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Variable interaction specificity and symbiont performance in Panamanian Trachymyrmex and Sericomyrmex fungus-growing ants.

ABSTRACT: BACKGROUND: Cooperative benefits of mutualistic interactions are affected by genetic variation among the interacting partners, which may have consequences for interaction-specificities across guilds of sympatric species with similar mutualistic life histories. The gardens of fungus-growing (attine) ants produce carbohydrate active enzymes that degrade plant material collected by the ants and offer them food in exchange. The spectrum of these enzyme activities is an important symbiont service to the host but may vary among cultivar genotypes. The sympatric occurrence of several Trachymyrmex and Sericomyrmex higher attine ants in Gamboa, Panama provided the opportunity to do a quantitative study of species-level interaction-specificity. RESULTS: We genotyped the ants for Cytochrome Oxidase and their Leucoagaricus fungal cultivars for ITS rDNA. Combined with activity measurements for 12 carbohydrate active enzymes, these data allowed us to test whether garden enzyme activity was affected by fungal strain, farming ants or combinations of the two. We detected two cryptic ant species, raising ant species number from four to six, and we show that the 38 sampled colonies reared a total of seven fungal haplotypes that were different enough to represent separate Leucoagaricus species. The Sericomyrmex species and one of the Trachymyrmex species reared the same fungal cultivar in all sampled colonies, but the remaining four Trachymyrmex species largely shared the other cultivars. Fungal enzyme activity spectra were significantly affected by both cultivar species and farming ant species, and more so for certain ant-cultivar combinations than others. However, relative changes in activity of single enzymes only depended on cultivar genotype and not on the ant species farming a cultivar. CONCLUSIONS: Ant cultivar symbiont-specificity varied from almost full symbiont sharing to one-to-one specialization, suggesting that trade-offs between enzyme activity spectra and life-history traits such as desiccation tolerance, disease susceptibility and temperature sensitivity may apply in some combinations but not in others. We hypothesize that this may be related to ecological specialization in general, but this awaits further testing. Our finding of both cryptic ant species and extensive cultivar diversity underlines the importance of identifying all species-level variation before embarking on estimates of interaction specificity.

SUBMITTER: De Fine Licht HH

PROVIDER: S-EPMC4262973 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Variable interaction specificity and symbiont performance in Panamanian Trachymyrmex and Sericomyrmex fungus-growing ants.

De Fine Licht Henrik H HH Boomsma Jacobus J JJ

BMC evolutionary biology 20141204

<h4>Background</h4>Cooperative benefits of mutualistic interactions are affected by genetic variation among the interacting partners, which may have consequences for interaction-specificities across guilds of sympatric species with similar mutualistic life histories. The gardens of fungus-growing (attine) ants produce carbohydrate active enzymes that degrade plant material collected by the ants and offer them food in exchange. The spectrum of these enzyme activities is an important symbiont serv ...[more]

PMID: 25471204

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Project description:BACKGROUND:Termites of the subfamily Macrotermitinae live in a mutualistic symbiosis with basidiomycete fungi of the genus Termitomyces. Here, we explored interaction specificity in fungus-growing termites using samples from 101 colonies in South-Africa and Senegal, belonging to eight species divided over three genera. Knowledge of interaction specificity is important to test the hypothesis that inhabitants (symbionts) are taxonomically less diverse than 'exhabitants' (hosts) and to test the hypothesis that transmission mode is an important determinant for interaction specificity. RESULTS:Analysis of Molecular Variance among symbiont ITS sequences across termite hosts at three hierarchical levels showed that 47 % of the variation occurred between genera, 18 % between species, and the remaining 35 % between colonies within species. Different patterns of specificity were evident. High mutual specificity was found for the single Macrotermes species studied, as M. natalensis was associated with a single unique fungal haplotype. The three species of the genus Odontotermes showed low symbiont specificity: they were all associated with a genetically diverse set of fungal symbionts, but their fungal symbionts showed some host specificity, as none of the fungal haplotypes were shared between the studied Odontotermes species. Finally, bilaterally low specificity was found for the four tentatively recognized species of the genus Microtermes, which shared and apparently freely exchanged a common pool of divergent fungal symbionts. CONCLUSION:Interaction specificity was high at the genus level and generally much lower at the species level. A comparison of the observed diversity among fungal symbionts with the diversity among termite hosts, indicated that the fungal symbiont does not follow the general pattern of an endosymbiont, as we found either similar diversity at both sides or higher diversity in the symbiont. Our results further challenge the hypothesis that transmission-mode is a general key-determinant of interaction specificity in fungus-growing termites.

Project description:Here we describe a new species of Trachymyrmex, T. pakawasp. n., from the Gran Sierra Plegada range of the Sierra Madre Oriental, in the states of Coahuila and Nuevo Leon, northeastern Mexico. Trachymyrmex pakawa is a large-sized species compared to other North American Trachymyrmex. Its geographic distribution includes the piedmont of the Gran Sierra Plegada at La Estanzuela, Monterrey, as well as peripheral mountains segregated from the Sierra Madre Oriental (Cerro de las Mitras, Sierra de Zapalinamé, Cañon de San Lorenzo, Cerro de las Letras). The preferred habitats of T. pakawa include oak-pine forest at La Estanzuela, xeric oak forest at Zapalinamé and mesic Chihuahuan desert scrub with sotol (Dasylirion) at other sites. All localities are on slopes, on very rocky, shallow lithosols overlaying large boulders. This species nests under and between large boulders and rocks. It has not been observed on alluvial or better developed, deeper soils, and it is absent from sites with human activity (urban, disturbed, and landscaped areas). It is closely related to and morphologically similar to Trachymyrmex smithi. The known distribution ranges of T. pakawa and T. smithi almost overlap in Saltillo, Coahuila state. The main character that distinguishes the new species from T. smithi is longer antennal scapes in T. pakawa; also, different nesting habits (rocky slopes vs. alluvial sites or deep sand in T. smithi), and geographic distribution. Phylogenetic analysis of DNA sequences from the mitochondrial marker cytochrome c oxidase subunit I (COI) and the first intron of the F1 copy of the nuclear protein-coding gene Elongation Factor 1- ? (EF1-?-F1) confirm a sister-species relationship between T. pakawa and T. smithi. Bayesian coalescent analyses indicate a divergence time of about 8.00 million years before present (95% confidence interval: 4.8-11.5 mya) between T. pakawa and T. smithi. The divergence of the lineages of T. pakawa and T. smithi could have been driven by the Pliocene-Holocene desertification of southwestern North America. This process resulted in isolated mesic refugia and forests in the Madrean ranges and piedmonts of northeastern Mexico (the current habitat of T. pakawa) while T. smithi adapted to the deeper, often sandy soils on the drier desert plains of Coahuila and Chihuahua states in Mexico, and New Mexico and Texas in the USA. Within the Nearctic species of the Trachymyrmex septentrionalis species group, T. pakawa is the species that is closest (by geographical distribution) to Neotropical species of Trachymyrmex like T. saussurei.

Dataset Information

Variable interaction specificity and symbiont performance in Panamanian Trachymyrmex and Sericomyrmex fungus-growing ants.

Publications

Variable interaction specificity and symbiont performance in Panamanian Trachymyrmex and Sericomyrmex fungus-growing ants.

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