Performance of Single and Concatenated Sets of Mitochondrial Genes at Inferring Metazoan Relationships Relative to Full Mitogenome Data

Abstract

Mitochondrial (mt) genes are some of the most popular and widely-utilized genetic loci in phylogenetic studies of metazoan taxa. However, their linked nature has raised questions on whether using the entire mitogenome for phylogenetics is overkill (at best) or pseudoreplication (at worst). Moreover, no studies have addressed the comparative phylogenetic utility of mitochondrial genes across individual lineages within the entire Metazoa. To comment on the phylogenetic utility of individual mt genes as well as concatenated subsets of genes, we analyzed mitogenomic data from 1865 metazoan taxa in 372 separate lineages spanning genera to subphyla. Specifically, phylogenies inferred from these datasets were statistically compared to ones generated from all 13 mt protein-coding (PC) genes (i.e., the “supergene” set) to determine which single genes performed “best” at, and the minimum number of genes required to, recover the “supergene” topology. Surprisingly, the popular marker COX1 performed poorest, while ND5, ND4, and ND2 were most likely to reproduce the “supergene” topology. Averaged across all lineages, the longest ∼2 mt PC genes were sufficient to recreate the “supergene” topology, although this average increased to ∼5 genes for datasets with 40 or more taxa. Furthermore, concatenation of the three “best” performing mt PC genes outperformed that of the three longest mt PC genes (i.e, ND5, COX1, and ND4). Taken together, while not all mt PC genes are equally interchangeable in phylogenetic studies of the metazoans, some subset can serve as a proxy for the 13 mt PC genes. However, the exact number and identity of these genes is specific to the lineage in question and cannot be applied indiscriminately across the Metazoa.

Reducing the information gap on Loricarioidei (Siluriformes) mitochondrial genomics

“…In order to evaluate this in Neotropical catfishes, phylogenetic trees were generated using the three longest mitochondrial genes, which also harbor the majority of informative sites (cox1, nad4 and nad5) and the three mitochondrial genes with the highest performance (nad2, nad4 and nad5), as identified by Havird & Santos [13]. Those trees did not recover the same topology as encountered in the tree recovered using information on the 15 mitochondrial genes (Additional file 6).…”

Next-generation sequencing, phylogenetic signal and comparative mitogenomic analyses in Metacrangonyctidae (Amphipoda: Crustacea)

“…We can conclude that the genes with more accumulative phylogenetic informativeness are nad5, nad2, nad1, cob and nad6 , while cox1 and cox2 are relatively poor in phylogenetic informativeness despite their prevalence in phylogenetic reconstruction studies. Havird and Santos [30] have recently analysed a large metazoan mitogenomic data set concluding that nad5, nad4 and nad2 genes were the more likely to reproduce the phylogeny obtained from concatenation of all 13 PCGs, while the popular marker cox1 and some of the other long PCGs were the less phylogenetically reliable at this deep taxonomic level. Although particular genes can provide phylogenetic power at distinct divergence time intervals and be more informative in some lineages than others, our data agree with the analysis by [30] in that genes of the NADH dehydrogenase subunits have in general more phylogenetic power than genes coding for the cytochrome subunits.

Figure 4 Metacrangonyctidae mitochondrial protein-coding gene phylogenetic informativeness.

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Mitogenomic phylogenetic analyses of Leptogorgia virgulata and Leptogorgia hebes (Anthozoa: Octocorallia) from the Gulf of Mexico provides insight on Gorgoniidae divergence between Pacific and Atlantic lineages

“…This discrepancy is most likely attributed to our use of complete mitochondrial genomes that include fourteen protein‐coding genes and two RNAs instead of a single, partial gene ( mtMutS ). There are numerous studies of multiple taxa showing a pattern of incongruent tree topology between single mitochondrial markers and complete mitochondrial genomes despite the fact that they are the same locus and therefore share the same phylogenetic history (Havird & Santos, ; Knaus et al, ; Luo et al, ; Nadimi et al, ; Pacheco et al, ; Rohland et al, ; Urantowka et al, ; Wang et al, ; Willerslev et al, ). For example, Havird, Santos Scott, and Schierwater, () analyze the performance of single and concatenated sets of mitochondrial genes relative to complete mitochondrial genomes for phylogenetic reconstruction of metazoans.…”

“…For example, Havird, Santos Scott, and Schierwater, () analyze the performance of single and concatenated sets of mitochondrial genes relative to complete mitochondrial genomes for phylogenetic reconstruction of metazoans. Their findings show that single genes are not able to reproduce the topology of a mitogenomic phylogeny (Havird & Santos, ). A similar study, but focusing on birds, showed that single mitochondrial genes resulted in incorrect and contradictory phylogenetic relationships, while the use of complete mitochondrial genomes accurately reflected the species tree (Urantowka et al, ).…”

“…Although mitochondrial genomes have been shown to be problematic for phylogenetic reconstruction of scleractinian corals due to the presence of substitution saturation and long branch attraction (i.e., Kitahara et al, ), it is only an issue within the Hexacorallia and it does not affect the Octocorallia, such as the gorgonian corals in our study (Figueroa & Baco, ). Complete mitochondrial genomes have been demonstrated to provide robust and well‐supported phylogenies for Octocorallia (e.g., Figueroa & Baco, ; Figueroa & Baco, ; Kayal, Roure, Philippe, Collins, & Lavrov, ; Poliseno et al, ), while the use of single mitochondrial genes has been demonstrated to result in incongruent largely unresolved trees across a wide range of taxa (Havird & Santos, ; Knaus, Cronn, Liston, Pilgrim, & Schwartz, ; Luo et al, ; Nadimi, Daubois, & Hijri, ; Pacheco et al, ; Rohland et al, ; Urantowka, Kroczak, & Mackiewicz, ; Wang et al, ; Willerslev et al, ). Therefore, we expect that the taxonomic position of L. hebes and L. virgulata will be fully resolved by reconstructing their phylogeny using mitochondrial genomes.…”