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The extent of within-species genetic variation across the diversity of animal life is an underexplored problem in ecology and evolution. Although neutral genetic variation should scale positively with population size, mitochondrial diversity levels are believed to show little variation across animal species. Here, we report an unprecedented case of extreme mitochondrial diversity within natural populations of two morphospecies of chaetognaths (arrow worms). We determine that this diversity is composed of deep sympatric mitochondrial lineages, which are in some cases as divergent as human and platypus. Additionally, based on 54 complete mitogenomes, we observed mitochondrial gene order differences between several of these lineages. We examined nuclear divergence patterns (18S, 28S, and an intron) to determine the possible origin of these lineages, but did not find congruent patterns between mitochondrial and nuclear markers. We also show that extreme mitochondrial divergence in chaetognaths is not driven by positive selection. Hence, we propose that the extreme levels of mitochondrial variation could be the result of either a complex scenario of reproductive isolation, or a combination of large population size and accelerated mitochondrial mutation rate. These findings emphasize the importance of characterizing genome-wide levels of nuclear variation in these species and promote chaetognaths as a remarkable model to study mitochondrial evolution.

Extreme Mitogenomic Variation in Natural Populations of Chaetognaths