skip to main content


Search for: All records

Award ID contains: 1941546

Note: When clicking on a Digital Object Identifier (DOI) number, you will be taken to an external site maintained by the publisher. Some full text articles may not yet be available without a charge during the embargo (administrative interval).
What is a DOI Number?

Some links on this page may take you to non-federal websites. Their policies may differ from this site.

  1. Abstract Background

    Circadian clocks allow organisms to anticipate daily fluctuations in their environment by driving rhythms in physiology and behavior. Inter-organismal differences in daily rhythms, called chronotypes, exist and can shift with age. In ants, age, caste-related behavior and chronotype appear to be linked. Brood-tending nurse ants are usually younger individuals and show “around-the-clock” activity. With age or in the absence of brood, nurses transition into foraging ants that show daily rhythms in activity. Ants can adaptively shift between these behavioral castes and caste-associated chronotypes depending on social context. We investigated how changes in daily gene expression could be contributing to such behavioral plasticity inCamponotus floridanuscarpenter ants by combining time-course behavioral assays and RNA-Sequencing of forager and nurse brains.

    Results

    We found that nurse brains have three times fewer 24 h oscillating genes than foragers. However, several hundred genes that oscillated every 24 h in forager brains showed robust 8 h oscillations in nurses, including the core clock genesPeriodandShaggy. These differentially rhythmic genes consisted of several components of the circadian entrainment and output pathway, including genes said to be involved in regulating insect locomotory behavior. We also found thatVitellogenin, known to regulate division of labor in social insects, showed robust 24 h oscillations in nurse brains but not in foragers. Finally, we found significant overlap between genes differentially expressed between the two ant castes and genes that show ultradian rhythms in daily expression.

    Conclusion

    This study provides a first look at the chronobiological differences in gene expression between forager and nurse ant brains. This endeavor allowed us to identify a putative molecular mechanism underlying plastic timekeeping: several components of the ant circadian clock and its output can seemingly oscillate at different harmonics of the circadian rhythm. We propose that such chronobiological plasticity has evolved to allow for distinct regulatory networks that underlie behavioral castes, while supporting swift caste transitions in response to colony demands. Behavioral division of labor is common among social insects. The links between chronobiological and behavioral plasticity that we found inC. floridanus, thus, likely represent a more general phenomenon that warrants further investigation.

     
    more » « less
  2. 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.

     
    more » « less
  3. 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.

     
    more » « less
  4. During surveys in central Florida of the zombie-ant fungus Ophiocordyceps camponoti-floridani , which manipulates the behavior of the carpenter ant Camponotus floridanus , two distinct fungal morphotypes were discovered associated with and purportedly parasitic on O. camponoti-floridani . Based on a combination of unique morphology, ecology and phylogenetic placement, we discovered that these morphotypes comprise two novel lineages of fungi. Here, we propose two new genera, Niveomyces and Torrubiellomyces , each including a single species within the families Cordycipitaceae and Ophiocordycipitaceae , respectively. We generated de novo draft genomes for both new species and performed morphological and multi-loci phylogenetic analyses. The macro-morphology and incidence of both new species, Niveomyces coronatus and Torrubiellomyces zombiae , suggest that these fungi are mycoparasites since their growth is observed exclusively on O. camponoti-floridani mycelium, stalks and ascomata, causing evident degradation of their fungal hosts. This work provides a starting point for more studies into fungal interactions between mycopathogens and entomopathogens, which have the potential to contribute towards efforts to battle the global rise of plant and animal mycoses. 
    more » « less
  5. Garsin, Danielle A. (Ed.)
    ABSTRACT Transmission is a crucial step in all pathogen life cycles. As such, certain species have evolved complex traits that increase their chances to find and invade new hosts. Fungal species that hijack insect behaviors are evident examples. Many of these “zombie-making” entomopathogens cause their hosts to exhibit heightened activity, seek out elevated positions, and display body postures that promote spore dispersal, all with specific circadian timing. Answering how fungal entomopathogens manipulate their hosts will increase our understanding of molecular aspects underlying fungus-insect interactions, pathogen-host coevolution, and the regulation of animal behavior. It may also lead to the discovery of novel bioactive compounds, given that the fungi involved have traditionally been understudied. This minireview summarizes and discusses recent work on zombie-making fungi of the orders Hypocreales and Entomophthorales that has resulted in hypotheses regarding the mechanisms that drive fungal manipulation of insect behavior. We discuss mechanical processes, host chemical signaling pathways, and fungal secreted effectors proposed to be involved in establishing pathogen-adaptive behaviors. Additionally, we touch on effectors’ possible modes of action and how the convergent evolution of host manipulation could have given rise to the many parallels in observed behaviors across fungus-insect systems and beyond. However, the hypothesized mechanisms of behavior manipulation have yet to be proven. We, therefore, also suggest avenues of research that would move the field toward a more quantitative future. 
    more » « less