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Nutrition Mediates the Expression of Cultivar–Farmer Conflict in a Fungus-Growing Ant

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Nutrition Mediates the Expression of Cultivar–Farmer Conflict in a Fungus-Growing Ant Nutrition mediates the expression of cultivar–farmer conflict in a fungus-growing ant Jonathan Z. Shika,b,1, Ernesto B. Gomezb, Pepijn W. Kooija,c, Juan C. Santosd, William T. Wcislob, and Jacobus J. Boomsmaa aCentre for Social Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark; bSmithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama; cJodrell Laboratory, Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, Richmond TW9 3DS, United Kingdom; and dDepartment of Biology, Brigham Young University, Provo, UT 84602 Edited by Bert Hölldobler, Arizona State University, Tempe, AZ, and approved July 8, 2016 (received for review April 16, 2016) Attine ants evolved farming 55–60 My before humans. Although whose sexual fruiting bodies represent considerable investments. evolutionarily derived leafcutter ants achieved industrial-scale farm- An illustrative example is offered by the fungus-growing attine ing, extant species from basal attine genera continue to farm loosely ants, whose dispersing queens transmit symbionts vertically and domesticated fungal cultivars capable of pursuing independent re- whose farming workers therefore actively suppress wasteful for- productive interests. We used feeding experiments with the basal mation of inedible mushrooms (16, 17). Another example is pro- attine Mycocepurus smithii to test whether reproductive allocation vided by two independently derived lineages of fungus-growing Termitomyces conflicts between farmers and cultivars constrain crop yield, possibly termites that both evolved vertical transmission of explaining why their mutualism has remained limited in scale and cultivars while terminating mushroom production (18). However, productivity. Stoichiometric and geometric framework approaches although such correlated adaptive states are consistent with the- oretical predictions, and have been tested and confirmed in some showed that carbohydrate-rich substrates maximize growth of both plant–microbe symbioses (6, 7), no experimental work has tested edible hyphae and inedible mushrooms, but that modest protein whether allocation conflicts affect the ecological dynamics of an- provisioning can suppress mushroom formation. Worker foraging imal ectosymbioses in similar ways. was consistent with maximizing long-term cultivar performance: Here, we present such a test, using the common and widely ant farmers could neither increase carbohydrate provisioning with- distributed (Argentina to northern Mexico) basal fungus-growing EVOLUTION out cultivars allocating the excess toward mushroom production, nor ant Mycocepurus smithii as a model (19). This ant species is no- increase protein provisioning without compromising somatic cultivar table for being parthenogenetic (19), allowing controlled experi- growth. Our results confirm that phylogenetically basal attine farm- mentation with genetically uniform worker ants. It also rears an ing has been very successful over evolutionary time, but that unusual variety of fungal symbiont clones that are not irreversibly unresolved host–symbiont conflict may have precluded these wild- domesticated and apparently continue to exchange genes with type symbioses from rising to ecological dominance. That status was free-living relatives (16, 20). Cultivars have thus retained their full achieved by the evolutionarily derived leafcutter ants following full sexual potential so that ant farmers have explicit potential conflicts domestication of a coevolving cultivar 30–35 Mya after the first with their crops over mushroom production that may damage attine ants committed to farming. symbiotic performance when expressed. The phylogenetically basal “lower attine” lineages to which social evolution | crop domestication | symbiosis | geometric framework | M. smithii belongs evolved more than 50 Mya when the ants Mycocepurus smithii Significance esources derived from mutualists often enhance the ecological Rdominance of partnered species (1, 2), but can also lead to Early subsistence farming implied significant physiological chal- conflicts between them (3, 4). Such conflicts typically stem from lenges for Neolithic farmers until they genetically isolated their diverging reproductive interests between hosts and symbionts, which crops through artificial selection and polyploidization. The attine may arise for two reasons. First, there is a fundamental conflict over ants faced analogous challenges when they adopted fungus symbiont mixing because any host compartment that is accessible farming 55–60 Mya. Whereas evolutionarily derived attine line- for multiple symbiont strains incurs a risk of symbionts competing ages irreversibly domesticated cultivars approximately 25 Mya for host resources (5) or of one of them free-riding on the services and ultimately realized industrial-scale farming, basal lineages of the other (6, 7), to the detriment of the host. The most harmo- retained small-scale farming, diversified, and now coexist with nious mutualisms are therefore expected to always involve a single advanced fungus-farmers in most New World tropical ecosys- strain of clonal symbiont per individual host. Typical examples are tems. We show that management of independent sexual re- the mitochondria and plastids that were domesticated by early eu- production in cultivars constrained farming productivity, echoing karyote protists (8, 9), and nutritional symbionts of insects with early human farming of unspecialized low-productivity crops. Loss of cultivar gene exchange with nondomesticated relatives specialized diets that are clonal within host individuals but geneti- – cally variable across hosts (10–12). Second, when mutualisms evolve likely reduced host symbiont conflict over reproduction, foster- ing the rise of ecologically dominant ant-agriculture. vertical symbiont transmission, hosts are selected to suppress ten- dencies of their symbiont to continue investing in traits favoring Author contributions: J.Z.S., W.T.W., and J.J.B. designed research; J.Z.S. and E.B.G. per- horizontal transmission, because to quote Axelrod and Hamilton, formed research; J.Z.S. and P.W.K. contributed new reagents/analytic tools; J.Z.S., P.W.K., “...[a]nysymbiontthatstill has a transmission ‘horizontally’...would J.C.S., and J.J.B. analyzed data; and J.Z.S. and J.J.B. wrote the paper. be expected to shift from mutualism to parasitism...” (13). Such The authors declare no conflict of interest. selfish symbiont traits that use host resources to enhance independent This article is a PNAS Direct Submission. reproductive success without offering the host any returns (14) have Freely available online through the PNAS open access option. been likened to parasitic virulence (5), highlighting that mutualisms Data deposition: The sequences reported in this paper have been deposited in the Gen- are forms of reciprocal exploitation unless reproductive interests are Bank database. For a list of accession numbers, see Table S9. completely aligned (9, 15). 1To whom correspondence should be addressed. Email: [email protected]. – Host symbiont conflicts over horizontal symbiont transmission This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. are particularly acute when symbionts are multicellular eukaryotes 1073/pnas.1606128113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1606128113 PNAS | September 6, 2016 | vol. 113 | no. 36 | 10121–10126 Downloaded by guest on September 27, 2021 specialized in farming gardens of basidiomycete fungi provisioned cultivar performance in vitro? (ii)Doantfarmersprioritize with nutritionally poor forest-floor detritus (21–23). This commit- harvesting proteins and carbohydrates based on their distinct ment to farming later led to the emergence of the “higher attines,” effects on somatic and reproductive growth of cultivars? (iii)Do including the Acromyrmex and Atta leafcutter ants that rear truly naturally available foraging targets allow farming ants to nutri- domesticated and coevolving cultivars on fresh plant-material sub- tionally regulate garden growth under field conditions? strates (22–25). However, it has remained underappreciated that (iv) Do farming ants deviate from maximal foraging expecta- relatively unproductive farming in the lower attines has otherwise tions for somatic cultivar growth to avoid overt reproductive been very successful in coping with the nutritional challenges of an conflict with their cultivars? The results that we obtained show exclusive fungal diet, in maintaining homeostatic growth conditions that there is a continuous threat of host–symbiont conflict over for small gardens, and in controlling fungal pathogens and social resource allocation toward horizontal symbiont transmission, – parasites (26 28). The continued survival and diversification of consistent with fundamental constraints in crop-yield pro- these small-scale farming mutualisms over evolutionary time thus ductivity that may have precluded the evolution of larger-scale suggests that these ants have found ways to control potential con- farming in phylogenetically basal attine ants. flicts emanating from the unavoidable sexual inclinations of their symbiotic cultivars. Results Because growth and reproduction in free-living basidiomycete Question 1: What Nutritional Blends Maximize Fungal Cultivar Performance fungi depend on access to specific amounts of protein and car- M. smithii in Vitro? We mapped somatic (hyphal) and reproductive (mushroom) bohydrates (29,
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