Mitochondrial genomes in the iconic reindeer lichens: Architecture, variation, and synteny across multiple evolutionary scales

Variation in mitochondrial genome composition across intraspecific, interspecific, and higher taxonomic scales has been little studied in lichen obligate symbioses. <i>Cladonia</i> is one of the most diverse and ecologically important lichen genera, with over 500 species representing an array of unique morphologies and chemical profiles. Here, we assess mitochondrial genome diversity and variation in this flagship genus, with focused sampling of two clades of the “true” reindeer lichens, <i>Cladonia</i> subgenus <i>Cladina</i>, and additional genomes from nine outgroup taxa. We describe composition and architecture at the gene and the genome scale, examining patterns in organellar genome size in larger taxonomic groups in Ascomycota. Mitochondrial genomes of <i>Cladonia, Pilophorus</i>, and <i>Stereocaulon</i> were consistently larger than those of <i>Lepraria</i> and contained more introns, suggesting a selective pressure in asexual morphology in <i>Lepraria</i> driving it toward genomic simplification. Collectively, lichen mitochondrial genomes were larger than most other fungal life strategies, reaffirming the notion that coevolutionary streamlining does not correlate to genome size reductions. Genomes from <i>Cladonia ravenelii</i> and <i>Stereocaulon pileatum</i> exhibited ATP9 duplication, bearing paralogs that may still be functional. Homing endonuclease genes (HEGs), though scarce in <i>Lepraria</i>, were diverse and abundant in <i>Cladonia</i>, exhibiting variable evolutionary histories that were sometimes independent of the mitochondrial evolutionary history. Intraspecific HEG diversity was also high, with <i>C. rangiferina</i> especially bearing a range of HEGs with one unique to the species. This study reveals a rich history of events that have transformed mitochondrial genomes of <i>Cladonia</i> and related genera, allowing future study alongside a wealth of assembled genomes.