The complete mitogenomes of lobsters and crayfish (Crustacea: Decapoda: Astacidea) reveal surprising differences in closely related taxa and convergences to Priapulida

Abstract

We sequenced the complete mitogenomes of three species of Decapoda, Astacidea, comprising Astacida (freshwater crayfish) and Homarida (marine clawed lobsters): 1. Procambarus fallax f. virginalis (Astacida, Astacoidea), 2. Homarus gammarus (Homarida, Nephropoidea) and 3. Enoplometopus occidentalis (Homarida, Enoplometopoidea). Together with the available species in GenBank, the taxon Astacidea is covered with at least one representative for each of the four main subtaxa. Astacidea show unexpectedly diverse genomic organizations. Ten different gene arrangements have been observed in the 28 investigated species. Compared with the decapod ground pattern, a huge inversion, involving more than half of the mitogenome, has been found in four freshwater crayfish species of Astacoidea and convergently in one lobster species. Surprisingly, this inversion can also be observed in the distantly related Priapulida. This multiple convergent evolution suggests a relative ease in the evolution of great similarities in mitochondrial gene order. In addition, a partial or complete loss of the protein‐coding gene nad2 has been found in E. occidentalis and H. gammarus but not in Nephrops norvegicus, Homarus americanus and Enoplometopus debelius. A reversal of the strand asymmetry has been found in five astacideans which is supposed to be caused by the inversion of a replication origin in the control region.

Advancing our understanding of the connectivity, evolution and management of marine lobsters through genetics

“…The Southern hemisphere crayfish (Parastacoidea) and Northern hemisphere crayfish (Astacoidea), both freshwater groups, are well-supported sister taxa as are the reef lobsters (Enoplometopidae) and Nephropidae (the latter family containing the Thaumatochlidae) (Tsang et al 2008;Bracken-Grissom et al 2014). Focusing specifically on the Astacidea, Shen et al (2015) investigated mitochondrial gene order rearrangements and showed convergent evolution in mitochondrial gene order in several instances. This indicates that mitochondrial gene order is not a useful phylogenetic character within this infraorder and will likely be limited in its utility at a deeper phylogenetic level.…”

Absence of evidence is not evidence of absence: Nanopore sequencing and complete assembly of the European lobster (Homarus gammarus) mitogenome uncovers the missing nad2 and a new major gene cluster duplication

“…The veracity of the current European lobster reference mitogenome in the NCBI database (Accession Number: NC_020020.1) is questioned given its unusual features e.g. missing nad2 , large mitogenome inversion and translocated tRNAs [9, 10, 24] that were not observed in its close relative, the American lobster, Homarus americanus [8]. Although subsequent PCR and Sanger sequencing has been carried out on additional individuals to validate the observed abnormalities [10], a secondary validation by a separate group using different sequencing technology is highly desirable to provide confirmation of this atypical crustacean mitogenome sequence.…”

“…missing nad2 , large mitogenome inversion and translocated tRNAs [9, 10, 24] that were not observed in its close relative, the American lobster, Homarus americanus [8]. Although subsequent PCR and Sanger sequencing has been carried out on additional individuals to validate the observed abnormalities [10], a secondary validation by a separate group using different sequencing technology is highly desirable to provide confirmation of this atypical crustacean mitogenome sequence. We, therefore, sequenced another individual of Homarus gammarus using Illumina technology, which removes the need for the laborious and presumably error-prone steps required in traditional mitogenome sequencing such as long-range PCR and primer walking that may lead to the unintentional misassembly of mitogenome.…”

“…The complete mitogenome of H. americanus has been sequenced, assembled and annotated and is consistent with the pancrustacean gene order [8]. However, in stark contradistinction, the recently published H. gammarus mitogenome [9] deviates substantially as it was reported to have not only a large inversion but to be also missing the nad2 genes and a few tRNA genes [10]. While minor and major departures from the pancrustacean gene order have been observed in multiple lineages of decapod crustaceans notably among scampi and Southern Hemisphere freshwater crayfish species [11–16], all 13 mitochondrial protein-coding genes are always present in the assembled mitogenome occasionally with some species having duplicated tRNA genes and occassionally the control region [14].…”

“…However, the mitogenome exhibits the typical 13 protein-coding genes, 22 tRNAs, 2 rRNAs and a control region, suggesting that Illumina short read data alone can also accomplish the same objective as reported in various mussel mitogenomic studies [31–34]. Unlike the green-lipped mussel mitogenome, the Homarus gammarus mitogenome represents an interesting case due to its atypical gene organization that has been partially verified using PCR across a few individuals in a follow-up study [10]. Furthermore, the high genetic variation observed in the 3 kb mitochondrial region that excludes the control region is unexpected [7] but can be explained by the presence of a large tandem duplication event followed by pseudogenization which warrants further investigation.…”