Fungus growing ants

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De Souza et al. (2007) - The fungus-growing ants are a New World group of > 200 species, all obligate symbionts with a fungus they use for food. The These ants are found across the American continents and the West Indies.

Leal et al. (2011) - These ants are known as fungus growers because they maintain an obligate mutualism with fungi cultured inside their nests, and which is the only food source for the larvae and an important resource for the adult ants as well (Weber 1972). A wide variety of material can be used as substrate for fungus culturing (Holldobler and Wilson 1990, Rico-Gray and Oliveira 2007), and this variation can be used to categorize the genera into two groups based on their agricultural habits. The so-called lower genera include species that collect mainly fowers, fruits, insect corpses, and feces fallen in the vicinity of their nests (Leal and Oliveira 2000, Mehdiabadi and Schultz 2010). The higher genera include nonleaf-cutting species (genera Trachymyrmex and Sericomyrmex) that collect mostly fallen leaflets, fruit, and flowers, as well as the typical leafcutters that collect fresh leaves from shrubs and trees (genera Atta and Acromyrmex) (see Schultz and Brady 2008, Mehdiabadi and Schultz 2010).

Sosa-Cavlo et al. 2015. Figure 3.

Leaf-cutting ants are very well known due to their remarkable effects on vegetation as herbivores. For example, they can 1) remove up to 15% of the standing leaf crop (Wirth et al. 2003, Urbas et al. 2007) and up to 50% of the plant species in their foraging territory each year (Vasconcelos and Fowler 1990); 2) reduce the vegetation cover by up to 18% and increase light availability within foraging areas (Wirth et al. 2003); and 3) secondarily disperse seeds of forest and savanna plants (Leal and Oliveira 1998, Silva et al. 2007, Christianini and Oliveira 2009). Moreover, leaf-cutters are considered important ecosystem engineers because their huge nests can significantly alter soil attributes (Sternberg et al. 2007) and light regimes (Farji-Brener and Illes 2000), which in turn may influence forest structure, composition, and dynamics (Correa et al. 2010), even after 15 yr of colony death or nest abandonment (Bieber et al. 2010).

Although nonleaf-cutters comprise a diverse and abundant group of fungus-growing ants, only more recently the general biology of these less conspicuous species have been investigated in greater detail (Fernandez-Marín et al. 2004, Pitts-Singer and Espelie 2007, Adams and Longino 2007, Diehl-Fleig and Diehl 2007, Klingenberg and Brandao 2009, Solomon et al. 2011). Lack of field data are probably due to their small colonies and the small size and discrete habit of foragers, which make them less noticeable in nature (Weber 1972, Holldobler and Wilson 2011). Perhaps most importantly, because nonleaf-cutters use mostly fallen plant material and feces as substrate for fungus culturing, their impact on vegetation and economic importance as crop pests is irrelevant compared with leaf-cutting Atta and Acromyrmex (Vander Meer et al. 1990, Wirth et al. 2003, and references therein).

Sapountzis et al. (2018) - The leaf-cutting ants are the crown group of the attine fungus-growing ants, a monophyletic tribe that evolved 55–60 MYA when their ancestor switched from a hunter-gatherer lifestyle to an exclusive fungal diet (Nygaard et al., 2016; Branstetter et al., 2017). The evolutionarily derived attine lineages rear fully domesticated and co-adapted fungal cultivars that provide the ant farmers with specialized hyphal tips (gongylidia) containing mostly carbohydrates and lipids that the workers harvest and digest (De Fine Licht et al., 2014; Quinlan and Cherrett, 1979). The ant brood is completely dependent on the ingestion of fungal biomass (Ho¨lldobler and Wilson, 1990), but workers may ingest and assimilate liquids as well (Littledyke and Cherrett, 1976; Shik et al., 2018). However, similar to other ants, they cannot ingest solid plant or animal fragments that they collect to provision their fungus gardens because a sieve in the infrabuccal cavity filters out any particles in excess of ca. 100 mm (Mueller et al., 2001). This obligate reciprocity between cultivation and nutrition facilitated further innovations in the terminal clade of Acromyrmex and Atta leaf-cutting ants, which evolved 15-20 MYA (Nygaard et al., 2016; Branstetter et al., 2017). These two genera obtained functionally polyploid cultivars (Kooij et al., 2015), adopted multiple queen-mating so their colonies became genetic chimeras (Villesen et al., 2002), and became herbivores with massive ecological footprints in Latin America (Schultz and Brady, 2008; Mehdiabadi and Schultz, 2010; Schiøtt et al., 2010; Leal et al., 2014; Shik et al., 2014).

Previous studies have shown that Acromyrmex and Atta leaf-cutting ants harbor low-diversity microbiomes, which include Wolbachia (only in Acromyrmex), Mollicutes and hindgut Rhizobiales (Van Borm et al., 2002; Andersen et al., 2012; Sapountzis et al., 2015; Meirelles et al., 2016), symbionts that were inferred to possibly complement the nitrogen-poor diets of Acromyrmex leaf-cutting ants (Sapountzis et al., 2015). Depending on the actual species studied, Mollicutes – tiny bacteria that lack a cell-wall – can often be found as abundant endosymbionts in up to 100% of leaf-cutting ant colonies (Sapountzis et al., 2015; Meirelles et al., 2016; Zhukova et al., 2017), but the absence of in-depth genomic studies has precluded more than speculation about their putative roles as either parasites (Meirelles et al., 2016) or mutualists (Sapountzis et al., 2015).

See this chapter of The Ants for a general overview of these intriguing ants.

Ant-Fungus mutualism

The evolution and maintenance of the complex mutualism between fungus growing ants and the fungi they cultivate is an intriguing area of study. While much has been discovered about the ants, the coevolution between fungus growing ants and their fungi is a rich study area that is being explored by numerous labs and researchers.

Bacteria are also an integral part of these co-evolved relationships.

Here are some examples:

Fungal Ploidy

Flowering plants are rife with species that exhibit polyploidy, i.e., possess more than two sets of chromosomes. The evolutionary basis and potential fitness advantages of this condition have been explored for many decades. Kooij et al. (2015) discovered analogous duplications of genetic material in attine fungi. They examined fungi samples that were representatives of the different evolutionary stages of fungus farming, i.e., higher attine ants with domesticated gongylidia-bearing fungi and lower- and paleo-attine ants growing fungi without obvious adaptations to being crops.

They found: Domesticated symbionts of higher attine ants are polykaryotic with 7–17 nuclei per cell, whereas nonspecialized crops of lower attines are dikaryotic similar to most free-living basidiomycete fungi. Our opposite ploidy models indicated that the symbionts of Trachymyrmex and Sericomyrmex are likely to be lowly and facultatively polyploid (just over two haplotypes on average), whereas Atta and Acromyrmex symbionts are highly and obligatorily polyploid (ca. 5–7 haplotypes on average). Genetic variation, as shown by examining variation in microsatellite loci revealed the polykaryotic symbionts of the basal higher attine genera Trachymyrmex and Sericomyrmex was only slightly enhanced, but the evolutionarily derived crop fungi of Atta and Acromyrmex leaf-cutting ants had much higher genetic variation. This stepwise transition appears analogous to ploidy variation in plants and fungi domesticated by humans and in fungi domesticated by termites and plants, where gene or genome duplications were typically associated with selection for higher productivity but allopolyploid chimerism was incompatible with sexual reproduction.

Atta, Acromyrmex, and fungi

Mueller et al. (2017) explored the biodiversity and biogeography of fungal cultivars within the genera Atta and Acromyrmex:

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.

Social Parasitism

De Souza et al. (2007) - Social parasitism, the exploitation of the nest of another species without contributing to colony maintenance, for example the cultivation of a fungus garden, has been reported occasionally in the attine ants. Megalomyrmex species can coexist as social parasites in attine colonies, consuming the fungus garden (Brandão, 1990; Adams et al., 2000). Gnamptogenys hartmani is also a specialized agro-predator of Trachymyrmex and Sericomyrmex fungus-growing ants in Panama (Dijkstra & Boomsma, 2003). Five taxa are known to be social parasites of other Acromyrmex species, living in and feeding on their fungus gardens, but not contributing to its maintenance: Pseudoatta argentina and Pseudoatta argentina platensis (parasites of Acromyrmex lundii, Acromyrmex heyeri and possibly Acromyrmex balzani), and Pseudoatta sp. (a parasite of Acromyrmex rugosus) produce no worker caste (Santschi, 1926; Bruch, 1928; Gallardo, 1929; Delabie et al., 1993). Rabeling and Bacci (2010) have discovered a workerless inquiline species Mycocepurus castrator that parasitizes Mycocepurus goeldii. In contrast, the recently discovered Acromyrmex insinuator (a parasite of Acromyrmex echinatior) does produce workers (Schultz et al., 1998). Sumner et al. (2004) found that Pseudoatta sp. was not closely related to its host, but A. insinuator was closely related to its host, A. echinatior. Acromyrmex ameliae, a social parasite of Acromyrmex subterraneus in Minas Gerais, Brasil. Like A. insinuator, it produces workers and appears to be closely related to its hosts.

Rabeling et al. 2019. In general, inquiline social parasites preferentially produce sexual offspring and have lost the sterile worker caste. Host queen tolerance is observed in all inquiline parasites of fungus-growing ants (Schultz et al. 1998; De Souza et al. 2007; Rabeling and Bacci 2010; Rabeling et al. 2015, Rabeling et al. 2019), except for Pseudoatta argentina, which either kills the host queen(s) or preferentially parasitizes queenless host colonies (Bruch 1928; Gallardo 1929; Rabeling and Bollazzi, unpubl. data).

The parasitic fungus-growing ants, Pseudoatta argentina, Mycocepurus castrator, and Acromyrmex charruanus have lost their worker caste (Gallardo 1916; Rabeling and Bacci 2010; Rabeling et al. 2015), whereas Acromyrmex ameliae and Acromyrmex insinuator still maintain a reduced number of workers in their colonies (Schultz et al. 1998; Bekkevold and Boomsma 2000; De Souza et al. 2007; Soares et al. 2011).

Acromyrmex social parasites (A. fowleri, A. insinuator, A. ameliae, and A. charruanus, any others???) are an example of parallel evolution and show a mosiac pattern of parasitic species evolution. No all of these parasites are specialized to the same degree. A congeneric mosaic of parasitic traits exhibits striking parallels the evolution of inquiline social parasites in the ant genus Pheidole (Wilson 1984). Morphologically less specialized inquilines are known to conduct mating flights (Schultz et al. 1998; Soares et al. 2010; De Souza et al. 2011; Rabeling et al. 2015), whereas the highly specialized inquiline parasites with adelphogamous males (xxxP. argentina and M. castrator) mate inside the host colony, presumably with their siblings (Bruch 1928; Gallardo 1929; Rabeling and Bacci 2010).

The male of Acromyrmex fowleri resembles the male of A. rugosus closely, and interestingly, the male of A. fowleri is not gynaecomorphic. In contrast, the males of many highly modified inquiline social parasites resemble the queen caste or become pupoid (Wilson 1971). The males of Pseudoatta argentina and Mycocepurus castrator are gynaecomorphic and closely resemble the queen, whereas the males of all other attine inquilines can be clearly recognized as Acromyrmex males (Rabeling and Bacci 2010).

Delabie’s observations that the fungus garden of parasitized A. rugosus colonies looked healthy and showed no evidence of colony decline provide circumstantial evidence for semelparous reproduction of the parasite A. fowleri, similar to M. castrator (Rabeling and Bacci 2010). In contrast, Acromyrmex insinuator and Acromyrmex charruanus reproduce iteroparously and the host colonies do not seem to be able to recover from the mass production of parasite alates and collapse after the parasites’ nuptial flights (Bekkevold and Boomsma 2000; Rabeling et al. 2015).

Culturing Laboratory Colonies

Sosa-Cavlo et al. (2015) presented an excellent synthesis of their collective experience, including numerous methods others have developed and they have refined, finding and collecting whole nests of fungus growing ants for their eventual culturing of whole colonies in the lab. If you are interested in studying fungus growing ants and want to find colonies in the field or are interested in maintaining laboratory colonies but need to know what you need to set up and maintain them, this paper is an excellent source of information.

Sosa-Cavlo et al. 2015. Figure 9.