Coupled evolutionary rates shape a Hawaiian insect-symbiont system.

Abstract

Background: The Hawaiian Pariaconus psyllid radiation represents a unique system to study the co-evolution of nuclear, mitochondrial, and endosymbiont genomes. These psyllids, which diversified across the Hawaiian Islands during the last 3-3.5 million years vary with their ecological niches on their plant host 'Ōhi'a lehua (Metrosideros polymorpha) (free-living, open-gall, and closed-gall lifestyles) and harbor one to three beneficial bacterial endosymbionts. Co-evolutionary studies of other multi-endosymbiont insect systems have shown decoupled rates of sequence evolution between mitochondria and endosymbionts. Here we examine the evolutionary trends in Pariaconus psyllids, their mitochondria and their endosymbionts to determine if they fit this paradigm.

Results: We sequenced a new Carsonella genome from the ohialoha species group (closed-gall, one symbiont), revealing a remarkable degree of gene conservation between two of the most divergent species from this diverse species group that has dispersed across multiple islands. Further, despite the rapid radiation of psyllid species, we observed complete synteny among mitochondrial genomes from all six Pariaconus species in this study, suggesting the preservation of genome structure due to strong purifying selection. Phylogenetic analyses of the nuclear, mitochondrial, and endosymbiont genomes across these six Pariaconus species revealed correlated rates of substitutions, contrary to prior reports of decoupling between mitochondrial and endosymbiont genomes in other insect systems with multiple symbiont partners. Finally, we found that free-living psyllids with three symbionts exhibited elevated mutation rates (~ 1.2-1.6x) across all genomes and elevated rates of fixation of nonsynonymous substitutions in the insect nuclear genome and one of the endosymbionts.

Conclusions: This study highlights the interplay between ecological diversification and genomic evolution in Pariaconus. Further, these data indicate that multiple endosymbiont partners alone are not sufficient to result in decoupling rates of sequence evolution. Future work on basal members of this species radiation will refine our understanding of the mechanisms shaping this dynamic insect-symbiont system and its implications for genome evolution.