Comparative mitogenomics


Any phylogenetic analysis starts with the alignment of nucleotide sequences, where supposedly homologous nucleotide positions (orthologs, sites) are juxtaposed (Cucini et al., 2021). Protein-coding DNA sequences are usually easily aligned. In contrast, the alignment of DNA sequences encoding tRNAs, rRNAs and the control region may be challenging due to the presence of insertions and deletions (indels). In these cases, conserved sequence blocks serve as landmarks aiding correct alignment (Castresana, 2000). Sequences that cannot be aligned have to be excluded from analysis. 

Although nucleotide-sequence alignments provide the basis for all phylogenetic analyses, they are hardly ever published. To bridge this gap, I decided to retrieve DNA sequences of a number of selected land- and waterfowl species (superorder Galloanserae) from GenBank for manual alignment. The selection includes representatives of all families (Galliformes: Megapodiidae, Cracidae, Numididae, Odontophoridae, Phasianidae; Anseriformes: Anhimidae, Anseranatidae, Anatidae). 

Case study #1: control region (CR) of Galloanserae

Aligned partial control region sequences of thirty selected species of Galloanserae. Eleven unalignable regions (U-1 to U-11) and elven alignable regions (A-1 to A-11) are distinguished, with only the elongate terminal unalignable region (U-12) not being represented. [Colour symbols: dark blue for "G", light blue for "A", dark green for "T", light green for "C", pink for nucleotide transitions, purple for nucleotide transversions, orange for mixed transitions/ transversions, black for unresolved anseriform/galliform ground-pattern apomorphies, red for apomorphies in general, yellow for convergences, grey for deletions, and brown for insertions of varying lengths that are indicated by numbers]

As can be seen from the above sequences, the alignment is not always straightforward, and different regions vary with respect to alignability. Whenever multiple indels occur in variable regions, alignability is immediately lost. On the other hand, there are several conserved regions where only a limited number of nucleotide substitutions are encountered. A schematic map of the control region of Galloanserae is given below in order to provide an overview of the observed distribution of alignable and unalignable regions: 

Schematic map of the control region in Galloanserae, with unalignable regions (U-1 to U-12) and alignable regions (A-1 to A-11) being distinguished. For comparison, the traditionally recognised domains and conserved boxes are presented in colour below. [Note that some of the alignable regions (e.g. A-2, A-7, A-8, A-9, as well as parts of A-5 and A-10) are lacking a corresponding traditional conserved box although no base substitutions were observed in Galloanserae]

Taken together, the control region exhibits a remarkable mix of variable and conserved regions. Because only the conserved regions are alignable, the control region turned out to be particularly informative in resolving phylogenetic relationships at the family level: 

List of control-region apomorphies mapped onto the phylogeny of Galloanserae. While some relationships are particularly well resolved, others lack support altogether. Overall, the degree of homoplasy is limited, but some convergencies are encountered (summarised in the yellow box). Most "fake" apomorphies are easily recognised as such, because they are far outnumbered by true apomorphies. However, there are two remarkable exceptions: (I) the data weakly support a sister-group relationship between Oxyurinae and Anserinae (based on the putative apomorphy C106T, where T was replaced by C at position 106), which is, however, not supported by nuclear data, and (II) the data impressively suggest a sister-group relationship between Anhimidae and Anseranatidae (based on a remarkable set of 11 apomorphies), which is likewise not supported by nuclear data. This special issue will be discussed in the text. Note that basal relationships within Galliformes (landfowl) and Anseriformes (waterfowl), respectively, are not shown, as there were no Struthioniformes or Neoaves included as outgroups. 

One finding deserves particular consideration: from nuclear studies we know that screamers (Anhimidae) represent the basalmost family of waterfowl, and that magpie-geese (Anseranatidae) diverge next (Prum et al., 2015; Kuhl et al., 2021). These results are corroborated by morphological data (Livezey, 1986). Therefore, it is very surprising to find that control-region sequences provide strong evidence (by 11 apomorphies) for a sister-group relationship between these two families. In other cases of mito-nuclear discordance, inconsistencies among different data sets are usually attributed to incomplete lineage sorting and/or introgression as a result of hybridisation. However, because of the mere amount of conflicting data, in this particular case the hybridising species must have belonged to different families. Are viable hybrid offspring really to be expected under these conditions? Or is it even possible that mitochondria-derived nuclear pseudogenes (NUMTs) have been re-integrated into the mitochondrial genome? An explanation of this kind has already been put forward by Spiridonova et al. (2019).  

Species identification via COI barcoding

DNA barcoding is a method of species identification by comparing DNA sequences of an unknown sample with DNA sequences of known species via online reference databases. For animal species, the sequence used for DNA barcoding is a 648-bp fragment of the mitochondrial CO1 gene. The length of the fragment is determined by the limits of Sanger sequencing. 

COI-barcoding has been chosen as a species marker, because it turned out that most animal species (except cnidarians) are separated from congeneric species by CO1 sequence divergences higher than 2%, while sequence divergences among conspecifics are usually less than 2% (Hebert et al., 2003). This observation is referred to as the “barcode gap” (Meyer & Paulay, 2005). More than 94% of morphologically defined bird species have been confirmed with COI as a species-level marker gene (Wang et al., 2020). 

In a comparative avian mitogenomic study, the CO1 gene proved to be the one with the least amount of rate heterogeneity across avian orders, thus being closest to a “molecular clock” (Pacheco et al., 2011). This possibly explains its suitability as a reasonable indicator of species limits. 


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