Cinnyris, Cuvier, 1816

Marcaigh, Fionn Ó, Kelly, David J., O’Connell, Darren P., Analuddin, Kangkuso, Karya, Adi, Mccloughan, Jennifer, Tolan, Ellen, Lawless, Naomi, Marples, Nicola M., O, Darren P. & Connell, 2022, Small islands and large biogeographic barriers have driven contrasting speciation patterns in Indo-Pacific sunbirds (Aves: Nectariniidae), Zoological Journal of the Linnean Society 198 (1), pp. 72-92 : 13

CINNYRIS TAXONOMY

Our results indicate that the olive-backed sunbird represents a superspecies and should be split into at least four species (Supporting Information, Table S10). We have found support for the three-way split suggested by Eaton etal. (2021) while also providing the first genetic, acoustic and morphological evidence that the ‘Wakatobi sunbird’ warrants recognition as a full species. The Wakatobi population exhibits a strikingly non-linear arrangement of population structure, with a range enveloped within that of the more widespread species, and had previously been suggested as a ‘limbo split’ ( Rheindt, 2021) based on plumage differences alone ( Eaton et al., 2021). Our study has supported these differences with matching patterns in mtDNA and integrative species delimitation or ‘Tobias scoring’ ( Tobias et al., 2010). Due to the lower effective population size of mtDNA, along with other factors, differences in mtDNA should be integrated with other forms of evidence in this way ( Rubinoff & Holland, 2005). In the light of this new integrative evidence, we recommend that the ‘Wakatobi sunbird Cinnyris infrenatus ’, originally named by Hartert (1903), be reinstated as a separate species. In addition to its genetic divergence ( Fig. 3 ), the ‘Wakatobi sunbird’ has shorter wings, a shorter bill and longer tarsi than the ‘Sahul sunbird’ (Supporting Information, Fig. S9), as well as exhibiting slower and higher pitched calls over a smaller bandwidth (Supporting Information, Fig. S11). This study is one of several to have remarked upon the distinctness of the Wakatobi avifauna ( Kelly et al., 2014; O’Connell et al., 2019a, c), and so we reiterate the recommendation of O’Connell et al. (2020) that the Wakatobi Islands should be protected as an Endemic Bird Area ( Stattersfield et al., 1998).

In addition to the distinctive nature of the Wakatobi lineage, our work supports the splits suggested by Eaton et al. (2021) and one possible additional split in the Philippines ( Fig. 5 ). Under the Eaton et al. (2021) treatment, populations from Sulawesi to the Sahul Shelf and the Solomon Islands were recognized as a species-level taxon, the ‘Sahul sunbird Cinnyris clementiae ’, the Sunda Shelf populations become ‘ornate sunbird Cinnyris ornatus ’ and the Philippine birds retain the Cinnyris jugularis name and take ‘garden sunbird’ as a common name. This is supported by deep genetic divergences (all greater than 5%) between these three putative species, with the Sahul Shelf represented by our new Sulawesi, Australian and PNG sequences along with Solomon Islands birds from Smith & Filardi (2007), the Sunda Shelf by a sequence from Borneo ( Boyce et al., 2019) and the Philippines by a number of previously published partial sequences (Supporting Information, Table S3). Although this split has been suggested previously based on limited sampling and incomplete sequences, our more comprehensive sampling of full sequences, taken from both ends of the new ‘Sahul sunbird’ species range, offers stronger support for the division. Our study has also suggested another potential split in this species complex ( Fig. 5 ), outside the geographic range covered in detail by Eaton et al. (2021). ABGD considered the aurora sequences from Busuanga in the western Philippines to represent a distinct species, with a mean genetic distance of 4.5%, from the greater Philippine archipelago (subspecies obscurior and jugularis ). Ornithologists ( Rand, 1951; Billerman et al., 2022) have grouped the aurora subspecies separately from these other Philippine subspecies due to its orange breast plumage. The western chain of islands on which the aurora subspecies occurs is geologically and biogeographically distinct from the greater Philippine archipelago ( Diamond & Gilpin, 1983). The aurora subspecies displayed a similar level of genetic divergence to that of the more thoroughly sampled ‘Wakatobi sunbird’, but was represented in our analysis by two partial ND2 sequences from Campbell (2013), and so we recommend further sampling of this population.

The lack of divergence between the Menui population and the wider south-east Sulawesi population in the ‘Sahul sunbird’ confirms that the Menui population belongs to the plateni subspecies. On the Sahul Shelf itself, our ‘Sahul sunbirds’ exhibit a uniform population across PNG and Australia. This is in keeping with the current assignment of these populations to one subspecies, Cinnyris jugularis frenatus .

Figures

Figure 3. A, geographic distribution of Cinnyris jugularis (sensu Gill et al., 2022) haplotypes in Wallacea and the Sahul Shelf. Each circle represents an island and the fractions within the circle the haplotypes found on that island, proportioned to represent the frequency of each haplotype.The haplotypes are named according to the species-level divisions suggested by ABGD and coloured to represent the clades supported by our phylogenetic analyses. B, TCS haplotype network of Cinnyris haplotypes. Each circle represents a unique ND2–ND3 haplotype, sized to represent how many birds carried that haplotype. The hatch marks represent mutations between haplotypes, also given as numbers in brackets for the wider divergences.The unfilled, white nodes represent hypothetical ancestral states. C, Bayesian consensus tree of Cinnyris haplotypes. Nodes are labelled with Bayesian probabilities.

Figure 5. A, map of the Indo-Pacific with the range of the olive-backed sunbird shaded, as currently recognized by BirdLife International. Sampling sites of the birds included in our 697 bp partial ND2 analysis are marked with different triangles, according to the species they were assigned to by ABGD. Currently recognized subspecies are labelled (Gill et al., 2022). B, mean genetic distance (uncorrected p-distance) between each of the species recognized by ABGD, based on a 697 bp partial ND2 alignment. C, simplified version of a combined maximum likelihood (ML) and Bayesian phylogenetic tree of 697 bp of olive-backed sunbird ND2. In this figure the outgroup is omitted and each of the ABGD species is collapsed into a single branch. Nodes are labelled with Bayesian probability/ ML bootstraps.