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1. Genomic insights into the evolution of secondary metabolism of Escovopsis and its allies, specialized fungal symbionts of fungus-farming ants

   https://doi.org/10.1128/msystems.00576-24  

   Berasategui, Aileen; Salem, Hassan; Moller, Abraham G; Christopher, Yuliana; Vidaurre_Montoya, Quimi; Conn, Caitlin; Read, Timothy D; Rodrigues, Andre; Ziemert, Nadine; Gerardo, Nicole (July 2024, mSystems)

   The metabolic intimacy of symbiosis often demands the work of specialists. Natural products and defensive secondary metabolites can drive specificity by ensuring infection and propagation across host generations. But in contrast to bacteria, little is known about the diversity and distribution of natural product biosynthetic pathways among fungi and how they evolve to facilitate symbiosis and adaptation to their host environment. In this study, we define the secondary metabolism of Escovopsis and closely related genera, symbionts in the gardens of fungus-farming ants. We ask how the gain and loss of various biosynthetic pathways correspond to divergent lifestyles. Long-read sequencing allowed us to define the chromosomal features of representative Escovopsis strains, revealing highly reduced genomes composed of seven to eight chromosomes. The genomes are highly syntenic with macrosynteny decreasing with increasing phylogenetic distance, while maintaining a high degree of mesosynteny. An ancestral state reconstruction analysis of biosynthetic pathways revealed that, while many secondary metabolites are shared with non-ant-associated Sordariomycetes, 56 pathways are unique to the symbiotic genera. Reflecting adaptation to diverging ant agricultural systems, we observe that the stepwise acquisition of these pathways mirrors the ecological radiations of attine ants and the dynamic recruitment and replacement of their fungal cultivars. As different clades encode characteristic combinations of biosynthetic gene clusters, these delineating profiles provide important insights into the possible mechanisms underlying specificity between these symbionts and their fungal hosts. Collectively, our findings shed light on the evolutionary dynamic nature of secondary metabolism in Escovopsis and its allies, reflecting adaptation of the symbionts to an ancient agricultural system.Microbial symbionts interact with their hosts and competitors through a remarkable array of secondary metabolites and natural products. Here, we highlight the highly streamlined genomic features of attine-associated fungal symbionts. The genomes of Escovopsis species, as well as species from other symbiont genera, many of which are common with the gardens of fungus-growing ants, are defined by seven chromosomes. Despite a high degree of metabolic conservation, we observe some variation in the symbionts’ potential to produce secondary metabolites. As the phylogenetic distribution of the encoding biosynthetic gene clusters coincides with attine transitions in agricultural systems, we highlight the likely role of these metabolites in mediating adaptation by a group of highly specialized symbionts. 

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2. Evolutionary déjà vu? A case of convergent evolution in an ant–plant association

   https://doi.org/10.1098/rspb.2024.1214  

   Probst, Rodolfo S; Longino, John T; Branstetter, Michael G (July 2024, Proceedings of the Royal Society B: Biological Sciences)

   Obligatory ant–plant symbioses often appear to be single evolutionary shifts within particular ant lineages; however, convergence can be revealed once natural history observations are complemented with molecular phylogenetics. Here, we describe a remarkable example of convergent evolution in an ant–plant symbiotic system. Exclusively arboreal,Myrmelachistaspecies can be generalized opportunists nesting in several plant species or obligately symbiotic, live-stem nesters of a narrow set of plant species. Instances of specialization withinMyrmelachistaare known from northern South America and throughout Middle America. In Middle America, a diverse radiation of specialists occupies understory treelets of lowland rainforests. The morphological and behavioural uniformity of specialists suggests that they form a monophyletic assemblage, diversifying after a single origin of specialization. Using ultraconserved element phylogenomics and ancestral state reconstructions, we show that shifts from opportunistic to obligately symbiotic evolved independently in South and Middle America. Furthermore, our analyses support a remarkable case of convergence within the Middle American radiation, with two independently evolved specialist clades, arising nearly simultaneously from putative opportunistic ancestors during the late Pliocene. This repeated evolution of a complex phenotype suggests similar mechanisms behind trait shifts from opportunists to specialists, generating further questions about the selective forces driving specialization. 

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3. Context dependence in the symbiosis between Dictyostelium discoideum and Paraburkholderia

   https://doi.org/10.1002/evl3.281  

   Scott, Trey J.; Queller, David C.; Strassmann, Joan E. (June 2022, Evolution Letters)

   Abstract Symbiotic interactions change with environmental context. Measuring these context-dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, where the context is the abundance of host food bacteria. Paraburkholderia have been shown to harm hosts dispersed to food-rich environments, but aid hosts dispersed to food-poor environments by allowing hosts to carry food bacteria. Through measuring symbiont density and host spore production, we show that this food context matters in three other ways. First, it matters for symbionts, who suffer a greater cost from competition with food bacteria in the food-rich context. Second, it matters for host-symbiont conflict, changing how symbiont density negatively impacts host spore production. Third, data-based simulations show that symbiosis often provides a long-term fitness advantage for hosts after rounds of growth and dispersal in variable food contexts, especially when conditions are harsh with little food. These results show how food context can have many consequences for the Dictyostelium-Paraburkholderia symbiosis and that both sides can frequently benefit. 

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4. Myrmecophily among mesostigmatid mites

   https://doi.org/10.1007/s00040-024-01003-z  

   Klompen, H.; Campbell, K_U (October 2024, Insectes Sociaux)

   Abstract Ant nests are biodiversity hot spots, concentrating resources from a wide area that can be exploited by other organisms, known as myrmecophiles. The mite order Mesostigmata includes a wide range of lineages that have become myrmecophiles with many species reliant on ant nests for at least part of their development. The nature of the associations is quite variable, including predators of smaller arthropods in the nest (close to the ancestral lifestyle of these mites), scavengers, kleptoparasites, parasites, and parasitoids. A few mite species show extreme modifications of morphological and/or developmental patterns, others show almost none. Some host specificity is common but one-on-one host specialization is rare or poorly tested. Phoresy on the ants is common, but the target ant caste varies with the goal of phoresy. In general, the diversity of mesostigmatid mites in the nest of a given ant species is affected by habitat conditions along with a range of life history characteristics of the ants, including factors such as body size, colony size, colony founding mode, social parasitism, and nest density. Unfortunately, the life history of the majority of mites associated with ants is still unknown. 

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5. The genomic and cellular basis of biosynthetic innovation in rove beetles

   Kitchen, S.A; Naragon, T.H.; Brückner, A. Ladinsky; Quinodoz, S.A.; Badroos, J.M.; Viliunas, J.W.; Wagner, J.M.; Miller, D.R.; Yousefelahiyeh, M.; Antoshechkin, I.A.; et al (May 2023, bioRxiv)

   How evolution at the cellular level potentiates change at the macroevolutionary level is a major question in evolutionary biology. With >66,000 described species, rove beetles (Staphylinidae) comprise the largest metazoan family. Their exceptional radiation has been coupled to pervasive biosynthetic innovation whereby numerous lineages bear defensive glands with diverse chemistries. Here, we combine comparative genomic and single-cell transcriptomic data from across the largest rove beetle clade, Aleocharinae. We retrace the functional evolution of two novel secretory cell types that together comprise the tergal gland—a putative catalyst behind Aleocharinae’s megadiversity. We identify key genomic contingencies that were critical to the assembly of each cell type and their organ-level partnership in manufacturing the beetle’s defensive secretion. This process hinged on evolving a mechanism for regulated production of noxious benzoquinones that appears convergent with plant toxin release systems, and synthesis of an effective benzoquinone solvent that weaponized the total secretion. We show that this cooperative biosynthetic system arose at the Jurassic-Cretaceous boundary, and that following its establishment, both cell types underwent ∼150 million years of stasis, their chemistry and core molecular architecture maintained almost clade-wide as Aleocharinae radiated globally into tens of thousands of lineages. Despite this deep conservation, we show that the two cell types have acted as substrates for the emergence of adaptive, biochemical novelties—most dramatically in symbiotic lineages that have infiltrated social insect colonies and produce host behavior-manipulating secretions. Our findings uncover genomic and cell type evolutionary processes underlying the origin, functional conservation and evolvability of a chemical innovation in beetles. 

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