The tight genome size of ants: diversity and evolution under ancestral state reconstruction and base composition

Abstract

The mechanisms and processes driving change and variation in the genome size (GS) are not well known, and only a small set of ant species has been studied. Ants are an ecologically successful insect group present in most distinct ecosystems worldwide. Considering their wide distribution and ecological plasticity in different environmental contexts, we aimed to expand GS estimation within Formicidae to examine distribution patterns and variation in GS and base composition and to reconstruct the ancestral state of this character in an attempt to elucidate the generalized pattern of genomic expansions. Genome size estimates were generated for 99 ant species, including new GS estimates for 91 species of ants, and the mean GS of Formicidae was found to be 0.38 pg. The AT/GC ratio was 62.40/37.60. The phylogenetic reconstruction suggested an ancestral GS of 0.38 pg according to the Bayesian inference/Markov chain Monte Carlo method and 0.37 pg according to maximum likelihood and parsimony methods; significant differences in GS were observed between the subfamilies sampled. Our results suggest that the evolution of GS in Formicidae occurred through loss and accumulation of non-coding regions, mainly transposable elements, and occasionally by whole genome duplication. However, further studies are needed to verify whether these changes in DNA content are related to colonization processes, as suggested at the intraspecific level.

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

“…Thus, we do not discard that the minimum interaction theory may be a driving force behind karyotype evolution in ants; however, it seems that other forces may regulate chromosome number by imposing a general common karyotype number, such as n < 15, in fungus-farming ants. A few exceptions where the karyotype reaches higher chromosome numbers appear to overcome the barrier likely caused by the expansion of repetitive genomic elements [16]. This is in agreement with the heterochromatic pattern observed in fungus-farming ants.…”

“…We further extracted the heterochromatic banding pattern of the karyotypes, when available, coding the presence of positive heterochromatin blocks (+) or negative blocks (-) at centromeric (C), pericentromeric (PC), or interstitial (IN) positions, or along the long arm (LA) and/or short arm (SA). We further gathered the genome size information available for fungus-farming ants in Moura et al [16].…”

“…Considering the phylogenetic relationship of fungus-farming species, the general slight variation in genome size across lineages, with few exceptions, shows that a low chromosome number between 10 to 12 haploid chromosome and genome size near to 0.38 pg (see Figure 6), should be plesiomorphic features. Indeed, a low ancestral GS of ~0.37-0.38 has been estimated and proposed for Formicidae [16] and the chromosome number between 10 to 12 of metacentric/submetacentric chromosomes spreads widely across fungus-farming ant lineages. Thus, considering the tight GS in fungus-farming ants, the observed differences in chromosome number across fungus-farming ant genera suggests that changes in chromosome numbers evolve gradually over time, via multiple rearrangement events that culminate in different races due to the fixation of a single or a few chromosomal changes, followed by the extinction of intermediate karyotypes (see [10,17,[48][49][50]).…”

“…Therefore, karyotypes n ≤ 15 and GSs of approximately 0.38 pg should be frequent in fungus-farming ants, whereas karyotypes n > 15 and GS > 0.38 pg are exceptions and are restricted to only some fungus-farming ant lineages. The accumulation of repetitive DNA appears to be mainly responsible for genome size expansions, instead of genome duplication see [16]. These increases in repetitive DNA may promote changes in chromosome number since the heterochromatic regions are hotspots for chromosome breakpoints [51].…”

“…Beyond the number of DNA molecules, estimating the genome content of cell nuclei has contributed to our understanding of genomes through the tree of life. Recently, the nuclear content of approximately 100 ant species was estimated using flow cytometry [16], and now more genome size (GS) ant data has become available. This independent and primary genomic information has provided noteworthy data that can be coupled with cytogenetic data to shed light on the general patterns and processes of the chromosomal changes in fungus-farming ants.…”