Mito-nuclear discordance within Anthozoa, with notes on unique properties of their mitochondrial genomes

Abstract

Whole mitochondrial genomes are often used in phylogenetic reconstruction. However, discordant patterns in species relationships between mitochondrial and nuclear phylogenies are commonly observed. Within Anthozoa (Phylum Cnidaria), mitochondrial (mt)-nuclear discordance has not yet been examined using a large and comparable dataset. Here, we used data obtained from target-capture enrichment sequencing to assemble and annotate mt genomes and reconstruct phylogenies for comparisons to phylogenies inferred from hundreds of nuclear loci obtained from the same samples. The datasets comprised 108 hexacorals and 94 octocorals representing all orders and > 50% of extant families. Results indicated rampant discordance between datasets at every taxonomic level. This discordance is not attributable to substitution saturation, but rather likely caused by introgressive hybridization and unique properties of mt genomes, including slow rates of evolution driven by strong purifying selection and substitution rate variation. Strong purifying selection across the mt genomes caution their use in analyses that rely on assumptions of neutrality. Furthermore, unique properties of the mt genomes were noted, including genome rearrangements and the presence of nad5 introns. Specifically, we note the presence of the homing endonuclease in ceriantharians. This large dataset of mitochondrial genomes further demonstrates the utility of off-target reads generated from target-capture data for mt genome assembly and adds to the growing knowledge of anthozoan evolution.

A Cnidarian Phylogenomic Tree Fitted With Hundreds of 18S Leaves

“…The four transcriptomic phylogenies generated here (Fig. 2, S2-4) recovered all sampled hexacoral lineages (i.e., Scleractinia, Corallimorpharia, Actiniaria, Zoantharia, Ceriantharia) as monophyletic and found Scleractinia and A Cnidarian Phylogenomic Tree Fitted With Hundreds of 18S Leaves Corallimorpharia as sister taxa (discussed further below), concurring with many recent phylogenomic studies (Kayal et al, 2018;Quattrini et al, 2017Quattrini et al, , 2020Quattrini et al, , 2023Zapata et al, 2015). In the 18S tree, Zoantharia was non-monophyletic with a sample labeled as Zoanthus falling out among the Antipatharia; we suspect that this is a contaminant or mislabeled sequence rather than evidence for zoantharian polyphyly.…”

“…Columns labeled D2024-18S and D2024-Tr indicate the 18S and transcriptomic datasets generated in this study, respectively. The other studies included are Chang et al, 2015;Kayal et al, 2018;Quattrini et al, 2017Quattrini et al, , 2020Quattrini et al, , 2023Zapata et al, 2015, andStampar et al, 2019. (GCF_000090795), the placozoan Trichoplax adhaerens (ABGP00000000), the fruit fly Drosophila melanogaster (GCF_000001215), the marine annelid Capitella teleta (PR-JNA175705), the limpet Lottia gigantea (PRJNA175706), the purple sea urchin Strongylocentrotus purpuratus (https://metazoa.ensembl.org, release 47), and the zebra finch Taeniopygia guttata (ABQF00000000) (Table S3). We used diamond v0.9.…”

Analysis of mitogenomes from the family Keratoisididae reveals mitonuclear discordance and the presence of unknown open reading frames

“…By building a new conserved element phylogeny with an almost identical taxon set to the complete mitochondrial genome phylogeny, we provide evidence that differences are due to mitonuclear discordance and not insu cient or uneven taxon sampling. Mitonuclear discordance has been previously reported across deep to shallow divergences within Anthozoa (Quattrini et al 2023b). This is the rst time mitonuclear discordance has been reported within the family Keratoisididae.…”

“…However, the presence of discordance between mitochondrial and nuclear inferences provides evidence that concatenating sequences of nuclear and mitochondrial origin is inappropriate within Keratoisididae. Interfamilial studies using both nuclear and mitochondrial genomes have also found mitonuclear discordance at the familial rank within Anthozoa (Quattrini et al 2023b). Therefore, until more studies investigate within familial relationships, caution should be applied when making phylogenetic inferences inside any anthozoan family.…”

“…These novel methods have also been applied to resolve relationships within morphologically complex genera (Untiedt et al 2021), help erect new families (McFadden et al 2022), and date the origins of different groups of corals (Quattrini et al 2020;). However, the relationships among octocoral families are incongruent between inferences are made using nuclear and mitochondrial markers (Quattrini et al 2023b).…”