A complete logical approach to resolve the evolution and dynamics of mitochondrial genome in bilaterians

Abstract

Investigating how recombination might modify gene order during the evolution has become a routine part of mitochondrial genome analysis. A new method of genomic maps analysis based on formal logic is described. The purpose of this method is to 1) use mitochondrial gene order of current taxa as datasets 2) calculate rearrangements between all mitochondrial gene orders and 3) reconstruct phylogenetic relationships according to these calculated rearrangements within a tree under the assumption of maximum parsimony. Unlike existing methods mainly based on the probabilistic approach, the main strength of this new approach is that it calculates all the exact tree solutions with completeness and provides logical consequences as highly robust results. Moreover, this method infers all possible hypothetical ancestors and reconstructs character states for all internal nodes of the trees. We started by testing our method using the deuterostomes as a study case. Then, with sponges as an outgroup, we investigated the evolutionary history of mitochondrial genomes of 47 bilaterian phyla and emphasised the peculiar case of chaetognaths. This pilot work showed that the use of formal logic in a hypothetico-deductive background such as phylogeny (where experimental testing of hypotheses is impossible) is very promising to explore mitochondrial gene order in deuterostomes and should be applied to many other bilaterian clades.

Fig 1

Diagram of three possible transpositions (top) and two possible inversions (bottom) in a circular genome leading to the same gene order. A. Because of the circularity of the genome, there are always three possible transpositions leading to a similar gene order ([B A C] = [A C B] = [C B A]) from a given gene order ([A B C]). Thus, it is not possible to determine which block of genes is concerned by a transposition. B. Similarly, there are always two possible inversions leading to a similar gene order ([-A B] = [A -B]) from a given gene order ([A B]). Thus, it is not possible to determine which block of genes is inverted (A or B). In each example, the transposed or inverted block is underlined. The black arrowheads indicate where the transposed block is inserted. By convention, the circular genomes are read clockwise.

Fig 2. The two most parsimonious trees for deuterostomes (12 evolutionary steps) deduced from the order of protein-coding and ribosomal RNA mitochondrial (mt) genes.

The maximum parsimony rearrangement events among the trees are indicated by different lines (blue dashed line, inversion; green dashed line, transposition; purple solid line, reverse transposition). Hypothetical ancestral mtDNAs (HTUs) are indicated by grey shaded dots. Grey-circled white dots indicate HTUs that correspond to ground patterns of clades. Ur-echinodermata is represented by the mtDNA of either Strongylocentrotus purpuratus (A) or Asterina pectinifera (B). Grey-shaded boxes on diagrammatic representations of hypothetical ancestral mtDNAs (HTU#1a to 3b) highlight genes transcribed from the opposite strand.

Fig 3. Two trees among extant Echinodermata as deduced from the order of protein-coding, ribosomal RNA(rRNA) and transfer RNA (tRNA) mitochondrial genes.

(A) One tree solution for the whole Echinodermata group calculated with mitochondrial genes (including tRNA genes). Among the 25 necessary steps, more than 6 involved the mitochondrial protein-coding and rRNA genes. (B) Tree solution calculated with mitochondrial protein-coding and rRNA genes with Asterina pectinifera as Ur-echinodermata (Fig 2B) on which 20 necessary rearrangements of tRNA genes have been added a posteriori. Among the 26 steps, 6 involved the mitochondrial protein-coding and rRNA genes.

Fig 4. The six most parsimonious trees deduced from the order of protein-coding and ribosomal RNA mitochondrial (mt) genes in bilaterians.

The rearrangements are indicated by different lines (blue dashed line, inversion; green dashed line, transposition; purple solid line, reverse transposition). Hypothetical ancestral mtDNAs (HTUs) are indicated at each node of the trees by grey shaded dots. Grey-circled white dots indicate HTUs that correspond to ground patterns of deuterostomes, ecdysozoans and lophotrochozoans. Gene orders of HTUs are indicated in Table 2.