Dry habitats were crucibles of domestication in the evolution of agriculture in ants.

Michael G Branstetter,Ted R Schultz,Ana Ješovnik,Brant C Faircloth,Michael W Lloyd,Seán G Brady,Jeffrey Sosa-Calvo

doi:10.1098/rspb.2017.0095

Abstract

The evolution of ant agriculture, as practised by the fungus-farming ‘attine’ ants, is thought to have arisen in the wet rainforests of South America about 55–65 Ma. Most subsequent attine agricultural evolution, including the domestication event that produced the ancestor of higher attine cultivars, is likewise hypothesized to have occurred in South American rainforests. The ‘out-of-the-rainforest’ hypothesis, while generally accepted, has never been tested in a phylogenetic context. It also presents a problem for explaining how fungal domestication might have occurred, given that isolation from free-living populations is required. Here, we use phylogenomic data from ultra-conserved element (UCE) loci to reconstruct the evolutionary history of fungus-farming ants, reduce topological uncertainty, and identify the closest non-fungus-growing ant relative. Using the phylogeny we infer the history of attine agricultural systems, habitat preference and biogeography. Our results show that the out-of-the-rainforest hypothesis is correct with regard to the origin of attine ant agriculture; however, contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable to the growth of free-living populations of attine fungal cultivars. We suggest that dry habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur.

Highlights

During the past 10 000 years, humans have domesticated over 260 plant, 470 animal and 100 mushroom-forming fungal species [1,2,3]
We find that the out-of-the-rainforest hypothesis is supported with regard to the origin of attine 2 ant agriculture; contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable, at least during the dry season, to the growth of free-living populations of attine fungal cultivars
We suggest that inhospitable habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur

Summary

Introduction

During the past 10 000 years, humans have domesticated over 260 plant, 470 animal and 100 mushroom-forming fungal species [1,2,3]. We describe the results of a phylogenomic analysis of the fungus-farming ants, in which we used hundreds of ultra-conserved element (UCE) loci to resolve outstanding ambiguities in attine ant phylogeny This robust phylogeny permits the identification of major evolutionary transitions on specific lineages, including the transition from lower to higher agriculture, with greatly reduced phylogenetic uncertainty. Using the Attine-118T-F75 alignment set, we investigated the effects of inference method and data partitioning on results (see electronic supplementary material, appendix A2 for additional detail). We generated a new set of alignments filtered at 75% taxon occupancy (‘Attine-119T-F75’), concatenated the loci, and performed an unpartitioned analysis with RAxML. We performed trait reconstruction analyses to examine the evolution of attine ant (i) agriculture and (ii) habitat preference In both cases, we used the same pruned BEAST tree that we used for biogeography.

Results

Findings

Discussion

Conclusion