiries into the biology, taxonomy, and classification of Myrmeciinae. 

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5. Complete genomic and epigenetic maps of human centromeres

   https://doi.org/10.1126/science.abl4178  

   Altemose, Nicolas ; Logsdon, Glennis A. ; Bzikadze, Andrey V. ; Sidhwani, Pragya ; Langley, Sasha A. ; Caldas, Gina V. ; Hoyt, Savannah J. ; Uralsky, Lev ; Ryabov, Fedor D. ; Shew, Colin J. ; et al ( April 2022 , Science)

   INTRODUCTION To faithfully distribute genetic material to daughter cells during cell division, spindle fibers must couple to DNA by means of a structure called the kinetochore, which assembles at each chromosome’s centromere. Human centromeres are located within large arrays of tandemly repeated DNA sequences known as alpha satellite (αSat), which often span millions of base pairs on each chromosome. Arrays of αSat are frequently surrounded by other types of tandem satellite repeats, which have poorly understood functions, along with nonrepetitive sequences, including transcribed genes. Previous genome sequencing efforts have been unable to generate complete assemblies of satellite-rich regions because of their scale and repetitive nature, limiting the ability to study their organization, variation, and function. RATIONALE Pericentromeric and centromeric (peri/centromeric) satellite DNA sequences have remained almost entirely missing from the assembled human reference genome for the past 20 years. Using a complete, telomere-to-telomere (T2T) assembly of a human genome, we developed and deployed tailored computational approaches to reveal the organization and evolutionary patterns of these satellite arrays at both large and small length scales. We also performed experiments to map precisely which αSat repeats interact with kinetochore proteins. Last, we compared peri/centromeric regions among multiple individuals to understand how these sequences vary across diverse genetic backgrounds. RESULTS Satellite repeats constitute 6.2% of the T2T-CHM13 genome assembly, with αSat representing the single largest component (2.8% of the genome). By studying the sequence relationships of αSat repeats in detail across each centromere, we found genome-wide evidence that human centromeres evolve through “layered expansions.” Specifically, distinct repetitive variants arise within each centromeric region and expand through mechanisms that resemble successive tandem duplications, whereas older flanking sequences shrink and diverge over time. We also revealed that the most recently expanded repeats within each αSat array are more likely to interact with the inner kinetochore protein Centromere Protein A (CENP-A), which coincides with regions of reduced CpG methylation. This suggests a strong relationship between local satellite repeat expansion, kinetochore positioning, and DNA hypomethylation. Furthermore, we uncovered large and unexpected structural rearrangements that affect multiple satellite repeat types, including active centromeric αSat arrays. Last, by comparing sequence information from nearly 1600 individuals’ X chromosomes, we observed that individuals with recent African ancestry possess the greatest genetic diversity in the region surrounding the centromere, which sometimes contains a predominantly African αSat sequence variant. CONCLUSION The genetic and epigenetic properties of centromeres are closely interwoven through evolution. These findings raise important questions about the specific molecular mechanisms responsible for the relationship between inner kinetochore proteins, DNA hypomethylation, and layered αSat expansions. Even more questions remain about the function and evolution of non-αSat repeats. To begin answering these questions, we have produced a comprehensive encyclopedia of peri/centromeric sequences in a human genome, and we demonstrated how these regions can be studied with modern genomic tools. Our work also illuminates the rich genetic variation hidden within these formerly missing regions of the genome, which may contribute to health and disease. This unexplored variation underlines the need for more T2T human genome assemblies from genetically diverse individuals. Gapless assemblies illuminate centromere evolution. ( Top ) The organization of peri/centromeric satellite repeats. ( Bottom left ) A schematic portraying (i) evidence for centromere evolution through layered expansions and (ii) the localization of inner-kinetochore proteins in the youngest, most recently expanded repeats, which coincide with a region of DNA hypomethylation. ( Bottom right ) An illustration of the global distribution of chrX centromere haplotypes, showing increased diversity in populations with recent African ancestry. 

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