No abstract

Leafcutter ants propagate co-evolving fungi for food. The nearly 50 species of leafcutter ants (Atta, Acromyrmex) range from Argentina to the United States, with the greatest species diversity in southern South America. We elucidate the biogeography of fungi cultivated by leafcutter ants using DNA sequence and microsatellite-marker analyses of 474 cultivars collected across the leafcutter range. Fungal cultivars belong to two clades (Clade-A and Clade-B). The dominant and widespread Clade-A cultivars form three genotype clusters, with their relative prevalence corresponding to southern South America, northern South America, Central and North America. Admixture between Clade-A populations supports genetic exchange within a single species, Leucocoprinus gongylophorus. Some leafcutter species that cut grass as fungicultural substrate are specialized to cultivate Clade-B fungi, whereas leafcutters preferring dicot plants appear specialized on Clade-A fungi. Cultivar sharing between sympatric leafcutter species occurs frequently such that cultivars of Atta are not distinct from those of Acromyrmex. Leafcutters specialized on Clade-B fungi occur only in South America. Diversity of Clade-A fungi is greatest in South America, but minimal in Central and North America. Maximum cultivar diversity in South America is predicted by the Kusnezov-Fowler hypothesis that leafcutter ants originated in subtropical South America and only dicot-specialized leafcutter ants migrated out of South America, but the cultivar diversity becomes also compatible with a recently proposed hypothesis of a Central American origin by postulating that leafcutter ants acquired novel cultivars many times from other nonleafcutter fungus-growing ants during their migrations from Central America across South America. We evaluate these biogeographic hypotheses in the light of estimated dates for the origins of leafcutter ants and their cultivars.

Although life-history trade-offs result from the differential acquisition and allocation of nutritional resources to competing physiological functions, many aspects of this topic remain poorly understood. Wingpolymorphic insects, which possess alternative morphs that trade off allocation to flight capability versus early reproduction, provide a good model system for exploring this topic. In this study, we used the wingpolymorphic cricket Gryllus firmus to test how expression of the flight capability versus reproduction trade-off was modified across a heterogeneous protein-carbohydrate nutritional landscape. Newly molted adult female long-and short-winged crickets were given one of 13 diets with different concentrations and ratios of protein and digestible carbohydrate; for each cricket, we measured consumption patterns, growth and allocation to reproduction (ovary mass) versus flight muscle maintenance (flight muscle mass and somatic lipid stores). Feeding responses in both morphs were influenced more by total macronutrient concentration than by protein-carbohydrate ratio, except at high-macronutrient concentration, where proteincarbohydrate balance was important. Mass gain tended to be greatest on protein-biased diets for both morphs, but was consistently lower across all diets for long-winged females. When long-winged females were fed high-carbohydrate foods, they accumulated greater somatic lipid stores; on high-protein foods, they accumulated greater somatic protein stores. Food protein-carbohydrate content also affected shortwinged females (selected for early reproductive onset), which showed dramatic increases in ovary size, including ovarian stores of lipid and protein, on protein-biased foods. This is the first study to show how the concentration and ratio of dietary protein and carbohydrate affects consumption and allocation to key physiological features associated with the reproduction-dispersal life-history trade-off.

Summary1. Nutrient regulation should covary with life history, but actual demonstrations of this connection are rare. 2. Here, we use a wing-polymorphic cricket, Gryllus firmus, that trades off dispersal and reproduction; the long-winged morph with functional flight muscles [LW(f)] is adapted for dispersal at the expense of egg production, while the short-winged (SW) morph is adapted for egg production at the expense of flight. We explore the extent to which these two morphs differentially regulate macronutrient intake to best match their life-history strategy. 3. In a 'choice' experiment, we offered female crickets of each morph [LW(f) and SW] two nutritionally complementary foods varying in protein and digestible carbohydrate content. In a second 'no-choice' experiment, we confined crickets to one of five foods, each with a different protein/carbohydrate ratio. In both experiments, and for both morphs, we measured food intake, mass gain and lipid concentration. 4. In the 'choice' experiments, LW(f) females selected a more carbohydrate-biased diet than SW females. The two morphs gained similar total mass, but the LW morph had higher lipid concentration. 5. In the no-choice experiment, the two morphs practised different nutrient 'consumption rules'. SW females ate similar total nutrient amounts (protein plus carbohydrate) across diets, while LW(f) females decreased intake as the protein/carbohydrate ratio of the available food became increasingly imbalanced. Overall mass gain was marginally higher in the SW morph and lowest for both morphs on the diets that were extremely carbohydrate biased. LW(f) and SW females had similar lipid concentrations across the diets, even though LW(f) crickets ate less carbohydrate on the two carbohydrate-biased diets. Our data suggest that for LW(f) females, there are costs of overeating nutrients in excess of requirements, but they are efficient at utilizing ingested nutrients. 6. Our results shed new light on how the nutritional environment interacts with the direct trade-off between dispersal and reproduction occurring in adult G. firmus crickets. Dispersal is linked to heightened diet selectivity and an emphasis on nutrients promoting flight fuel (lipid) storage over protein acquisition for egg laying, such that nutritional regulation complements the metabolic mechanisms that generate this trade-off.