Mitochondrial genome evolution in fire ants (Hymenoptera: Formicidae)

Abstract

Background: Complete mitochondrial genome sequences have become important tools for the study of genome architecture, phylogeny, and molecular evolution. Despite the rapid increase in available mitogenomes, the taxonomic sampling often poorly reflects phylogenetic diversity and is often also biased to represent deeper (family-level) evolutionary relationships.

Results: We present the first fully sequenced ant (Hymenoptera: Formicidae) mitochondrial genomes. We sampled four mitogenomes from three species of fire ants, genus Solenopsis, which represent various evolutionary depths. Overall, ant mitogenomes appear to be typical of hymenopteran mitogenomes, displaying a general A+T-bias. The Solenopsis mitogenomes are slightly more compact than other hymentoperan mitogenomes (~15.5 kb), retaining all protein coding genes, ribosomal, and transfer RNAs. We also present evidence of recombination between the mitogenomes of the two conspecific Solenopsis mitogenomes. Finally, we discuss potential ways to improve the estimation of phylogenies using complete mitochondrial genome sequences.

Conclusions: The ant mitogenome presents an important addition to the continued efforts in studying hymenopteran mitogenome architecture, evolution, and phylogenetics. We provide further evidence that the sampling across many taxonomic levels (including conspecifics and congeners) is useful and important to gain detailed insights into mitogenome evolution. We also discuss ways that may help improve the use of mitogenomes in phylogenetic analyses by accounting for non-stationary and non-homogeneous evolution among branches.

Figure 1

Available hymenopteran mitogenomes ordered phylogenetically (based on [11,54]). Parentheses indicate monophyly, superfamilies and families are assumed to be monophyletic. Asterices indicates partially sequenced genomes. Citations and GenBank accession numbers are also given.

Figure 2

Schematic of gene order in the Solenopsis mitogenomes compared to the ancestral arthropod/hymenopteran mitogenome. All protein-coding genes and rRNAs are oriented in the same direction as all other hymenopterans and the hypothetical ancestral arthropod mitogenome. Underlined loci indicate location on the N strand. Arrows are coded by hatching and indicate changes in tRNA order relative to the ancestral arthropod mitogenome.

Figure 3

Maximum likelihood phylogeny of hymenopteran tRNAs. Only the Solenopsis tRNAs are labeled. Black branches identify tRNA-D loci. Blue identify all tRNA-N loci, including "new" and "degenerated" loci in Solenopsis. Green branches are tRNA-V loci, again with the "new" and "degenerated" loci labeled. The values above the long major branches are bootstrap support (100 replicates).

Figure 4

Phylogenetic hypotheses of Hymenoptera based on protein coding genes and rRNA genes. A. Phylogeny recovered from maximum likelihood analyses. Topology of the homogeneous (PhyML) and non-homogeneous (nhPhyML) analyses were identical. Values above internal branches are bootstrap (100 replicates) and aLRT (SH-like) branch support estimates. Values for percent A+T-bias are shown after genus name (values in parentheses are calculated from incomplete genome sequences). The apocritan and aculeatan clades are highlighted. The blue stars indicate posterior probabilities of 0.85 in the heterotachous Bayesian analysis (see B below); the other branches in this part of the tree were recovered with posterior probabilities of 1.0. B. Phylogeny derived from Bayesian inference. The tree topology between the homogenous and heterotachous analyses are identical, except for the clade highlighted in blue: the heterotachous analysis recovered phylogenetic relationships of these taxa which are identical to the maximum likelihood analyses shown in A. Bayesian posterior probabilities are given for the homogeneous model of nucleotide substitution, which is identical to that of the heterotachous model except for the clade in blue (see A above).

Figure 5

Average nucleotide bias in protein coding genes averaged across all 4 Solenopsis mitogenomes. There are no significant differences between mitogenomes (data not shown).

Figure 6

Recombination graph of RPD (significant) and Chimaera (non-significant) analyses. Regardless of the significance level, both show evidence of the same ~500 bp recombination event (grey shading) from the minor parent (VMS) to the recombinant daughter (PMS). The maximum likelihood phylogenies for the non-recombinant (left) and the recombinant (right) fragments are shown.