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Allopatric divergence is a fundamental component of most traditional models of biogeography and community assembly. Gene flow between allopatric populations should be influenced by the nature of geographic barriers and can have a profound impact on adaptation, the speciation process, and phylogenetic inference. Superspecies—monophyletic groups of taxa with species-level differences in phenotype or genotype that are found exclusively in allopatry or parapatry—present an opportunity to characterize the effects of gene flow on the divergence process. Here, we investigate patterns of gene flow, population structure, and inferred phylogenetic relationships for members of an avian superspecies, the Solomons Monarchs (Aves: Symposiachrus barbatus complex) occupying the Solomon Islands. We found that gene flow among allopatric species matches predictions based on geography, but phylogenetic relationships were not concordant with the most likely colonization history based on a stepping-stone colonization model. Notably, the most isolated island, Makira, has a species that was inferred to be sister to the taxa on all other islands in concatenated phylogenetic analyses, despite Makira being farthest from the presumed original source of immigrants. We use population genetic simulations to demonstrate that such a result could be driven by bias resulting from low levels of gene flow, reflecting a challenge in phylogeographic inference that results when one population is differentially isolated. These simulated findings demonstrate a distinguishability issue in phylogeographic inference, where gene flow and colonization history can be difficult to disentangle. 

Abstract Secondary contact between previously allopatric lineages offers a test of reproductive isolating mechanisms that may have accrued in isolation. Such instances of contact can produce stable hybrid zones—where reproductive isolation can further develop via reinforcement or phenotypic displacement—or result in the lineages merging. Ongoing secondary contact is most visible in continental systems, where steady input from parental taxa can occur readily. In oceanic island systems, however, secondary contact between closely related species of birds is relatively rare. When observed on sufficiently small islands, relative to population size, secondary contact likely represents a recent phenomenon. Here, we examine the dynamics of a group of birds whose apparent widespread hybridization influenced Ernst Mayr’s foundational work on allopatric speciation: the whistlers of Fiji (Aves: Pachycephala). We demonstrate two clear instances of secondary contact within the Fijian archipelago, one resulting in a hybrid zone on a larger island, and the other resulting in a wholly admixed population on a smaller island. We leveraged low genome-wide divergence in the hybrid zone to pinpoint a single genomic region associated with observed phenotypic differences. We use genomic data to present a new hypothesis that emphasizes rapid plumage evolution and post-divergence gene flow. 

Abstract Secondary contact between previously allopatric lineages offers a test of reproductive isolating mechanisms that may have accrued in isolation. Such instances of contact can produce stable hybrid zones—where reproductive isolation can further develop via reinforcement or phenotypic displacement—or result in the lineages merging. Ongoing secondary contact is most visible in continental systems, where steady input from parental taxa can occur readily. In oceanic island systems, however, secondary contact between closely related species of birds is relatively rare. When observed on sufficiently small islands, relative to population size, secondary contact likely represents a recent phenomenon. Here, we examine the dynamics of a group of birds whose apparent widespread hybridization influenced Ernst Mayr’s foundational work on allopatric speciation: the whistlers of Fiji (Aves:Pachycephala). We demonstrate two clear instances of secondary contact within the Fijian archipelago, one resulting in a hybrid zone on a larger island, and the other resulting in a wholly admixed population on a smaller, adjacent island. We leveraged low genome-wide divergence in the hybrid zone to pinpoint a single genomic region associated with observed phenotypic differences. We use genomic data to present a new hypothesis that emphasizes rapid plumage evolution and post-divergence gene flow. 

Abstract The paradox of the great speciators describes a contradictory biogeographic pattern exhibited by numerous avian lineages in Oceania. Specifically, these lineages display broad geographic distributions across the region, implying strong over-water dispersal capabilities; yet, they also display repeated genetic and phenotypic divergence—even between geographically proximate islands—implying poor inter-island dispersal capabilities. One group originally cited as evidence for this paradox is the dwarf kingfishers of the genus Ceyx. Here, using genomic sequencing and comprehensive geographic sampling of the monophyletic Ceyx radiation from northern Melanesia, we find repeated, deep genetic divergence and no evidence for gene flow between lineages found on geographically proximate islands, providing an exceptionally clear example of the paradox of the great speciators. A dated phylogenetic reconstruction suggests a significant burst of diversification occurred rapidly after reaching northern Melanesia, between 3.9 and 2.9 MYA. This pattern supports a shift in net diversification rate, concordant with the expectations of the “colonization cycle” hypothesis, which implies a historical shift in dispersiveness among great speciator lineages during the evolutionary past. Here, we present a formalized framework that explains how repeated founder effects and shifting selection pressures on highly dispersive genotypes are the only ultimate causes needed to generate the paradox of the great speciators. Within this framework, we emphasize that lineage-specific traits and island-specific abiotic factors will result in varying levels of selection pressure against dispersiveness, caused by varying proximate eco-evolutionary mechanisms. Overall, we highlight how understanding patterns of diversification in the Ceyx dwarf kingfishers helped us generate a cohesive framework that provides a rigorous mechanistic explanation for patterns concordant with the paradox of the great speciators and the repeated emergence of geographic radiations in island archipelagoes across the globe. 

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 inTodiramphuskingfishers 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.