Extreme Mitogenomic Variation in Natural Populations of Chaetognaths

Abstract

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.

Novel genomic resources for shelled pteropods: a draft genome and target capture probes for Limacina bulimoides, tested for cross-species relevance

“…High levels of mitochondrial polymorphism among individuals of L. bulimoides could have further complicated the capture, resulting in low capture success of mitochondrial targets. Hyperdiversity in mitochondrial genes, with more than 5% nucleotide diversity in synonymous sites has been reported for several animal clades, including gastropods [63,64] and chaetognaths [65]. Only 13 of the 41 non-coding targeted regions were recovered, which may indicate that these regions were also too divergent to be captured by the probes.…”

Evolutionary history of inversions in the direction of architecture-driven mutational pressures in crustacean mitochondrial genomes

“…Therefore, we strongly suspect that the elevated evolutionary rate is largely a product of the ORI event, and not reflective of the average evolutionary rate in other barnacles. Finally, the fact that some, but not all, architectural rearrangements will produce mutational bursts may also be a partial explanation for the observation that there is only a weak association between the GO rearrangement and base substitution rates in mitogenomes of many animal lineages (Shao et al 2003;Hassanin 2006;Marlétaz et al 2017;Tan et al 2019). Therefore, in agreement with previous observation that demonstrating the occurrence of adaptive substitutions in mtDNA evolution can be difficult (Lavrov and Pett 2016), all studies aiming to study the evolution of mtDNA should pay close attention to architectural rearrangements and misleading mutational signals that they may produce.…”

Resolving the psyllid tree of life: phylogenomic analyses of the superfamily Psylloidea (Hemiptera)

“…For resolving systematic relationships, both mitogenomic and meta‐mitogenomic approaches have proven effective with insect lineages at multiple taxonomic scales (Cui et al ., ; Gillett et al ., ; Tang et al ., ; Crampton‐Platt et al ., ; Choo et al ., ). However, despite the proven phylogenetic utility of the mitogenome, there remain justified doubts in relying solely on maternally inherited haploid genomes to reconstruct evolutionary histories (Marlétaz et al ., ; Rodríguez et al ., ). Therefore, combining a mitogenomic approach with an amenable nuclear data approach, such as genome‐wide targeted hybrid enrichment methods (Prum et al ., ; Hamilton et al ., ; Young et al ., ), should improve resolution as well as confidence in phylogenetic reconstructions from mitochondria alone.…”