Extreme Mitogenomic Variation Without Cryptic Speciation in Chaetognaths

Abstract

The extent of within-species genetic variation across the diversity of animal life is a fundamental but largely unexplored problem in ecology and evolution. The neutral theory of molecular evolution predicts that genetic variation scales positively with population size. However, the genetic diversity of mitochondrial DNA, a prominent marker used in DNA barcoding studies, shows very little variation across animal species. Here, we report an unprecedented case of extreme mitochondrial variation within natural populations of two species of chaetognaths (arrow worms). We determined that this diversity is composed of deep intraspecific mitochondrial lineages within single populations that could be as divergent as human and newt. This mitochondrial diversity is the highest ever reported in animals without evidence of cryptic speciation or allopatric divergence as supported by nuclear evidence. We sequenced 54 complete mitogenomes revealing gene order rearrangements between these intraspecific lineages. Such structural differences have never previously been reported within single species. We confirm that this divergence was not driven by positive selection, and conversely show that these lineages evolved under purifying selection, consistently with neutral expectations. Our findings question the generally accepted narrow range of genetic variation in animal mitochondria and argue for a reappraisal of DNA barcoding techniques. Furthermore, extreme levels of mitogenomic variation in chaetognaths challenge classical views regarding mitochondrial evolution and cytonuclear co-evolution.