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1. Multiomic interpretation of fungus-infected ant metabolomes during manipulated summit disease

   https://doi.org/10.1038/s41598-023-40065-0  

   Will, I. ; Attardo, G. M. ; de Bekker, C. ( September 2023 , Scientific Reports)

   Camponotus floridanusants show altered behaviors followed by a fatal summiting phenotype when infected with manipulatingOphiocordyceps camponoti-floridanifungi. Host summiting as a strategy to increase transmission is also observed with parasite taxa beyond fungi, including aquatic and terrestrial helminths and baculoviruses. The drastic phenotypic changes can sometimes reflect significant molecular changes in gene expression and metabolite concentrations measured in manipulated hosts. Nevertheless, the underlying mechanisms still need to be fully characterized. To investigate the small molecules producing summiting behavior, we infectedC. floridanusants withO. camponoti-floridaniand sampled their heads for LC–MS/MS when we observed the characteristic summiting phenotype. We link this metabolomic data with our previous genomic and transcriptomic data to propose mechanisms that underlie manipulated summiting behavior in “zombie ants.” This “multiomic” evidence points toward the dysregulation of neurotransmitter levels and neuronal signaling. We propose that these processes are altered during infection and manipulation based on (1) differential expression of neurotransmitter synthesis and receptor genes, (2) altered abundance of metabolites and neurotransmitters (or their precursors) with known behavioral effects in ants and other insects, and (3) possible suppression of a connected immunity pathway. We additionally report signals for metabolic activity during manipulation related to primary metabolism, detoxification, and anti-stress protectants. Taken together, these findings suggest that host manipulation is likely a multi-faceted phenomenon, with key processes changing at multiple levels of molecular organization.

    

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2. Plant killing by Neotropical acacia ants: ecology, decision‐making, and head morphology

   https://doi.org/10.1111/btp.12695  

   Amador‐Vargas, Sabrina ( September 2019 , Biotropica)

   Mutualistic species often associate with several partners that vary in the benefits provided. In some protective ant–plant mutualisms, ants vary in the extent at which they kill neighboring vegetation. Particularly, in acacia ants (Pseudomyrmex), the area around the host tree that ants keep free from vegetation (“clearings”) vary depending on the species. This study assessed whether interspecific variation in clearing size corresponds to workers biting on plant tissue of different thickness. As expected, workers from species making the largest clearings bit more often on thicker plant tissues than workers from species making smaller clearings. Because head shape affects mandible force, I also assessed whether pruning on thick tissue in mutualistic ant species or being a predator in non‐mutualistic species correlated with broader heads, which yield stronger mandible force. The species with the broader heads were non‐mutualistic predators or mutualistic pruners of thick tissues, which suggest that pruning neighboring vegetation in non‐predatory species demands force even when the ants do not kill prey with their mandibles. The findings reveal that clearing size variation in mutualistic ant partners of plants can also be observed at the level of individual decision‐making processes among workers, and suggest that head morphology could be a trait under selection in protective ant–plant mutualisms.

   Abstract in Spanish is available with online material.

    

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3. Cold adaptations along a range limit in an obligate symbiosis

   https://doi.org/10.1111/1365-2435.14120  

   Senula, Sarah F. ; Scavetta, Joseph T. ; Mueller, Ulrich G. ; Seal, Jon Nicholas ; Kellner, Katrin ( July 2022 , Functional Ecology)

   Symbionts can have profound effects on host fitness, adaptations and range distributions. Stress‐induced evolution is difficult to show in obligate symbioses; however, adaptive evolution within an obligate symbiosis can be investigated experimentally or by correlating trait variation with stress along an ecological cline (i.e. temperature‐stress gradient).

   We investigated the cold tolerance of the fungus‐growing antTrachymyrmex septentrionalisby performing cold tolerance assays comparing two populations collected from either the southernmost range of their distribution (Bastrop, Texas) or from a site that is approximately 600 km further north (Norman, Oklahoma). We first compared isolated fungal symbionts grown on artificial media to determine cold tolerance of fungus alone. Subsequently, we conducted cross‐fostering experiments between northern and southern host and symbionts to test for synergisms between the partners in generating adaptations of cold tolerance.

   Ants of the northern fungal populations were more cold adapted than southern fungal populations. Northern nests were deeper and northern colonies initially rejected fungi from the southern population. The cross‐fostering experiments demonstrated that only one partner must be cold tolerant to confer maximum cold tolerance to the ant–fungus symbiosis, because northern ants growing southern fungus under cold stress performed just as well as northern ants growing northern fungi.

   Our results suggest that cold stress has been an important selective factor during the migration of this ant–fungus symbiosis into northern latitudes during the last 10,000 years, and that cold tolerance likely is an energetically demanding trait that may be traded off with other aspects of the symbiosis' life history. The symbiosis also appears to have evolved several additional adaptations that increase survival in cold environments, such as building deeper nests that insulate the fungi from cold surface.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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4. Landscape genomics of an obligate mutualism: Concordant and discordant population structures between the leafcutter ant Atta texana and its two main fungal symbiont types

   https://doi.org/10.1111/mec.15111  

   Smith, Chad C. ; Weber, Jesse N. ; Mikheyev, Alexander S. ; Roces, Flavio ; Bollazzi, Martin ; Kellner, Katrin ; Seal, Jon N. ; Mueller, Ulrich G. ( May 2019 , Molecular Ecology)

   To explore landscape genomics at the range limit of an obligate mutualism, we use genotyping‐by‐sequencing (ddRADseq) to quantify population structure and the effect of host–symbiont interactions between the northernmost fungus‐farming leafcutter antAtta texanaand its two main types of cultivated fungus. Genome‐wide differentiation between ants associated with either of the two fungal types is of the same order of magnitude as differentiation associated with temperature and precipitation across the ant's entire range, suggesting that specific ant–fungus genome–genome combinations may have been favoured by selection. For the ant hosts, we found a broad cline of genetic structure across the range, and a reduction of genetic diversity along the axis of range expansion towards the range margin. This population‐genetic structure was concordant between the ants and one cultivar type (M‐fungi, concordant clines) but discordant for the other cultivar type (T‐fungi). Discordance in population‐genetic structures between ant hosts and a fungal symbiont is surprising because the ant farmers codisperse with their vertically transmitted fungal symbionts. Discordance implies that (a) the fungi disperse also through between‐nest horizontal transfer or other unknown mechanisms, and (b) genetic drift and gene flow can differ in magnitude between each partner and between different ant–fungus combinations. Together, these findings imply that variation in the strength of drift and gene flow experienced by each mutualistic partner affects adaptation to environmental stress at the range margin, and genome–genome interactions between host and symbiont influence adaptive genetic differentiation of the host during range evolution in this obligate mutualism.

    

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5. Dietary specialization in mutualistic acacia‐ants affects relative abundance but not identity of host‐associated bacteria

   https://doi.org/10.1111/mec.14834  

   Rubin, Benjamin E. R. ; Kautz, Stefanie ; Wray, Brian D. ; Moreau, Corrie S. ( August 2018 , Molecular Ecology)

   Acacia‐ant mutualists in the genusPseudomyrmexnest obligately in acacia plants and, as we show through stable isotope analysis, feed at a remarkably low trophic level. Insects with diets such as these sometimes depend on bacterial symbionts for nutritional enrichment. We, therefore, examine the bacterial communities associated with acacia‐ants in order to determine whether they host bacterial partners likely to contribute to their nutrition. Despite large differences in trophic position, acacia‐ants and related species with generalized diets do not host distinct bacterial taxa. However, we find that a small number of previously undescribed bacterial taxa do differ in relative abundance between acacia‐ants and generalists, including several Acetobacteraceae and Nocardiaceae lineages related to common insect associates. Comparisons with an herbivorous generalist, a parasite that feeds on acacias and a mutualistic species with a generalized diet show that trophic level is likely responsible for these small differences in bacterial community structure. While we did not experimentally test for a nutritional benefit to hosts of these bacterial lineages, metagenomic analysis reveals aBartonellarelative with an intact nitrogen‐recycling pathway widespread acrossPseudomyrmexmutualists and generalists. This taxon may be contributing to nitrogen enrichment of its ant hosts through urease activity and, concordant with an obligately host‐associated lifestyle, appears to be experiencing genomewide relaxed selection. The lack of distinctiveness in bacterial communities across trophic level in this group of ants shows a remarkable ability to adjust to varied diets, possibly with assistance from these diverse ant‐specific bacterial lineages.

    

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