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1. Phylogeny and evolution of the cryptic fungus‐farming ant genus Myrmicocrypta F. Smith (Hymenoptera: Formicidae) inferred from multilocus data

   https://doi.org/10.1111/syen.12313  

   Sosa‐Calvo, Jeffrey; Fernández, Fernando; Schultz, Ted_R (July 2018, Systematic Entomology)

   Abstract Fungus‐farming ants (Hymenoptera: Formicidae) have become model systems for exploring questions regarding the evolution of symbiosis. However, robust phylogenetic studies of both the ant agriculturalists and their fungal cultivars are necessary for addressing whether or not observed ant–fungus associations are the result of coevolution and, if so, whether that coevolution has been strict or diffuse. Here we focus on the evolutionary relationships of the species within the ant genusMyrmicocryptaand of their fungal cultivars. The fungus‐farming ant genusMyrmicocryptawas created by Fr. Smith in 1860 based on a single alate queen. Since then, 31 species and subspecies have been described. Until now, the genus has not received any taxonomic treatment and the relationships of the species within the genus have not been tested. Our molecular analyses, using ∼40 putative species and six protein‐coding (nuclear and mitochondrial) gene fragments, recoverMyrmicocryptaas monophyletic and as the sister group of the genusMycocepurusForel. The speciesM. tuberculataWeber is recovered as the sister to the rest ofMyrmicocrypta. The time‐calibrated phylogeny recovers the age of stem groupMyrmicocryptaplus its sister group as 45 Ma, whereas the inferred age for the crown groupMyrmicocryptais recovered as 27 Ma. Ancestral character‐state analyses suggest that the ancestor ofMyrmicocryptahad scale‐like or squamate hairs and that, although such hairs were once considered diagnostic for the genus, the alternative state of erect simple hairs has evolved at least seven independent times. Ancestral‐state analyses of observed fungal cultivar associations suggest that the most recent common ancestor ofMyrmicocryptacultivated clade 2 fungal species and that switches to clade 1 fungi have occurred at least five times. It is our hope that these results will encourage additional species‐level phylogenies of fungus‐farming ants and their fungal cultivars, which are necessary for understanding the evolutionary processes that gave rise to agriculture in ants and that produced the current diversity of mutualistic ant–fungus interactions. 

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2. Natural history and ecological effects on the establishment and fate of Florida carpenter ant cadavers infected by the parasitic manipulator Ophiocordyceps camponoti ‐ floridani

   https://doi.org/10.1111/1365-2435.14224  

   Will, Ian; Linehan, Sara; Jenkins, David G.; de Bekker, Charissa (November 2022, Functional Ecology)

   Abstract Ophiocordycepsfungi manipulate the behaviour of their ant hosts to produce a summit disease phenotype, thereby establishing infected ant cadavers onto vegetation at elevated positions suitable for fungal growth and transmission. Multiple environmental and ecological factors have been proposed to shape the timing, positioning and outcome of these manipulations.We conducted a long‐term field study ofOphiocordyceps camponoti‐floridaniinfections ofCamponotus floridanusants—the Florida zombie ants. We propose and refine hypotheses on the factors that shape infection outcomes by tracking the occurrence of and fungal growth from hundreds of ant cadavers. We modelled and report these data in relation to weather, light, vegetation and attack by hyperparasites.We investigated environmental factors that could affect the occurrence and location of newly manipulated ant cadavers. New cadaver occurrence was preferentially biased towards epiphyticTillandsiabromeliads, canopy openness and summer weather conditions (an interactive effect of temperature, humidity and precipitation). Furthermore, we suggest that incident light at the individual cadaver level reflects microhabitat choice by manipulated ants or selective pressure on cadaver maintenance for conditions that improve fungal survival.We also asked which environmental conditions affect fungal fitness. Continued fungal development of reproductive structures and putative transmission increased with moist weather conditions (interaction of humidity and precipitation) and canopy openness, while being reduced by hyperparasitic mycoparasite infections. Moreover, under the most open canopy conditions, we found an atypicalOphiocordycepsgrowth morphology that could represent a plastic response to conditions influenced by high light levels.Taken together, we explore general trends and the effects of various ecological conditions on host and parasite disease outcomes in the Florida zombie ant system. These insights from the field can be used to inform experimental laboratory setups that directly test the effects of biotic and abiotic factors on fungus–ant interactions or aim to uncover underlying molecular mechanisms. Read the freePlain Language Summaryfor this article on the Journal blog. 

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3. 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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4. Hijacking time: How Ophiocordyceps fungi could be using ant host clocks to manipulate behavior

   https://doi.org/10.1111/pim.12909  

   de Bekker, Charissa; Das, Biplabendu (February 2022, Parasite Immunology)

   Abstracts Ophiocordycepsfungi manipulate ant behaviour as a transmission strategy. Conspicuous changes in the daily timing of disease phenotypes suggest thatOphiocordycepsand other manipulators could be hijacking the host clock. We discuss the available data that support the notion thatOphiocordycepsfungi could be hijacking ant host clocks and consider how altering daily behavioural rhythms could benefit the fungal infection cycle. By reviewing time‐course transcriptomics data for the parasite and the host, we argue thatOphiocordycepshas a light‐entrainable clock that might drive daily expression of candidate manipulation genes. Moreover, ant rhythms are seemingly highly plastic and involved in behavioural division of labour, which could make them susceptible to parasite hijacking. To provisionally test whether the expression of ant behavioural plasticity and rhythmicity genes could be affected by fungal manipulation, we performed a gene co‐expression network analysis on ant time‐course data and linked it to available behavioural manipulation data. We found that behavioural plasticity genes reside in the same modules as those affected during fungal manipulation. These modules showed significant connectivity with rhythmic gene modules, suggesting thatOphiocordycepscould be indirectly affecting the expression of those genes as well. 

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5. Hawaiian larval stomatopods: molecular and morphological diversity

   https://doi.org/10.11646/zootaxa.5214.2.5  

   STECK, MIREILLE; WINNICKI, ELIZABETH; KOBAYASHI, DONALD R.; WHITNEY, JONATHAN L.; AHYONG, SHANE T.; PORTER, MEGAN L. (December 2022, Zootaxa)

   Estimating stomatopod species diversity using morphology alone has long been difficult; though over 450 species have been described, new species are still being discovered regularly despite the cryptic behaviors of adults. However, the larvae of stomatopods are more easily obtained due to their pelagic habitat, and have been the focus of recent studies of diversity. Studies of morphological diversity describe both conserved and divergent traits in larval stomatopods, but generally cannot be linked to a particular species. Conversely, genetic studies of stomatopod larvae using DNA barcoding can be used to estimate species diversity, but are generally not linked to known species by analyses of morphological characters. Here we combine these two approaches, larval morphology and genetics, to estimate stomatopod species diversity in the Hawaiian Islands. Over 22 operational taxonomic units (OTUs) were identified genetically, corresponding to 20 characterized morphological types. Species from three major superfamilies of stomatopod were identified: Squilloidea (4 OTUs, 3 morphotypes), Gonodactyloidea (9, 8), and Lysiosquilloidea (6, 7). Among these, lysiosquilloids were more diverse based on larval morphotypes and OTUs as compared to previously documented Hawaiian species (3), while squilloids had a lower diversity of species represented by collected larvae as compared to the seven species previously documented. Two OTUs / morphotypes could not be identified to superfamily as their molecular and morphological features did not closely match any available information, suggesting they belong to poorly sampled superfamilies. The pseudosquillid, Pseudosquillana richeri, was discovered for the first time from Hawaiʻi. This study contributes an updated estimate for Hawaiian stomatopod diversity for a total of 24 documented species, provides references for identification of larval stomatopods across the three major superfamilies, and emphasizes the lack of knowledge of species diversity in more cryptic stomatopod superfamilies, such as Lysiosquilloidea.   

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