Comparative mitogenomics of the Decapoda reveals evolutionary heterogeneity in architecture and composition

Abstract

The emergence of cost-effective and rapid sequencing approaches has resulted in an exponential rise in the number of mitogenomes on public databases in recent years, providing greater opportunity for undertaking large-scale comparative genomic and systematic research. Nonetheless, current datasets predominately come from small and disconnected studies on a limited number of related species, introducing sampling biases and impeding research of broad taxonomic relevance. This study contributes 21 crustacean mitogenomes from several under-represented decapod infraorders including Polychelida and Stenopodidea, which are used in combination with 225 mitogenomes available on NCBI to investigate decapod mitogenome diversity and phylogeny. An overview of mitochondrial gene orders (MGOs) reveals a high level of genomic variability within the Decapoda, with a large number of MGOs deviating from the ancestral arthropod ground pattern and unevenly distributed among infraorders. Despite the substantial morphological and ecological variation among decapods, there was limited evidence for correlations between gene rearrangement events and species ecology or lineage specific nucleotide substitution rates. Within a phylogenetic context, predicted scenarios of rearrangements show some MGOs to be informative synapomorphies for some taxonomic groups providing strong independent support for phylogenetic relationships. Additional comparisons for a range of mitogenomic features including nucleotide composition, strand asymmetry, unassigned regions and codon usage indicate several clade-specific trends that are of evolutionary and ecological interest.

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

“…Also, it did not cluster with the remaining two available species from this family, which also indicates unique evolutionary pressures (or a taxonomic artefact). Among the species with highly conserved AAGO, along with the relatively basal (Shen et al 2013;Tan et al 2019) species within the Decapod clade Penaeus monodon, discussed previously ( Figure 1D), we also plotted skews for a highly derived species Pachygrapsus marmoratus (Figure 11). Both GC and AT skew plots exhibited maxima that corresponded to the strand distribution of genes.…”

“…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.…”

“…Over the last few decades, the phylogeny and taxonomy of crustaceans were characterised by a bewildering array of often highly contradictory hypotheses (Schram 2001;Timm and Bracken-Grissom 2015;Lozano-Fernandez et al 2019), many of which were derived using mitochondrial molecular data, e.g. (Wetzer 2002;Tan et al 2015Tan et al , 2019Timm and Bracken-Grissom 2015;Cheng et al 2018). A majority of crustaceans exhibit negative GC skews for genes on the mitochondrial 'majority strand' (the strand encoding a majority of genes in the ancestral crustacean mitogenomic architecture is named so by convention), but several crustacean lineages, for example most isopods, exhibit inversed (positive) GC skews (Hassanin 2006;Kilpert and Podsiadlowski 2006;Kilpert et al 2012;Pons et al 2014;Yu et al 2018;Zhang et al 2019b;Zou et al 2020).…”

“…We have recently shown that in isopods these compositional biases caused by inversions in the strand replication order are so strong that they render mitochondrial data an unsuitable tool for phylogenetics (Zhang et al 2019b). As these compositional biases can and do affect mitochondrial data-based molecular evolutionary studies in other crustacean lineages as well (Tan et al 2019), we suspect that a proportion of the contradictory hypotheses for other crustacean lineages may also be attributable to skew-driven phylogenetic artefacts.…”

“…Despite this limitation, mitochondrial data, especially complete mitochondrial genomes, can be a suitable tool for inferring lower-level phylogenies and studying evolutionary patterns in crustacean taxa that did not undergo ORI events. While many crustacean lineages exhibit the highly conserved ancestral arthropod mitochondrial architecture (Boore et al 1998;Cheng et al 2018;Tan et al 2018), a number of lineages exhibit exceptionally high plasticity of mitochondrial architecture (Kilpert et al 2012;Tan et al 2019;Zou et al 2020). As this includes common CR duplication events and extremely low levels of conservedness of CR sequences (Pie 2008), no study has ever attempted to systematically infer the evolutionary history of ORI events in crustaceans.…”