Mitonuclear discordance results from incomplete lineage sorting, with no detectable evidence for gene flow, in a rapid radiation of Todiramphus kingfishers

Abstract

Many organisms possess multiple discrete genomes (i.e. nuclear and organellar), which are inherited separately and may have unique and even conflicting evolutionary histories. Phylogenetic reconstructions from these discrete genomes can yield different patterns of relatedness, a phenomenon known as cytonuclear discordance. In many animals, mitonuclear discordance (i.e. discordant evolutionary histories between the nuclear and mitochondrial genomes) has been widely documented, but its causes are often considered idiosyncratic and inscrutable. We show that a case of mitonuclear discordance in Todiramphus kingfishers can be explained by extensive genome‐wide incomplete lineage sorting (ILS), likely a result of the explosive diversification history of this genus. For these kingfishers, quartet frequencies reveal that the nuclear genome is dominated by discordant topologies, with none of the internal branches in our consensus nuclear tree recovered in >50% of genome‐wide gene trees. Meanwhile, a lack of inter‐species shared ancestry, non‐significant pairwise tests for gene flow, and little evidence for meaningful migration edges between species, leads to the conclusion that gene flow cannot explain the mitonuclear discordance we observe. This lack of evidence for gene flow combined with evidence for extensive genome‐wide gene tree discordance, a hallmark of ILS, leads us to conclude that the mitonuclear discordance we observe likely results from ILS, specifically deep coalescence of the mitochondrial genome. Based on this case study, we hypothesize that similar demographic histories in other ‘great speciator’ taxa across the Indo‐Pacific likely predispose these groups to high levels of ILS and high likelihoods of mitonuclear discordance.

Genetic diversity and connectivity of the invasive gastropod,Callinina georgiana(Caenogastropoda: Viviparidae) across a fragmented riverscape: a mitonuclear perspective

“…This observed mitonuclear discordance could be due to several factors. Given that nuclear genes generally evolve slower than mitochondrial genes, leading to the retention of ancestral genetic variation over longer time periods, the discordance might reflect incomplete lineage sorting, which has been reported in other animals at both the genetic and genomic levels (Toews & Brelsford, 2012; DeRaad et al, 2023). In this case, the clear differentiation in mtDNA could be reflecting a more recent divergence or selective sweep while the nuclear marker may be retaining a signal of ancestral polymorphism.…”

Islands promote diversification within the silvereye clade: a phylogenomic analysis of a great speciator

“…Under the ‘taxon cycle’ framework—the idea that speciation on islands proceeds through phases of range expansion and contraction (Wilson, 1961) —a great speciator has undergone the first two phases of a cycle: an initial expansion followed by a reduction in dispersive behaviour that promotes population differentiation and sub-speciation. This pattern can be seen in multiple south-west Pacific birds, including kingfishers (Andersen et al, 2018; DeRaad et al, 2023; O’Connell et al, 2019), corvids (Pepke et al, 2019) and passerines (Estandía, Sendell-Price, Oatley, et al, 2023; Klicka et al, 2023; Pedersen et al, 2018).…”

“…Genomics now allows us to reconstruct evolutionary relationships with increased confidence (Lee & Palci, 2015), although it is still challenging for those clades that radiate rapidly, such as many great speciators (Moyle et al, 2009). The condensed sequence of cladogenetic events and increased levels of incomplete lineage sorting (ILS) driven by rapid radiation (DeRaad et al, 2023) and recent divergence (Irestedt et al, 2013) complicate phylogenetic inference (Meleshko et al, 2021). Additionally, gene flow can lead to reticulate evolution (Xu, 2000).…”