EVOLUTIONARY TRANSITIONS IN ENZYME ACTIVITY OF ANT FUNGUS GARDENS

Fungus‐growing (attine) ants and their fungal symbionts passed through several evolutionary transitions during their 50 million year old evolutionary history. The basal attine lineages often shifted between two main cultivar clades, whereas the derived higher‐attine lineages maintained an association with a monophyletic clade of specialized symbionts. In conjunction with the transition to specialized symbionts, the ants advanced in colony size and social complexity. Here we provide a comparative study of the functional specialization in extracellular enzyme activities in fungus gardens across the attine phylogeny. We show that, relative to sister clades, gardens of higher‐attine ants have enhanced activity of protein‐digesting enzymes, whereas gardens of leaf‐cutting ants also have increased activity of starch‐digesting enzymes. However, the enzyme activities of lower‐attine fungus gardens are targeted primarily toward partial degradation of plant cell walls, reflecting a plesiomorphic state of nondomesticated fungi. The enzyme profiles of the higher‐attine and leaf‐cutting gardens appear particularly suited to digest fresh plant materials and to access nutrients from live cells without major breakdown of cell walls. The adaptive significance of the lower‐attine symbiont shifts remains unclear. One of these shifts was obligate, but digestive advantages remained ambiguous, whereas the other remained facultative despite providing greater digestive efficiency.     

Forage collection,substrate preparation,and diet composition in fungus‐growing ants

1. Variation and control of nutritional input is an important selective force in the evolution of mutualistic interactions and may significantly affect coevolutionary modifications in partner species. 2. The attine fungus‐growing ants are a tribe of more than 230 described species (12 genera) that use a variety of different substrates to manure the symbiotic fungus they cultivate inside the nest. Common ‘wisdom’ is that the conspicuous leaf‐cutting ants primarily use freshly cut plant material, whereas most of the other attine species use dry and partly degraded plant material such as leaf litter and caterpillar frass, but systematic comparative studies of actual resource acquisition across the attine ants have not been done. 3. Here we review 179 literature records of diet composition across the extant genera of fungus‐growing ants. The records confirm the dependence of leaf‐cutting ants on fresh vegetation but find that flowers, dry plant debris, seeds (husks), and insect frass are used by all genera, whereas other substrates such as nectar and insect carcasses are only used by some. 4. Diet composition was significantly correlated with ant substrate preparation behaviours before adding forage to the fungus garden, indicating that diet composition and farming practices have co‐evolved. Neither diet nor preparation behaviours changed when a clade within the paleoattine genus Apterostigma shifted from rearing leucocoprinous fungi to cultivating pterulaceous fungi, but the evolutionary derived transition to yeast growing in the Cyphomyrmex rimosus group, which relies almost exclusively on nectar and insect frass, was associated with specific changes in diet composition. 5. The co‐evolutionary transitions in diet composition across the genera of attine ants indicate that fungus‐farming insect societies have the possibility to obtain more optimal fungal crops via artificial selection, analogous to documented practice in human subsistence farming.     

Impact of plant flowering phenology on the cost/benefit balance in a nursery pollination mutualism,with honest males and cheating females

This study documents the flowering phenology and its potential consequences on a nursery pollination mutualism between a dioecious plant, in which honest male plants, but not cheating females, allow the specific pollinator to reproduce within inflorescences. Very few pollinators were found to emerge during plant anthesis, leading to a low (if any) potential benefit through pollen dispersal. This opens the question why male plants do not also cheat their pollinators. Female plants flowered late in the season, when many males had just achieved their own anthesis, which increased the efficiency of pollen transfer. Finally, some late‐flowering males reached their anthesis simultaneously with females, which open the possibility for pollinator to choose between honest males and cheating females. Nevertheless, female plants were found to produce fruits, even though fruit production was limited by pollen (and pollinator) supply, meaning that cheating was not entirely retaliated by the mutualistic partner.     

The group selection controversy

Many thought Darwinian natural selection could not explain altruism. This error led Wynne‐Edwards to explain sustainable exploitation in animals by selection against overexploiting groups. Williams riposted that selection among groups rarely overrides within‐group selection. Hamilton showed that altruism can evolve through kin selection. How strongly does group selection influence evolution? Following Price, Hamilton showed how levels of selection interact: group selection prevails if Hamilton’s rule applies. Several showed that group selection drove some major evolutionary transitions. Following Hamilton’s lead, Queller extended Hamilton’s rule, replacing genealogical relatedness by the regression on an actor’s genotypic altruism of interacting neighbours’ phenotypic altruism. Price’s theorem shows the generality of Hamilton’s rule. All instances of group selection can be viewed as increasing inclusive fitness of autosomal genomes. Nonetheless, to grasp fully how cooperation and altruism evolve, most biologists need more concrete concepts like kin selection, group selection and selection among individuals for their common good.     

Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species

Many legumes form tripartite symbiotic associations with rhizobia and arbuscular mycorrhizal fungi (AMF). Rhizobia are located in root nodules and provide the plant with fixed atmospheric nitrogen, while AMF colonize plant roots and deliver several essential nutrients to the plant. Recent studies showed that AMF are also associated with root nodules. This might point to interactions between AMF and rhizobia inside root nodules. Here, we test whether AMF colonize root nodules in various plant-AMF combinations. We also test whether nodules that are colonized by AMF fix nitrogen. Using microscopy, we observed that AMF colonized the root nodules of three different legume species. The AMF colonization of the nodules ranged from 5% to 74% and depended on plant species, AMF identity and nutrient availability. However, AMF-colonized nodules were not active, that is, they did not fix nitrogen. The results suggest that AMF colonize old senescent nodules after nitrogen fixation has stopped, although it is also possible that AMF colonization of nodules inhibits nitrogen fixation.     

Soil biota and invasive plants

Interactions between plants and soil biota resist invasion by some nonnative plants and facilitate others. In this review, we organize research and ideas about the role of soil biota as drivers of invasion by nonnative plants and how soil biota may fit into hypotheses proposed for invasive success. For example, some invasive species benefit from being introduced into regions of the world where they encounter fewer soil-borne enemies than in their native ranges. Other invasives encounter novel but strong soil mutualists which enhance their invasive success. Leaving below-ground natural enemies behind or encountering strong mutualists can enhance invasions, but indigenous enemies in soils or the absence of key soil mutualists can help native communities resist invasions. Furthermore, inhibitory and beneficial effects of soil biota on plants can accelerate or decelerate over time depending on the net effect of accumulating pathogenic and mutualistic soil organisms. These 'feedback' relationships may alter plant-soil biota interactions in ways that may facilitate invasion and inhibit re-establishment by native species. Although soil biota affect nonnative plant invasions in many different ways, research on the topic is broadening our understanding of why invasive plants can be so astoundingly successful and expanding our perspectives on the drivers of natural community organization.     

Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia

In nursery pollination systems, pollinator offspring usually feed on pollinated fruits or seeds. Costs and benefits of the interaction for plant and pollinator, and hence its local outcome (antagonism-mutualism), can be affected by the presence of 'third-party' species. Infection of Silene latifolia plants by the fungus Microbotryum violaceum halts the development of fruits that provide shelter and food for larvae of the pollinating moth Hadena bicruris. We investigated whether the moth secures its benefit by selective oviposition on uninfected flowers. Oviposition was recorded in eight natural populations as a function of plant infection status, local neighbourhood, plant and flower characteristics. Oviposition was six times lower on flowers from infected than on those from uninfected plants. Oviposition decreased with decreasing flower and ovary size. Moths could use the latter to discriminate against diseased flowers. Although moths show an adaptive oviposition response, they reduce the future potential of healthy hosts because they still visit infected plants for nectar, vectoring the disease, and they reduce any fitness advantage gained by disease-resistant plants through selective predation of those plants.