Phylogeography of a ‘great speciator’ (Aves:Edolisoma tenuirostre) reveals complex dispersal and diversification dynamics across the Indo‐Pacific

Abstract

Aim We derive a new phylogenetic framework of the Indo‐Pacific avian genus Edolisoma based on a dense taxon sampling and use it in an explicit spatiotemporal framework to understand the history of intraspecific diversification dynamics in a ‘great speciator’, the Cicadabird Edolisoma tenuirostre/remotum complex. Location The Indo‐Pacific island region, Australia and New Guinea. Taxon Corvoid passerine birds (Passeriformes). Methods We used Bayesian phylogenetic methods (beast) to construct a time‐calibrated molecular phylogeny of all 19 species in the genus Edolisoma and 27 of 29 subspecies of the E. tenuirostre/remotum complex (previously Coracina tenuirostris) primarily based on one mitochondrial DNA marker. Ancestral area reconstruction methods (‘BioGeoBEARS’) were used to infer the historical biogeography of the genus. We used population‐level analyses to assess intraspecific phylogeography and a molecular species delimitation test to evaluate the current taxonomy. A morphometric dataset was used to discuss differential dispersal ability among taxa. Results Edolisoma originated in the late Miocene and diversification within the E. tenuirostre/remotum complex began in the Pleistocene. Within the North Melanesian and North Wallacean archipelagos, which have experienced several waves of diversification, we find significant patterns of genetic isolation by distance, but not within the Australo‐Papuan ‘mainland’, which was recently back‐colonized from these archipelagos. Based on the phylogeny, we suggest several taxonomic changes. We also discuss evidence of taxon cycles within Edolisoma based on correlations of species age, elevational ranges and dispersal ability. Main conclusions The biogeographical history and patterns of differentiation between phylogroups within E. tenuirostre support the importance of barriers to gene flow in island systems. Examples of both recent genetic exchange across significant sea barriers and differentiation across much smaller water gaps suggest complex dispersal and diversification dynamics. The capacity for dispersal away from islands, and gradual shifts in dispersal ability in relation to the geographical setting, is supported as important factors in generating a ‘great speciator’.

Diversification of a ‘great speciator’ in the Wallacea region: differing responses of closely related resident and migratory kingfisher species (Aves: Alcedinidae:Todiramphus)

“…The lack of diversification in such a widespread bird seems remarkable, particularly considering the level of diversification in the Collared Kingfisher species complex (Andersen et al 2015b) and several other vagile taxa (Cibois et al 2014, Andersen et al 2015a, Garcia-R et al 2017) over the same area as the Sacred Kingfisher's range. However, these findings for the Sacred Kingfisher tally with those of Pedersen et al (2018), who found that populations of the Common Cicadabird species complex (E. t. pellingi and E. t. obiense) remained morphologically and genetically similar, despite being separated by 500 km of deep ocean. One population of the Common Cicadabird (E. t. tenuirostre) also migrates between Australia and New Guinea (Taylor & Kirwan 2018).…”

“…Mayr and Diamond (2001) developed the 'great speciator' concept for their study system in Northern Melanesia to describe a group of birds with high inter-island geographical variation, including diverse taxa found across many islands (e.g. In recent years modern molecular methods have enabled researchers to begin to uncover the intricate evolutionary histories of the 'great speciators', showing them to be complexes of closely related species (Andersen et al 2013, Irestedt et al 2013, Pedersen et al 2018. Because of their wide ranges and multiple distinct populations, the 'great speciators' have provided ideal study systems for developing many key concepts in evolutionary biology (Mayr 1942, Diamond 1974, Diamond et al 1976).…”

Reconciling supertramps, great speciators and relict species with the taxon cycle stages of a large island radiation (Aves: Campephagidae)

“…Elevational ranges were obtained from Taylor () and following Pedersen et al. () we assigned all species into one of three elevational range classes: species usually inhabiting (a) coastal, (b) lowland or (c) montane areas (see Table S1.3 in Appendix S1).…”

“…These species may be undifferentiated and continuously distributed across all small islands in a region, often including coastal and other marginal habitats on larger islands within their range. Diamond (, ) was not able to assess the temporal mode of supertramp evolution, but today we know, from molecular phylogenetic analyses, that the supertramp stage can extend over 700 kyr (Jønsson et al., ; Pedersen, Irestedt, Joseph, Rahbek, & Jønsson, ). Rapid sweepstake colonizations followed by a reduction in dispersal ability and subsequent population differentiation across the range of a widespread ‘tramp’ species (isolation by distance) may then result in a stage where the species is recognized as a ‘great speciator’ (stage II), which represents another ‘extreme’ diversification stage (Figure ).…”

“…We focus on the three most species‐rich genera of the core Campephagidae Coracina (cuckoo‐shrikes), Edolisoma (cicadabirds) and Lalage (trillers), which have overlapping distributions across the Indo‐Pacific island region including Australia and South Asia. This group includes both single island endemics, widespread species with extreme geographical variation (great speciators) and highly vagile tramp or supertramp species with large continuous distributions (Fuchs, Cruaud, Couloux, & Pasquet, ; Jønsson et al., ; Jønsson, Irestedt, et al., ; Pedersen et al., ).…”