Causes and consequences of a complex recombinational landscape in the ant Cardiocondyla obscurior.

Eusocial Hymenoptera have the highest recombination rates among all multicellular animals studied so far, but it is unclear why this is and how this affects the biology of individual species. A high-resolution linkage map for the ant Cardiocondyla obscurior corroborates genome-wide high recombination rates reported for ants (8.1 cM/Mb). However, recombination is locally suppressed in regions that are enriched with TEs, that have strong haplotype divergence, or that show signatures of epistatic selection in C. obscurior The results do not support the hypotheses that high recombination rates are linked to phenotypic plasticity or to modulating selection efficiency. Instead, genetic diversity and the frequency of structural variants correlate positively with local recombination rates, potentially compensating for the low levels of genetic variation expected in haplodiploid social Hymenoptera with low effective population size. Ultimately, the data show that recombination contributes to within-population polymorphism and to the divergence of the lineages within C. obscurior.

Evolutionary genomics of socially polymorphic populations of Pogonomyrmex californicus.

BACKGROUND: Social insects vary considerably in their social organization both between and within species. In the California harvester ant, Pogonomyrmex californicus (Buckley 1867), colonies are commonly founded and headed by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), unrelated queens cooperate not only during founding (pleometrosis) but also throughout the life of the colony (primary polygyny). The genetic architecture and evolutionary dynamics of this complex social niche polymorphism (haplometrosis vs pleometrosis) have remained unknown. RESULTS: We provide a first analysis of its genomic basis and evolutionary history using population genomics comparing individuals from a haplometrotic population to those from a pleometrotic population. We discovered a recently evolved (< 200 k years), 8-Mb non-recombining region segregating with the observed social niche polymorphism. This region shares several characteristics with supergenes underlying social polymorphisms in other socially polymorphic ant species. However, we also find remarkable differences from previously described social supergenes. Particularly, four additional genomic regions not in linkage with the supergene show signatures of a selective sweep in the pleometrotic population. Within these regions, we find for example genes crucial for epigenetic regulation via histone modification (chameau) and DNA methylation (Dnmt1). CONCLUSIONS: Altogether, our results suggest that social morph in this species is a polygenic trait involving a potential young supergene. Further studies targeting haplo- and pleometrotic individuals from a single population are however required to conclusively resolve whether these genetic differences underlie the alternative social phenotypes or have emerged through genetic drift.

Inhibition of HSP90 causes morphological variation in the invasive ant Cardiocondyla obscurior.

Canalization underlies the expression of steady phenotypes in the face of unsteady environmental conditions or varying genetic backgrounds. The chaperone HSP90 has been identified as a key component of the molecular machinery regulating canalization and a growing body of research suggests that HSP90 could act as a general capacitator in evolution. However, empirical data about HSP90-dependent phenotypic variation and its evolutionary impact is still scarce, particularly for non-model species. Here we report how pharmacological suppression of HSP90 increases morphological variation up to 87% in the invasive ant Cardiocondyla obscurior. We show that workers treated with the HSP90 inhibitor 17-DMAG are significantly more diverse compared to untreated workers in two of four measured traits: maximal eye distance and maximal propodeal spine distance. We further find morphological differentiation between natural populations of C. obscurior in the same traits that responded to our pharmacological treatment. These findings add support for the putative impact of HSP90 on canalization, the modularity of phenotypic traits, and its potential role in morphological evolution of ants.

Transposable elements and introgression introduce genetic variation in the invasive ant Cardiocondyla obscurior.

Introduced populations of invasive organisms have to cope with novel environmental challenges, while having reduced genetic variation caused by founder effects. The mechanisms associated with this "genetic paradox of invasive species" has received considerable attention, yet few studies have examined the genomic architecture of invasive species. Populations of the heart node ant Cardiocondyla obscurior belong to two distinct lineages, a New World lineage so far only found in Latin America and a more globally distributed Old World lineage. In the present study, we use population genomic approaches to compare populations of the two lineages with apparent divergent invasive potential. We find that the strong genetic differentiation of the two lineages began at least 40,000 generations ago and that activity of transposable elements (TEs) has contributed significantly to the divergence of both lineages, possibly linked to the very unusual genomic distribution of TEs in this species. Furthermore, we show that introgression from the Old World lineage is a dominant source of genetic diversity in the New World lineage, despite the lineages' strong genetic differentiation. Our study uncovers mechanisms underlying novel genetic variation in introduced populations of C. obscurior that could contribute to the species' adaptive potential.

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum.

BACKGROUND: Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. RESULTS: We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes. CONCLUSIONS: These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.