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Neotrop Entomol https://doi.org/10.1007/s13744-019-00735-z ECOLOGY, BEHAVIOR AND BIONOMICS The Diversity and Distribution of Wolbachia, Rhizobiales, and Ophiocordyceps Within the Widespread Neotropical Turtle Ant, Cephalotes atratus (Hymenoptera: Formicidae) 1 1 1,2 1,2,3 DD REEVES ,SLPRICE ,MORAMALHO ,CSMOREAU 1Department of Science and Education, Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA 2Department of Entomology, Cornell University, Ithaca, NY, USA 3Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA Keywords Abstract Symbiont, fungi, bacteria, microbes, giant Ants are an ecologically and evolutionarily diverse group, and they harbor turtle ant a wide range of symbiotic microbial communities that often greatly affect Correspondence their biology. Turtle ants (genus Cephalotes) engage in mutualistic rela- M.O. Ramalho, Department of Entomology, tionships with gut bacteria and are exploited by microbial parasites. Cornell University, Ithaca, NY, USA; [email protected] Studies have shown that associations among these microbial lineages and the turtle ant hosts vary geographically. However, these studies have Edited by Alberto S Corrêa – ESALQ/USP been limited, and thorough within-species analyses of the variation and Received 5 June 2019 and accepted 24 structure of these microbial communities have yet to be conducted. The October 2019 giant turtle ant, Cephalotes atratus (Linnaeus 1758), is a geographically widespread, genetically diverse Neotropical species that has been sampled * Sociedade Entomológica do Brasil 2020 extensively across its geographic range, making it ideal for analysis of microbial associations. In this study, we verified the presence, genetic variation, and geographic patterns at the individual, colony, and popula- tion level of three microbial groups associated with the giant turtle ant: Wolbachia, a genus of facultative bacteria which are often parasitic, af- fecting host reproduction; Rhizobiales, a mutualistic order of bacteria hy- pothesized to be an obligate nutritional symbiont in turtle ants; and Ophiocordyceps, a genus of endoparasitic fungi infecting many arthropod species by manipulating their behavior for fungal reproduction. In this study, we found varying degrees of prevalence for two distantly related genotypes (haplogroups) of Wolbachia and high degree of prevalence of Rhizobiales across colonies with little genetic variation. In addition, we found low occurrence of Ophiocordyceps. This study highlights a key first step in understanding the diversity, distribution, and prevalence of the microbial community of C. atratus. Introduction common host to a variety of symbionts, with parasitic and mutualistic interactions (Feldhaar et al 2007;Stollet al Ants can be one of the players in several complex symbiotic 2007; Pinto-Tomas et al 2009;Frostet al 2010; Evans et al. relationships such as ant-plant, ant-animal, and ant-microbe 2011; Russell et al 2012; Martins et al 2012; Vieira et al interactions. It has been known for over a century that ants 2017). Some ant groups at least partially owe their ecolog- possess intracellular bacteria, as first recognized by ical success to internal mutualists. This idea is well-studied Blochmann (1882)forCamponotus and Formica (subfamily: in carpenter ants (Formicinae: Camponotus), whose gut Formicinae). It has since been shown that ants are also a bacteria (Blochmannia) provide amino acids and nitrogen Reeves et al recycling for the host (Feldhaar et al 2007), and fungus- et al 2018) and can also be horizontally transmitted between growing ants (Formicinae: Attini), which possess antibiotic- species as they interact in their environment (Stouthamer et al producing bacteria (Streptomyces) that inhibit the growth 1999). The reproductive cycle of ants, in which a single queen of a parasitic fungus in the ants’ fungus gardens (Currie produces the entirety of a colony, should therefore predict the et al 1999). There are many other ant-microbe interactions same Wolbachia morph across a colony, or even a population, that are not as well-studied, despite the growing evidence although horizontal transmission makes strain variation possi- for the importance of symbionts in the ecology and evolu- ble (Ahmed et al 2015). tion of their hosts. In order to glean information on a As Cephalotes is a mainly herbivorous group, the diet of microbe’s life history, or the coevolutionary history be- many of the species is poor in some key nutrients such as tween host and microbe, a critical first step is to analyze nitrogen (Russell et al 2009a). It has been shown that their the presence and diversity of host-associated microbes. herbivory is facilitated by symbiotic bacteria specific to the gut The turtle ants are a widespread, arboreal, mainly (Russell et al 2009a;Huet al 2018) as in other insect groups Neotropical ant group (Price et al 2014). Hu et al (2013) surveyed (Engel & Moran 2013). Bacteria of the order Rhizobiales are the gut microbiota of the turtle ant species Cephalotes varians noteworthy symbionts in root nodules of plants but are also (subfamily: Myrmicinae Smith 1876), revealing varying microbial found in lichens and herbivorous ants (Erlacher et al 2015; abundance and genotypes between colonies and across the Russell et al 2009a). While Rhizobiales is nitrogen-fixing in geographic range of this species. Little is known of the variation plant-microbe symbiosis, it is unclear if the same process is within other Cephalotes species, however. Likely, the most com- mirrored in the turtle ant Rhizobiales strains, although it has mon turtle ant species Cephalotes atratus (Linnaeus 1758) occu- been hypothesized due to the nitrogen-poor diet of herbivorous pies an unusually large range for an insect, one that spans the ants (Russell et al 2009a;Hu2015). However, genes for a urea- entirety of South America’s longitude (Kempf 1951, de Andrade recycling complex were found in Rhizobiales found in the diges- &Urbani1999,seeFig1-A). This broad range lends to the diver- tive tracts of several Cephalotes species (Hu et al 2018). sity of habitats that C. atratus occupies, which predominantly Lastly, C. atratus makes an ideal system for studying interac- includes lowland wet forest but also savanna and xeric scrub- tions with another symbiont: the tropical, parasitic fungi genus lands (de de Andrade & Urbani 1999). The species’ larger body Ophiocordyceps (previously Cordyceps, see Sung et al 2007). size and enormous colonies also allow collection of large sam- Famously referred to as “zombie-ant fungi,” Ophiocordyceps is ples throughout its geographic range (Corn 1976). able to infect a variety of arthropod hosts with differing life Wolbachia is a commonly encountered reproductive para- history traits. Several species of Ophiocordyceps rely on ants site that targets invertebrates, with a list of effects such as for propagation, with spore-infected individuals dying and the cytoplasmic incompatibility, parthenogenesis, and male killing eventual germination of Ophiocordyceps fruiting bodies continu- or feminization (reviewed in Werren et al 2008). ing infection near and within colonies (Araújo et al 2015). Approximately 65% of insect species are host to the parasite, Cephalotes atratus was a notable host to Ophiocordyceps in highlighting its abundance (Hilgenboecker et al 2008). These early observations of the fungus, with workers extracting bacteria are incredibly well-documented across a wide range infected individuals from the colony and dropping them from of ant genera, showcasing the commonness of the microbe the canopy to the forest floor (Evans 1982). (Frost et al 2010,Frostet al 2014,Russellet al 2012, de Souza We analyze the presence, genetic variation, and geo- et al 2009,Souzaet al 2014,Kautzet al 2013,Martinset al graphic patterns of three microbes, Wolbachia, Rhizobiales, 2012, Ramalho et al 2017a, Ramalho et al 2017b, Ramalho et al and Ophiocordyceps, of a widespread and extensively collect- 2018), although it is still unknown how and if this bacterium ed turtle ant species, C. atratus. We survey these microbes affects ant hosts, particularly in the case of sterile ant workers across the geographic range of C. atratus at the individual, that are unable to reproduce. In ants, estimates range from colony, and population level. We then examine whether 29% to 50% prevalence in colonies (Russell et al 2009b, there is distinct genetic diversification within each symbiont. Wenseleers et al 1998). Kautz et al (2013) found high colony This survey and analysis provide an important first step in prevalence of Wolbachia within four of seven examined understanding the interactions and coevolutionary history Cephalotes species, including C. atratus, suggesting between this host and its microbes. Wolbachia parasitizes C. atratus.Despiteitscommonness, the specific methods through which Wolbachia parasitizes ants are unclear. Recent evidence rejects cytoplasmic incom- Materials and Methods patibility and parthenogenesis as viable methods, leaving male killing and feminization as possible candidates, at least in Collection and extraction Monomorium pharaonis (subfamily: Myrmicinae; Linnaeus 1758) (Pontieri et al 2017). Wolbachia transmits itself vertically Ants were collected across the geographic range of from mother to offspring (Wernegreen et al 2009, Ramalho C. atratus, including north and south Peru, northwestern Diversity and Distribution of Three Symbionts Within C. atratus Fig 1 Cephalotes atratus
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    46 Million Years of N-Recycling by the Core Symbionts of Turtle Ants

    bioRxiv preprint doi: https://doi.org/10.1101/185314; this version posted September 7, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Nitrogen conservation, conserved: 46 million years of N-recycling by the core symbionts of 2 turtle ants 3 4 Yi Hu1*, Jon G. Sanders2*, Piotr Łukasik1, Catherine L. D'Amelio 1, John S. Millar3, David R. 5 Vann4, Yemin Lan5, Justin A. Newton1, Mark Schotanus6, John T. Wertz6, Daniel J. C. 6 Kronauer7, Naomi E. Pierce2, Corrie S. Moreau8, Philipp Engel9, Jacob A. Russell1 7 8 1 Department of Biology, Drexel University, Philadelphia, PA 19104, USA 9 2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 10 02138, USA 11 3 Department of Medicine, Institute of Diabetes, Obesity and Metabolism, University of 12 Pennsylvania, Philadelphia, PA 19104, USA 13 4 Department of Earth and Environmental Science, University of Pennsylvania, Philadelphia, PA 14 19104, USA 15 5 School of Biomedical Engineering, Science and Health systems, Drexel University, 16 Philadelphia, PA 19104, USA 17 6 Department of Biology, Calvin College, Grand Rapids, MI 49546, USA 18 7 Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, 19 New York, NY 10065, USA 20 8 Department of Science and Education, Field Museum of Natural History, Chicago, IL 60605, 21 USA 22 9 Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, 23 Switzerland bioRxiv preprint doi: https://doi.org/10.1101/185314; this version posted September 7, 2017.