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Mutualist Ant Study Questions Red King Effect

NEW YORK (GenomeWeb) – Obligately mutualistic relationships may spur rather than mute molecular evolution rates in the species involved, according to a study appearing online today in Nature Communications.

A pair of researchers from the University of Chicago and the Field Museum of Natural History did de novo genome sequencing on an ant species within the Pseudomyrmex genus before resequencing half a dozen other Pseudomyrmex species including three generalists and three species that had obligate mutualist relationships with plants.

The team saw enhanced molecular evolution in the mutualist ants compared to the generalists — a finding that disputes the so-called Red King effect, which suggests co-evolving species have reduced rates of evolution to prevent unanticipated changes to their mutually beneficial relationship.

"We were surprised to learn that the mutualists actually had a higher rate of evolution across their genomes than the generalists," corresponding author Benjamin Rubin, an evolutionary biology researcher affiliated with the University of Chicago and the Field Museum of Natural History, said in a statement.

While the Red Queen hypothesis contends that competitive, co-evolving species are prone to enhanced rates of molecular evolution, a theory known as the Red King effect suggests that co-dependent mutualist species may benefit by dialing down evolutionary rates.

To explore that possibility, Rubin and co-author Corrie Moreau, also with the Field Museum's Integrative Research Center, focused on mutualistic ant-plant relationships involving ants that nest within host plants, protecting them from plant-munching herbivores in the process.

The pair used the Illumina HiSeq instrument to sequence P. gracilis, generating hundreds of millions of sequences that were used to put together a genome assembly spanning more than 390 million bases.

In that assembly, the team uncovered 16,069 predicted protein-coding genes — annotated with the help of transcriptome sequences from several P. gracilis life stages — and more than 2,500 repetitive elements. Nearly 5,700 of the apparent P. gracilis genes were not orthologous to genes documented in other species. Within that set, the group saw an over-representation of genes with features resembling genes involved in ATP synthesis.

The researchers then went on to sequence six more Pseudomyrmex species, including the generalists P. pallidus, P. elongatus, and P. sp. PSW-54 and the mutualists P. concolor, P. dendroicus, and P. flavicornis, producing sequences that typically spanned roughly two-thirds of the P. gracilis genome assembly.

Along with phylogenetic analyses of the ants, the team searched for signs of parallel evolution in the species that form ant-plant mutualist relationships and compared molecular evolution rates across the species. Its results indicated that the three mutualistic ant species not only evolved separately, without extensive parallel evolution, but also exhibit higher molecular evolution rates than their generalist counterparts.

A handful of genes exhibited signs of positive selection across all three mutualistic species, the researchers reported. That set included genes involved in everything from muscle function and morphogenesis to brain function.

"Though we cannot, here, positively disentangle all potential mechanisms underlying the observed differences in rates of substitution between taxa, we expect that genomic analyses of additional, diverse mutualisms will show similar accelerations in evolutionary rates," the authors wrote.