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Context Is Everything: Mapping Cyphomyrmex-Derived Compounds to the Fungus-Growing Ant Phylogeny

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Context Is Everything: Mapping Cyphomyrmex-Derived Compounds to the Fungus-Growing Ant Phylogeny Chemoecology (2018) 28:137–144 https://doi.org/10.1007/s00049-018-0265-5 CHEMOECOLOGY ORIGINAL ARTICLE Context is everything: mapping Cyphomyrmex-derived compounds to the fungus-growing ant phylogeny Natalie Hamilton1 · Tappey H. Jones2 · Jonathan Z. Shik3 · Bonnie Wall4 · Ted R. Schultz5 · Haley A. Blair6 · Rachelle M. M. Adams1 Received: 19 June 2018 / Accepted: 21 September 2018 / Published online: 3 October 2018 © Springer Nature Switzerland AG 2018 Abstract Ants communicate using a suite of chemicals with a level of sophistication that is inextricably linked to their ecological dominance. The fungus-growing ants have been the focus of chemical ecology studies for decades, especially the leaf-cutting ants. Some create long, conspicuous foraging trails to harvest fresh vegetation used to sustain large farming systems that feed millions of workers. However, of the ca. 250 fungus-growing ant species, most feed detritus rather than fresh material to their gardens, and colony sizes are tens to hundreds of workers. Colonies within the attine genus Cyphomyrmex use distinct methods of agriculture (i.e., yeast and lower fungus agriculture). We compared compounds found in five species from the yeast-growing Cyphomyrmex rimosus group (C. rimosus and C. salvini) and the lower agriculture Cyphomyrmex wheeleri group (C. costatus, C. longiscapus, C. muelleri). Compounds identified were compared with those reported in the literature and mapped onto the attine-ant phylogeny, and glands of origin suggested. There were 10 compounds across five species and two are known alarm compounds, 1-octen-3-o1 and 3-octanol. Of the six farnesenes detected, the most notable was the diversity of gaster-derived compounds in C. salvini and the high abundance of (3Z, 6E)-α-7-ethylhomofarnesene and α-6- bishomofarnesene in the three C. wheeleri group species. We also found 2,5-dimethyl-3-isoamylpyrazine in the heads of yeast-growing species, an unexpected result because pyrazines are known trail substances in other attines. Our results expand our understanding of semiochemicals found in fungus-growing ants and provides a starting point to generate hypotheses for more extensive comparative studies. Keywords Cyphomyrmex · Fungus-farming ants · Alarm pheromone · Trail pheromone · Chemical communication · Formicidae Introduction Ants (Hymenoptera: Formicidae) have over 75 glands pro- Communicated by Marko Rohlfs. ducing chemicals that guide their social organization, con- tributing to their ecological dominance around the world Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s0004 9-018-0265-5) contains (Jackson and Morgan 1993; Billen 2009). Chemicals provide supplementary material, which is available to authorized users. * Rachelle M. M. Adams 4 Department of Biology, University of Konstanz, [email protected] Universitätsstraße 10, 78464 Konstanz, Germany 5 Department of Entomology and Laboratories of Analytical 1 Department of Evolution, Ecology, and Organismal Biology, Biology, National Museum of Natural History, Smithsonian The Ohio State University, 318 W. 12th Ave. 300 Aronoff Institution, 10th St. and Constitution Ave. NW, Lab, Columbus, OH 43210, USA Washington, DC 20560, USA 2 Department of Chemistry, Virginia Military Institute, 6 Department of Chemistry, University of Virginia, Lexington, VA 24450, USA Charlotesville, VA 22904, USA 3 Department of Biology, Centre for Social Evolution, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark Vol.:(0123456789)1 3 138 N. Hamilton et al. advantages over visual signals, enabling information transfer 2014). Cyphomyrmex species also exhibit defense behaviors in dark nest cavities that can linger in the environment or dis- ranging from crypsis (i.e., playing dead when disturbed) to sipate quickly depending on their volatility (Morgan 2008). aggressive attack (Kweskin 2004; Adams and Longino 2007; Semiochemicals (i.e., allomones and pheromones) are used Adams et al. 2015). Thus, one might expect these species to in complex communication systems that influence territorial produce correspondingly diverse semiochemicals to medi- interactions (Salzemann et al. 1992; Cammaerts and Cam- ate these varied collective farming and defensive behaviors. maerts 1998), nestmate recognition systems (Sainz-Borgo The chemical ecology of fungus-growing ants has been et al. 2013; Norman et al. 2014), foraging recruitment (Van- traditionally focused on the most derived leaf-cutter spe- der Meer et al. 1988) and alarm signaling (Jackson and Mor- cies due to their pest status and large-scale farming sys- gan 1993; Morgan 2008). The importance of these diverse tems. More recently, several compounds have been found functions illustrate the complexity of social organization and to be conserved across the attine phylogeny, in genera that it is therefore not surprising that ants have evolved diverse diverged tens of millions of years ago (e.g., Atta, Apter- glands to produce such compounds (reviewed in: Billen ostigma, Trachymyrmex, and Sericomyrmex (Crewe and 2011). Blum 1972; Adams et al. 2012; Hogan et al. 2017; Norman Many compounds used for communication and defense et al. 2017). Like other ant species, attines use semiochemi- have predicable source glands among seemingly distantly cals in nestmate recognition (e.g., cuticular hydrocarbons) related ant species, but the conservation of semiochemicals (Martin and Drijfhout 2009; Neupert et al. 2018), trail fol- within genera is less known. Functional roles present an lowing (e.g., farnesenes, pyrazines) (David Morgan 2009 additional layer, as some signals depend on compounds from and references therein), nest marking (e.g., long-chain multiple glands (Billen 2006; Morgan 2008). For instance, hydrocarbons) (Salzemann et al. 1992), and alarm behav- the secondary alcohols and corresponding ketones of ant ior (e.g., 3-octanol) (Crewe and Blum 1972; Norman et al. mandibular glands are primarily responsible for the produc- 2017). There is a clear gap in knowledge surrounding the tion of alarm pheromones, whereas long-chain hydrocarbons majority of attine-derived semiochemicals and compara- stored in the postpharyngeal gland (PPG) and produced in tive work is greatly needed. It is likely that Cyphomyrmex- the Dufour’s gland tend to facilitate nestmate recognition derived semiochemicals are shared among various attines (Cammaerts et al. 1981; Jaffe and Marcuse 1983; Morgan despite their divergent farming practices, but this has yet 2008). Trail-marking chemicals and several alarm phero- to be tested. mones are also derived from abdominal glands (e.g., post- We described the chemical compounds found in the head pygidial, Dufour’s, and venom glands) and are frequently and abdomen (i.e., gaster) of five Cyphomyrmex species and made of linear and terpenoid hydrocarbons also known as propose their glandular origins. To our knowledge, of the farnesenes (Blum et al. 1964; Attygalle and Morgan 1984; 23 extant Cyphomyrmex species (Antweb 2018), the glan- Vander Meer et al. 1988). Furthermore, metapleural glands dular secretions of only C. rimosus have so far been studied produce acids with antimicrobial properties that can pro- (Crewe and Blum 1972). We place our findings in an evo- tect the ants from entomopathogens but may also have a lutionary context to highlight the rarity and convergence of communicative function (Morgan 2008; Yek and Mueller some compounds and discuss how farnesenes—likely used 2011). To summarize, all ant species rely on chemical com- as trail pheromones—separate the C. rimosus group (yeast munication and most biosynthesize a remarkable diversity agriculture) and the C. wheeleri group (lower “mycelium” of compounds. agriculture). Cyphomyrmex have great potential for high- The fungus-growing ants (Formicidae: Myrmicinae: lighting possible mechanisms enabling transitions from yeast Attini: subtribe Attina; hereafter “attine” ants) comprise a agriculture and lower agriculture to larger scale farming sys- monophyletic lineage that farms fungus for food (Mehdi- tems that arose over millions of years of attine evolution. abadi and Schultz 2009; Ward et al. 2015). Five key farm- ing practices can be mapped onto the attine phylogeny: (1) lower agriculture, (2) yeast agriculture, (3) coral fungus Materials and methods agriculture, (4) higher agriculture, and (5) leaf-cutter agri- culture (Schultz and Brady 2008). The genus Cyphomyrmex Sample collections occupies a phylogenetically intermediate position between other lower fungus-growing ant genera and the “higher” In May 2015 and 2017, Cyphomyrmex colonies were col- attines (including the leaf-cutting ants). This is particu- lected from four sites in Parque Nacional Soberanía Forest, larly interesting because Cyphomyrmex species from the Panamá. Three were along Pipeline Road (Rio La Seda: N C. wheeleri group (four species) practice lower agriculture 09.16330, W 79.39605; 16E creek: N 9.16379, W 79.74244; and species from the C. rimosus group (19 species) prac- 8W creek: N 9.16093, W 79.75181) and one on Plantation tice yeast agriculture (Mehdiabadi et al. 2012; Albuquerque Road (N 09.15277, W 79.73680), the latter located southeast 1 3 Context is everything: mapping Cyphomyrmex-derived compounds to the fungus-growing ant… 139 across the Río Chagres. Compounds were extracted from Table 1 Collection information Cyphomyrmex freshly collected colonies of five species [i.e., Species Collection code Collection loca- Sample type C. rimosus (2 colonies), C. salvini (6 colonies),
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