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Symbiotic Adaptations in the Fungal Cultivar of Leaf-Cutting Ants
ARTICLE Received 15 Apr 2014 | Accepted 24 Oct 2014 | Published 1 Dec 2014 DOI: 10.1038/ncomms6675 Symbiotic adaptations in the fungal cultivar of leaf-cutting ants Henrik H. De Fine Licht1,w, Jacobus J. Boomsma2 & Anders Tunlid1 Centuries of artificial selection have dramatically improved the yield of human agriculture; however, strong directional selection also occurs in natural symbiotic interactions. Fungus- growing attine ants cultivate basidiomycete fungi for food. One cultivar lineage has evolved inflated hyphal tips (gongylidia) that grow in bundles called staphylae, to specifically feed the ants. Here we show extensive regulation and molecular signals of adaptive evolution in gene trancripts associated with gongylidia biosynthesis, morphogenesis and enzymatic plant cell wall degradation in the leaf-cutting ant cultivar Leucoagaricus gongylophorus. Comparative analysis of staphylae growth morphology and transcriptome-wide expressional and nucleotide divergence indicate that gongylidia provide leaf-cutting ants with essential amino acids and plant-degrading enzymes, and that they may have done so for 20–25 million years without much evolutionary change. These molecular traits and signatures of selection imply that staphylae are highly advanced coevolutionary organs that play pivotal roles in the mutualism between leaf-cutting ants and their fungal cultivars. 1 Microbial Ecology Group, Department of Biology, Lund University, Ecology Building, SE-223 62 Lund, Sweden. 2 Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark. w Present Address: Section for Organismal Biology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg, Denmark. Correspondence and requests for materials should be addressed to H.H.D.F.L. -
Nutrition Mediates the Expression of Cultivar–Farmer Conflict in a Fungus-Growing Ant
Nutrition mediates the expression of cultivar–farmer conflict in a fungus-growing ant Jonathan Z. Shika,b,1, Ernesto B. Gomezb, Pepijn W. Kooija,c, Juan C. Santosd, William T. Wcislob, and Jacobus J. Boomsmaa aCentre for Social Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark; bSmithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama; cJodrell Laboratory, Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, Richmond TW9 3DS, United Kingdom; and dDepartment of Biology, Brigham Young University, Provo, UT 84602 Edited by Bert Hölldobler, Arizona State University, Tempe, AZ, and approved July 8, 2016 (received for review April 16, 2016) Attine ants evolved farming 55–60 My before humans. Although whose sexual fruiting bodies represent considerable investments. evolutionarily derived leafcutter ants achieved industrial-scale farm- An illustrative example is offered by the fungus-growing attine ing, extant species from basal attine genera continue to farm loosely ants, whose dispersing queens transmit symbionts vertically and domesticated fungal cultivars capable of pursuing independent re- whose farming workers therefore actively suppress wasteful for- productive interests. We used feeding experiments with the basal mation of inedible mushrooms (16, 17). Another example is pro- attine Mycocepurus smithii to test whether reproductive allocation vided by two independently derived lineages of fungus-growing Termitomyces conflicts between farmers and cultivars -
Sociobiology 63(3): 894-908 (September, 2016) DOI: 10.13102/Sociobiology.V63i3.1043
View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Portal de Periódicos Eletrônicos da Universidade Estadual de Feira de Santana (UEFS) Sociobiology 63(3): 894-908 (September, 2016) DOI: 10.13102/sociobiology.v63i3.1043 Sociobiology An international journal on social insects REsearch article - AnTs Amazon Rainforest Ant-Fauna of Parque Estadual do Cristalino: Understory and Ground- Dwelling Ants RE Vicente1, LP Prado2, TJ Izzo1 1 - Universidade Federal de Mato Grosso, Cuiabá-MT, Brazil 2 - Museu de Zoologia da Universidade de São Paulo, São Paulo-SP, Brazil Article History Abstract Ants are ecologically dominant and have been used as valuable bio-indicators Edited by of environmental change or disturbance being used in monitoring inventories. Frederico S. Neves, UFMG, Brazil Received 12 April 2016 However, the majority of inventories have concentrated on ground-dwelling Initial acceptance 28 May 2016 ant fauna disregarding arboreal fauna. This paper aimed to list the ant species Final acceptance 22 July 2016 collected both on the ground and in the vegetation of the Parque Estadual do Publication date 25 October 2016 Cristalino, an important protected site in the center of the southern Amazon. Moreover, we compared the composition of the ground dwelling and vegetation Keywords Arboreal ants, Conservation, Diversity, foraging ants. Two hundred and three (203) species distributed among 23 genera Formicidae, Inventory. and eight subfamilies were sampled, wherein 34 species had not yet been reported in the literature for Mato Grosso State. As expected, the abundance Corresponding author and richness of ants was higher on the ground than in the understory. -
The Coexistence
Myrmecological News 13 37-55 2009, Online Earlier Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini) Natasha J. MEHDIABADI & Ted R. SCHULTZ Abstract Ants of the tribe Attini comprise a monophyletic group of approximately 230 described and many more undescribed species that obligately depend on the cultivation of fungus for food. In return, the ants nourish, protect, and disperse their fungal cultivars. Although all members of this tribe cultivate fungi, attine ants are surprisingly heterogeneous with regard to symbiont associations and agricultural system, colony size and social structure, nesting behavior, and mating system. This variation is a key reason that the Attini have become a model system for understanding the evolution of complex symbioses. Here, we review the natural-history traits of fungus-growing ants in the context of a recently published phylo- geny, collating patterns of evolution and symbiotic coadaptation in a variety of colony and fungus-gardening traits in a number of major lineages. We discuss the implications of these patterns and suggest future research directions. Key words: Hymenoptera, Formicidae, fungus-growing ants, leafcutter ants, colony life, natural history, evolution, mating, agriculture, review. Myrmecol. News 13: 37-55 (online xxx 2008) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 12 June 2009; revision received 24 September 2009; accepted 28 September 2009 Dr. Natasha J. Mehdiabadi* (contact author) & Dr. Ted R. Schultz* (contact author), Department of Entomology and Laboratories of Analytical Biology, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, NHB, CE518, MRC 188, Washington, DC 20013-7012, USA. E-mail: [email protected]; [email protected] * Both authors contributed equally to the work. -
Nutrition Mediates the Expression of Cultivar–Farmer Conflict in a Fungus-Growing Ant
Nutrition mediates the expression of cultivar–farmer conflict in a fungus-growing ant Jonathan Z. Shika,b,1, Ernesto B. Gomezb, Pepijn W. Kooija,c, Juan C. Santosd, William T. Wcislob, and Jacobus J. Boomsmaa aCentre for Social Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark; bSmithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama; cJodrell Laboratory, Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, Richmond TW9 3DS, United Kingdom; and dDepartment of Biology, Brigham Young University, Provo, UT 84602 Edited by Bert Hölldobler, Arizona State University, Tempe, AZ, and approved July 8, 2016 (received for review April 16, 2016) Attine ants evolved farming 55–60 My before humans. Although whose sexual fruiting bodies represent considerable investments. evolutionarily derived leafcutter ants achieved industrial-scale farm- An illustrative example is offered by the fungus-growing attine ing, extant species from basal attine genera continue to farm loosely ants, whose dispersing queens transmit symbionts vertically and domesticated fungal cultivars capable of pursuing independent re- whose farming workers therefore actively suppress wasteful for- productive interests. We used feeding experiments with the basal mation of inedible mushrooms (16, 17). Another example is pro- attine Mycocepurus smithii to test whether reproductive allocation vided by two independently derived lineages of fungus-growing Termitomyces conflicts between farmers and cultivars -
Hymenoptera: Formicidae), with a Discussion of Social Parasitism in Fungus-Growing Ants
Systematic Entomology (2010), 35, 379–392 A new workerless inquiline in the Lower Attini (Hymenoptera: Formicidae), with a discussion of social parasitism in fungus-growing ants CHRISTIAN RABELING1 and MAURICIO´ BACCI Jr.2 1Section of Integrative Biology, The University of Texas, Austin, TX, U.S.A. and 2Center for the Study of Social Insects, Sao˜ Paulo State University, Rio Claro, SP, Brazil Abstract. Ant inquilines are obligate social parasites, usually lacking a sterile worker caste, which are dependent on their hosts for survival and reproduction. Social parasites are rare among the fungus-gardening ants (Myrmicinae: tribe Attini) and only four species are known until now, all being inquilines from the Higher Attini. We describe Mycocepurus castrator sp.n., the first inquiline social parasite to be discovered in the Lower Attini. Our study of the parasite’s behaviour and life history supports the conclusion drawn from external morphology: Mycocepurus castrator is an evolutionarily derived inquiline parasite of Mycocepurus goeldii. Inquilines are of great interest to evolutionary biology because it is debated if they originated via sympatric or allopatric speciation. We discuss the life history evolution, behaviour and morphology of socially parasitic, fungus-growing ants. Introduction sufficient workers of the parasitic species are produced, the colony becomes independent of the host. (ii) Dulotic or slave- Societies of all social organisms are defined by reproduc- making parasites steal worker brood from host colonies and tive division of labour, co-operative brood care and overlap- the emerging host workers provide social tasks (i.e. brood care, ping generations (Batra, 1966; Mitchener, 1969; Wilson, 1971; foraging, nest hygiene) that ensure the parasite colony’s sur- Holldobler¨ & Wilson, 1990). -
Reconstructing the Functions of Endosymbiotic Mollicutes in Fungus
RESEARCH ARTICLE Reconstructing the functions of endosymbiotic Mollicutes in fungus- growing ants Panagiotis Sapountzis*, Mariya Zhukova, Jonathan Z Shik, Morten Schiott, Jacobus J Boomsma* Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark Abstract Mollicutes, a widespread class of bacteria associated with animals and plants, were recently identified as abundant abdominal endosymbionts in healthy workers of attine fungus- farming leaf-cutting ants. We obtained draft genomes of the two most common strains harbored by Panamanian fungus-growing ants. Reconstructions of their functional significance showed that they are independently acquired symbionts, most likely to decompose excess arginine consistent with the farmed fungal cultivars providing this nitrogen-rich amino-acid in variable quantities. Across the attine lineages, the relative abundances of the two Mollicutes strains are associated with the substrate types that foraging workers offer to fungus gardens. One of the symbionts is specific to the leaf-cutting ants and has special genomic machinery to catabolize citrate/glucose into acetate, which appears to deliver direct metabolic energy to the ant workers. Unlike other Mollicutes associated with insect hosts, both attine ant strains have complete phage-defense systems, underlining that they are actively maintained as mutualistic symbionts. DOI: https://doi.org/10.7554/eLife.39209.001 *For correspondence: [email protected] (PS); Introduction [email protected] (JJB) Bacterial endosymbionts, defined here as comprising both intra- and extra-cellular symbionts Competing interests: The (Bourtzis and Miller, 2006), occur in all eukaryotic lineages and range from parasites to mutualists authors declare that no (Bourtzis and Miller, 2006; Martin et al., 2017). -
Kellner Et Al. 2017
Author's personal copy Microbial Ecology https://doi.org/10.1007/s00248-017-1124-6 HOST MICROBE INTERACTIONS Symbiont-Mediated Host-Parasite Dynamics in a Fungus-Gardening Ant Katrin Kellner1,2 & M. R. Kardish1,3 & J. N. Seal1,2 & T. A. Linksvayer4 & U. G. Mueller1 Received: 20 June 2017 /Accepted: 1 December 2017 # Springer Science+Business Media, LLC, part of Springer Nature 2017 Abstract Group-living can promote the evolution of adaptive strategies to prevent and control disease. Fungus-gardening ants must cope with two sets of pathogens, those that afflict the ants themselves and those of their symbiotic fungal gardens. While much research has demonstrated the impact of specialized fungal pathogens that infect ant fungus gardens, most of these studies focused on the so-called higher attine ants, which are thought to coevolve diffusely with two clades of leucocoprinaceous fungi. Relatively few studies have addressed disease ecology of lower Attini, which are thought to occasionally recruit (domesticate) novel leucocoprinaceous fungi from free-living populations; coevolution between lower-attine ants and their fungi is therefore likely weaker (or even absent) than in the higher Attini, which generally have many derived modifications. Toward understanding the disease ecology of lower-attine ants, this study (a) describes the diversity in the microfungal genus Escovopsis that naturally infect fungus gardens of the lower-attine ant Mycocepurus smithii and (b) experimentally determines the relative contributions of Escovopsis strain (a possible garden disease), M. smithii ant genotype, and fungal cultivar lineage to disease susceptibility and colony fitness. In controlled in-vivo infection laboratory experiments, we demonstrate that the susceptibility to Escovopsis infection was an outcome of ant-cultivar-Escovopsis interaction, rather than solely due to ant genotype or fungal cultivar lineage. -
(Hymenoptera: Formicidae) in Atlantic Forest in Southern Brazil
Anais da Academia Brasileira de Ciências (2017) 89(4): 2719-2729 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201720160892 www.scielo.br/aabc | www.fb.com/aabcjournal Richness and structure of ant assemblies (Hymenoptera: Formicidae) in Atlantic forest in southern Brazil JUNIR A. LUTINSKI1, CLADIS J. LUTINSKI2, CARIN GUARDA1, MARIA A. BUSATO1 and FLÁVIO R.M. GARCIA3 1Programa de Pós-Graduação em Ciências da Saúde, Universidade Comunitária da Região de Chapecó/ UNOCHAPECÓ, Av. Senador Attílio Fontana, 591-E, Efapi, Caixa Postal 1141, 89809-000 Chapecó, SC, Brazil 2Departamento de Biologia, Universidade Federal da Fronteira Sul/UFFS, Av. Fernando Machado, 108 E, 89802-112 Chapecó, SC, Brazil 3Programa de Pós-Graduação em Entomologia, Universidade Federal de Pelotas/UFPel, Instituto de Biologia, Porto, Caixa Postal 354, 96010-900 Pelotas, RS, Brazil Manuscript received on December 22, 2016; accepted for publication on August 14, 2017 ABSTRACT Ant diversity is influenced by the structural complexity of the environment. Ants are thus an ecologically important group due to their potential to serve as indicators of environmental quality. The objective of this study was to evaluate ant diversity in areas with different land use histories and thus, within different stages of regeneration in the Permanent Preservation Area of the Foz do Chapecó Hydroelectric Plant reservoir. Ant assemblies among sample sites were compared using rarefaction analysis, and estimated richness, frequency of occurrence, and relative abundance were calculated. Associations between species and sample sites were evaluated using Principal Component Analysis (PCA). -
Rabeling, C. 2020. Social Parasitism. In
S Social Parasitism life cycle, such as colony founding, but are other- wise able to live independently without the host’s Christian Rabeling help. Alternatively, social parasites can be obli- School of Life Sciences, Arizona State University, gately dependent on their hosts’ social behavior. Tempe, AZ, USA Among the Hymenoptera, social parasitism is commonly found in ants, social bees, and social wasps [25] (Figs. 1–4). However, it is not always In the broadest sense, social parasitism is a form of easy to recognize a true social parasite because brood parasitism, where the social parasite insect societies are readily exploited by scaven- depends on the social behavior of the host for gers, parasites, and predators, and consequently, survival and reproduction. Brood parasitism is nests of social insects are riddled with “guests” known from a variety of vertebrate species, such [10, 25]. Although highly intriguing and directly as mammals, birds, and fishes, where the host’s relevant to understanding the rich biology of brood care behavior is exploited by the parasite. social parasites, this overview primarily focuses Brood parasitism has been studied in great detail on interspecific social parasitism among eusocial in some bird species, including cuckoos, cow Hymenoptera. Other symbiotic interactions birds, and honeyguides, where parasites lay their between social insects and other organisms, such eggs into the nests of the host, deceiving the host as intraspecific parasitism (which is probably a into providing parental care for their offspring. widespread but often overlooked form of social In social insects, social parasites also exploit parasitism occurring in polygynous colonies of a the brood care behavior of their hosts and can single species), myrmecophily, interactions therefore be regarded as brood parasites. -
Myrmecological News Myrmecologicalnews.Org
Myrmecological News myrmecologicalnews.org Myrmecol. News 30 Digital supplementary material Digital supplementary material to DE LA MORA, A., SANKOVITZ, M. & PURCELL, J. 2020: Ants (Hymenoptera: Formicidae) as host and intruder: recent advances and future directions in the study of exploitative strategies. – Myrmecological News 30: 53-71. The content of this digital supplementary material was subject to the same scientific editorial processing as the article it accompanies. However, the authors are responsible for copyediting and layout. Supporting Material for: de la Mora, Sankovitz, & Purcell. Ants (Hymenoptera: Formicidae) as host and intruder: recent advances and future directions in the study of exploitative strategies Table S1: This table summarizes host/parasite relationships that have been described or discussed in the literature since 2000. Host and parasite nomenclature is up‐to‐date based on AntWeb.org, but note that some of the taxonomy is controversial and/or not fully resolved. Names are likely to change further in coming years. Due to changing nomenclature, it can be challenging to track which species have been well‐studied. We provide recently changed species and genus names parenthetically. In addition, we have split this table to show recent taxonomic revisions, compilations (e.g. tables in empirical papers), reviews, books, or species descriptions supporting relationships between hosts and parasites in one column and articles studying characteristics of host/parasite relationships in a second column. For well‐studied species, we limit the ‘primary research’ column to five citations, which are selected to cover different topics and different research teams when such diverse citations exist. Because of the active work on taxonomy in many groups, some misinformation has been inadvertently propagated in previous articles. -
Symbiotic Bacterial Communities in Rainforest Fungus-Farming Ants: Evidence for Species and Colony Specifcity Mariane U
www.nature.com/scientificreports OPEN Symbiotic bacterial communities in rainforest fungus-farming ants: evidence for species and colony specifcity Mariane U. V. Ronque 1 ✉ , Mariana L. Lyra 2, Gustavo H. Migliorini 3, Maurício Bacci Jr 4 & Paulo S. Oliveira 5 Animals may host diverse bacterial communities that can markedly afect their behavioral physiology, ecology, and vulnerability to disease. Fungus-farming ants represent a classical example of mutualism that depends on symbiotic microorganisms. Unraveling the bacterial communities associated with fungus-farming ants is essential to understand the role of these microorganisms in the ant-fungus symbiosis. The bacterial community structure of fve species of fungus-farmers (non-leaf-cutters; genera Mycocepurus, Mycetarotes, Mycetophylax, and Sericomyrmex) from three diferent environments in the Brazilian Atlantic rainforest (lowland forest, restinga forest, and sand dunes) was characterized with amplicon-based Illumina sequencing of 16 S ribosomal RNA gene. Possible diferences in bacterial communities between ants internal to the nest (on the fungus garden) and external foragers were also investigated. Our results on the richness and diversity of associated bacteria provide novel evidence that these communities are host- and colony-specifc in fungus-farming ants. Indeed, the bacterial communities associated with external foragers difer among the fve species, and among colonies of the same species. Furthermore, bacterial communities from internal ants vs. foragers do not difer or difer only slightly within each ant species. This study highlights the importance of describing ant-associated bacterial communities to better understand this host-bacterial interaction in the social environment of insect colonies and provides the foundation for future studies on the ecological and evolutionary processes that drive the success of fungus-farming ants.