Most ant colonies are comprised of workers that cooperate to harvest resources and feed developing larvae. Around 50 million years ago (MYA), ants of the attine lineage adopted an alternative strategy, harvesting resources used as compost to produce fungal gardens. While fungus cultivation is considered a major breakthrough in ant evolution, the associated ecological consequences remain poorly understood. Here, we compare the energetics of attine colony-farms and ancestral hunter-gatherer colonies using metabolic scaling principles within a phylogenetic context. We find two major energetic transitions. First, the earliest lower-attine farmers transitioned to lower mass-specific metabolic rates while shifting significant fractions of biomass from ant tissue to fungus gardens. Second, a transition 20 MYA to specialized cultivars in the higher-attine clade was associated with increased colony metabolism (without changes in garden fungal content) and with metabolic scaling nearly identical to hypometry observed in hunter-gatherer ants, although only the hunter-gatherer slope was distinguishable from isometry. Based on these evolutionary transitions, we propose that shifting living-tissue storage from ants to fungal mutualists provided energetic storage advantages contributing to attine diversification and outline critical assumptions that, when tested, will help link metabolism, farming efficiency, and colony fitness.
The metabolic and demographic composition of attine colony-farms
The raw data used for statistical inference regarding attine metabolism (MR, µl CO2 hr^-1) and demography. All masses are dry weight (mg). For Apt. dentigerum and C. longiscapus colony-farms, we did not make separate recordings of garden MR after removing workers. For these two species, we thus present only a whole colony-farm MR measurement. Mass is dry mass in mg. Locality abbreviations: Arizona (A), Barro Colorado Island, Panama (P), Oklahoma (O), Texas (T). Garden mass and MR contains embedded larvae. Notes: * 2 queens, whose individual masses were 0.44 and 0.40 mg, § worker mass includes 16 males (5.84 mg, 19% of total mass), ∫ Queen not removed prior to measurement of worker MR.
Table A1.xlsx
The metabolic and demographic composition of hunter-gather colonies.
Raw data used to analyze the metabolic rate (MR; µ l CO2 hr-1) and demography of hunter-gatherer colonies. Collection localities are either Oklahoma (O) or Panama (P). N refers to the number of colonies sampled for a given species. Worker number and mass sums minor and majors for colonies of Pheidole. Reproductive mass sums adult male and female alate tissue. Mass is dry mass in mg. Means followed by SD in parentheses.
TABLE A2.xlsx
Data used to calculate mass-specific metabolic rates of workers
Data used for examination of individual worker metabolic rates (MR: µl CO2 mg-1 hr-1), presented in online figure A2. Mass values are dry mass (mg).
Table A3.xlsx
Data for comparison of mass-specific MR of workers and fungus gardens
Mean mass-specific metabolic rate (MR; µl CO2 mg-1 hr-1) for workers and fungal gardens, and results of one sample t-tests comparing worker MR with the mean value for their fungal gardens. Size measured as dry mass. N indicates number of individual workers measured for MR, and the number of individual colonies from which fungal gardens were measured for MR. Means followed by SD in parentheses.
TABLE A4.xlsx
Accession numbers for the sequences used to infer the ant phylogeny
Accession numbers for the sequences used to infer the ant phylogeny. In species where molecular data were not available (indicated with *), we used sequences from closely related congeners. COI barcodes for the species listed as ‘Processing’ were provided by D. Donoso and obtained in collaboration with the Biodiversity Institute of Ontario, using sequencing techniques and analytical tools in the Barcode of Life Database (BOLD; www.boldsystems.org/). New sequences for the study, as well as sequences for C. sumichrasti and P. villosa, are publicly available in the BOLD database, in the project ‘AOFBA’ named Ants of BCI_2_Project Atta. Molecular data included three genes: Cy-tochrome Oxidase I (COI; mitochondrial), wingless (nuclear), and long wavelength rho-dopsin (LWRh; nuclear).
Table A5.xlsx