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Karyotype Diversity, Mode, and Tempo of the Chromosomal Evolution of Attina (Formicidae: Myrmicinae: Attini): Is There an Upper Limit to Chromosome Number?

ABSTRACT: Ants are an important insect group that exhibits considerable diversity in chromosome numbers. Some species show only one chromosome, as in the males of the Australian bulldog ant Myrmecia croslandi, while some have as many as 60 chromosomes, as in the males of the giant Neotropical ant Dinoponera lucida. Fungus-growing ants are a diverse group in the Neotropical ant fauna, engaged in a symbiotic relationship with a basidiomycete fungus, and are widely distributed from Nearctic to Neotropical regions. Despite their importance, new chromosome counts are scarcely reported, and the marked variation in chromosome number across species has been poorly studied under phylogenetic and genome evolutionary contexts. Here, we present the results of the cytogenetic examination of fungus-farming ants and compile the cytogenetic characteristics and genome size of the species studied to date to draw insights regarding the evolutionary paths of karyotype changes and diversity. These data are coupled with a fossil-calibrated phylogenetic tree to discuss the mode and tempo of chromosomal shifting, considering whether there is an upper limit for chromosome number and genome size in ants, using fungus-farming ants as a model study. We recognize that karyotypes are generally quite variable across fungus-farming ant phylogeny, mostly between genera, and are more numerically conservative within genera. A low chromosome number, between 10 and 12 chromosomes, seems to present a notable long-term evolutionary stasis (intermediate evolutionary stasis) in fungus-farming ants. All the genome size values were inside a limited spectrum below 1 pg. Eventual departures in genome size occurred with regard to the mean of 0.38 pg, indicating that there is a genome, and likely a chromosome, number upper limit.

SUBMITTER: Cardoso DC

PROVIDER: S-EPMC8707115 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Attine ants cultivate fungi as their most important food source and in turn the fungus is nourished, protected against harmful microorganisms, and dispersed by the ants. This symbiosis evolved approximately 50-60 million years ago in the late Paleocene or early Eocene, and since its origin attine ants have acquired a variety of fungal mutualists in the Leucocoprineae and the distantly related Pterulaceae. The most specialized symbiotic interaction is referred to as "higher agriculture" and includes leafcutter ant agriculture in which the ants cultivate the single species Leucoagaricus gongylophorus. Higher agriculture fungal cultivars are characterized by specialized hyphal tip swellings, so-called gongylidia, which are considered a unique, derived morphological adaptation of higher attine fungi thought to be absent in lower attine fungi. Rare reports of gongylidia-like structures in fungus gardens of lower attines exist, but it was never tested whether these represent rare switches of lower attines to L. gonglyphorus cultivars or whether lower attine cultivars occasionally produce gongylidia. Here we describe the occurrence of gongylidia-like structures in fungus gardens of the asexual lower attine ant Mycocepurus smithii. To test whether M. smithii cultivates leafcutter ant fungi or whether lower attine cultivars produce gongylidia, we identified the M. smithii fungus utilizing molecular and morphological methods. Results shows that the gongylidia-like structures of M. smithii gardens are morphologically similar to gongylidia of higher attine fungus gardens and can only be distinguished by their slightly smaller size. A molecular phylogenetic analysis of the fungal ITS sequence indicates that the gongylidia-bearing M. smithii cultivar belongs to the so-called "Clade 1"of lower Attini cultivars. Given that M. smithii is capable of cultivating a morphologically and genetically diverse array of fungal symbionts, we discuss whether asexuality of the ant host maybe correlated with low partner fidelity and active symbiont choice between fungus and ant mutualists.

Project description:In ants, dispersal strategies and morphology of female sexuals are generally linked to the mode of colony founding. In species using long-range dispersal tactics, queen/worker dimorphism is generally high and young queens are able to initiate new colonies by themselves, using their metabolic reserves. By contrast, in species using short-range dispersal strategies, queen/worker dimorphism is generally low and, due to their limited metabolic reserves, queens have lost the capacity to raise their brood alone and to found their colony independently. Moreover, polygyny is also often associated with short-range dispersal strategies, although the relationship between the number of queens and the dispersal strategy in ants is not clear-cut. Here, dispersal strategies were investigated in C. pygmaea, a highly polygynous and polydomous ant species from northeastern Brazil. Field observations and laboratory experiments show that this ant exhibits a suite of traits that are more commonly associated with long-range dispersal and independent colony foundation: functional wings in both males and females, high queen/worker dimorphism, strong weight loss in mature queens, nuptial flights and, in the lab, ability of young queens to found new colonies in haplometrotic conditions. On the other hand, this species shows a high degree of polygyny with a strong seasonal component, and, at least under laboratory conditions, mature queens seem able to develop propagules if they are accompanied by at least 10 workers. These features strongly suggest that (1) some of the gynes do not engage in a long-range dispersal but become new queens in their mother colony and (2) that budding events are possible in this species. We therefore speculate that C. pygmaea has a dual dispersal strategy probably related to environmental conditions: some gynes engage in long-range dispersal followed by independent colony foundation at the beginning of rainy season, while others mate in the parental colony and are re-adopted leading to high polygyny. During the rainy season, budding events can lead to colony extension and increased polydomy. Polydomy is commonly thought to improve resource discovery and exploitation through decentralized foraging behavior, a significant advantage during the rainy season when food ressources (mainly floral/extrafloral nectaries and hemipteran honeydew) are more abundant and when colony needs for food supplies are highest.

Dataset Information

Karyotype Diversity, Mode, and Tempo of the Chromosomal Evolution of Attina (Formicidae: Myrmicinae: Attini): Is There an Upper Limit to Chromosome Number?

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