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Abstract A rapid proliferation in the availability of whole genome sequences (WGS), often with relatively low read depth, offers an unprecedented opportunity for phylogenomic advances using publicly available data, but there are several key challenges in applying these data. Using low‐coverage WGS data for the ant species ofFormica, we conducted detailed comparisons on two different analytical pipelines (reference‐based vs. de novo genome assembly), four types of datasets (5‐kbp‐window, ultra‐conserved element [UCE], single‐copy ortholog [BUSCO] and mitogenome), and a series of analytical procedures (e.g. concatenation vs. coalescent analyses) to identify which are robust to typical WGS data. The results show that at a shallow scale of phylogenetic relationships of closely related species 5‐kbp‐windows from the reference‐based pipeline and UCEs from the de novo assemblies are more successful than the BUSCOs in recovering informative markers for phylogenetic inference. Compared with concatenation analyses, coalescent analyses often resulted in disparate deeper relationships in the phylogeny. This study also uncovers evident mito‐nuclear discordance and demonstrates genome‐wide gene conflicts in phylogenetic signals, both pointing to possible incomplete lineage sorting and/or hybridization during the early, rapid radiation ofFormicaants. Divergence dating analyses show that different types of data and analytical methods could result in inconsistent time estimates, highlighting the potential need for multiple approaches to better understand species divergence. The strengths and weaknesses of different analytical pipelines and strategies are discussed. Findings from this study provide valuable insights for large‐scale phylogenomic projects using WGS data. 

Abstract The study of social parasitism faces numerous challenges arising from the intricate and intranidal host–parasite interactions and the rarity of parasites compared to their free-living counterparts. As a result, our understanding of the ecology and evolution of most social parasites remains limited. Using whole-genome and reduced-representation sequence data, we conducted a study to fill knowledge gaps on host use, colony social structure, and population genetics of the facultative dulotic ant Formica aserva Forel. Our study reveals the remarkable ability of F. aserva to exploit at least 20 different host species across its wide geographic distribution. In some cases, one social parasite colony exploits multiple hosts simultaneously, suggesting a high degree of generalization even at a local spatial scale. Approximately 80% of the colonies were monogyne (with a single queen), with many exhibiting higher rates of polyandry compared to most Formica ants. Although we identified a supergene on chromosome 3, its association with colony structure remains uncertain due to the rarity of polygyny in our sample. Population genetic analyses reveal substantial geographic population structure, with the greatest divergence between California populations and those from the rest of the range. Mitochondrial population structure differs from structure inferred from the nuclear genome on a broad geographic scale, suggesting a possible role of adaptive introgression or genetic drift. This study provides valuable insights into the ecology and evolution of F. aserva, underscoring the need for further research to decipher the complexities of host interactions and the genetic mechanisms that regulate social structure. 

Abstract Most supergenes discovered so far are young, occurring in one species or a few closely related species. An ancient supergene in the ant genusFormicapresents an unusual opportunity to compare supergene‐associated phenotypes and the factors that influence the persistence of polymorphism in different species. We investigate the genetic architecture of social organization inFormica francoeuri, an ant species native to low‐ and mid‐elevation semiarid regions of southern California, and describe an efficient technique for estimating mode of social organization using population genomic data. Using this technique, we show thatF. francoeuriexhibits polymorphism in colony social organization and that the phenotypic polymorphism is strongly associated with genotypes within theFormicasocial supergene region. The distribution of supergene haplotypes inF. francoeuridiffers from that of related speciesFormica selysiin that colonies with multiple queens contain almost exclusively workers that are heterozygous for alternative supergene haplotypes. Moreover, heterozygous workers exhibit allele‐specific expression of the polygyne‐associated haplotype at the candidate geneKnockout,which is thought to influence social organization. We also report geographic population structure and variation in worker size across a large fraction of the species range. Our results suggest that, although theFormicasupergene is conserved within the genus, the mechanisms that maintain the supergene and its associated polymorphisms differ among species. 

Abstract Supergenes, regions of the genome with suppressed recombination between sets of functional mutations, contribute to the evolution of complex phenotypes in diverse systems. Excluding sex chromosomes, most supergenes discovered so far appear to be young, being found in one species or a few closely related species. Here, we investigate how a chromosome harbouring an ancient supergene has evolved over about 30 million years (Ma). TheFormicasupergene underlies variation in colony queen number in at least five species. We expand previous analyses of sequence divergence on this chromosome to encompass about 90 species spanning theFormicaphylogeny. Within the nonrecombining region, the geneknockoutcontains 22 single nucleotide polymorphisms (SNPs) that are consistently differentiated between two alternative supergene haplotypes in divergent EuropeanFormicaspecies, and we show that these same SNPs are present in mostFormicaclades. In these clades, including an early diverging NearcticFormicaclade, individuals with alternative genotypes atknockoutalso have higher differentiation in other portions of this chromosome. We identify hotspots of SNPs along this chromosome that are present in multipleFormicaclades to detect genes that may have contributed to the emergence and maintenance of the genetic polymorphism. Finally, we infer three gene duplications on one haplotype, based on apparent heterozygosity within these genes in the genomes of haploid males. This study strengthens the evidence that this supergene originated early in the evolution ofFormicaand that just a few loci in this large region of suppressed recombination retain strongly differentiated alleles across contemporaryFormicalineages. 

Antagonistic selection has long been considered a major driver of the formation and expansion of sex chromosomes. For example, sexually antagonistic variation on an autosome can select for suppressed recombination between that autosome and the sex chromosome, leading to a neo-sex chromosome. Autosomal supergenes, chromosomal regions containing tightly linked variants affecting the same complex trait, share similarities with sex chromosomes, raising the possibility that sex chromosome evolution models can explain the evolution of genome structure and recombination in other contexts. We tested this premise in a Formica ant species wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. We discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is in strong linkage disequilibrium with one chromosome 3 haplotype (P2) found in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single queen (monogyne) background, and thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social ‘environments’ (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen-size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We propose that miniaturized queens, 16-20% smaller than queens without 9r, could be incipient intraspecific social parasites. 

Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent–offspring conflict, genomic conflict, and cooperative breeding. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work predicted that worker control of sex ratio and variation in relatedness asymmetry among colonies would cause each colony to specialize in the production of one sex. While some empirical tests supported theoretical predictions, others deviated from them, leaving many questions about how split sex ratio emerges. One factor yet to be investigated is whether colony sex ratio may be influenced by the genotypes of queens or workers. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens future research on the evolutionary drivers of split sex ratio.