Leptocoma, Cabanis, 1850

LEPTOCOMA View in CoL TAXONOMY

The movement of species between the genera Cinnyris , Leptocoma and Nectarinia has previously caused confusion for taxonomists working with the black sunbird ( LeCroy, 2010). Our analyses suggest that the Leptocoma genus is not monophyletic ( Fig. 2). However, the genus-level branches in our tree had lower support than the species- and subspecies-level branches due to our use of mtDNA. We strongly recommend further sequencing of all species within Leptocoma to clarify the genus taxonomy.

Previous research based on plumage differences has not proposed any splits or ‘limbo splits’ within the black sunbird ( Eaton et al., 2021). Nonetheless, we found that the black sunbird exhibited genetic divergence consistent with a species-level split between Wallacea and the Sahul Shelf, with a high genetic distance between Sulawesi and PNG (9.1%). This presents a marked contrast to the ‘Sahul sunbird’, which exhibited minimal divergence between those same populations. Further sequencing of birds from intervening areas (such as the Maluku Islands) would help to clarify the boundaries between these potential species. As several intervening populations are absent from our analysis, we cannot rule out the possibility of clinal variation between the Sulawesi and PNG populations ( Brumfield, 2005; Cros & Rheindt, 2017). However, the genetic divergence we found was so strong (mean p-distance of 9.1%, higher than any observed in the olive-backed sunbird complex) that it seems more likely the two populations represent two species. The patterns we have observed suggest a division along Lydekker’s Line, and so we predict that sampling of the intervening populations would show a Wallacean species occurring from Sulawesi to the Maluku Islands and a separate species on New Guinea. This would involve the elevation of one of the Wallacean subspecies names to species level, as Lesson & Garnot (1828) named the black sunbird initially for a specimen from Manokwari (Doréry) on the New Guinea mainland. The discovery of cryptic species in the black sunbird highlights the importance of comprehensive sampling of species across their range, even in the absence of obvious plumage differences.

The structure within the black sunbird contrasted with the patterns shown by the olive-backed sunbird and ‘Sahul sunbird’ in several ways. The black sunbird exhibited a split between Sulawesi and PNG, where the ‘Sahul sunbird’ had a continuous population. The black sunbird also exhibited structure within both of these regions. Most taxonomic treatments ( Cheke et al., 2001; Billerman et al., 2022) split the black sunbird into distinct subspecies in PNG’s Western Province (L. a. aspasia ), Northern Province (L. a. vicina Mayr 1936) and the Bismarck Islands (L. a. corinna). However, Gill et al. (2022) merged L. a. vicina into L. a. aspasia , following Rand (1967). Our genetic work supports L. a. aspasia and L. a. vicina as distinct subspecies, whereas L. a. corinna appears to warrant species status based on ABGD. However, as this was based on a single sequence, we recommend that the Bismarck populations be examined further before a judgement is made. The Menui black sunbird population was genetically distinct from Sulawesi and the land-bridge islands, with a mean genetic distance (1.72%), a distance greater than that between the two subspecies in PNG (1.48%). This population was also found to be distinct in wing length, bill length, weight and tarsus length (MANOVA, P <0.001 in females). These findings suggest the Menui population of black sunbird may warrant recognition as an endemic subspecies.

IMPLICATIONS FOR BIOGEOGRAPHY AND EVOLUTION

The division between the ‘Sahul sunbird’ in Sulawesi and the ‘ornate sunbird’ in neighbouring Borneo ( Eaton et al., 2021) reflects one of the most iconic patterns in biogeography. Between these islands runs the boundary between the shallow Sunda Shelf and the deeper waters of Wallacea, which corresponds to the original and best-known version of ‘Wallace’s Line’ ( Wallace, 1863; Fig. 1). However, Wallace’s Line, Wallacea and related biogeographic ideas have been treated in an entangled way in the literature, the treatment of Sulawesi and the Philippines being particularly contentious ( Ali & Heaney, 2021). The three-way split of the olive-backed sunbird ( Eaton et al., 2021), which our work supports, reinforces the more widely used versions of Wallace’s Line (west of Sulawesi, south-east of the Philippines) and Wallacea (excluding the Philippines), as there are separate species in Wallacea (‘Sahul sunbird’), the Philippines (‘garden sunbird’) and the Sunda Shelf (‘ornate sunbird’).

Unlike Wallace’s Line, a similar barrier in the east has not prevented gene flow in this species, as the ‘Sahul sunbird’ appears to cross Lydekker’s Line with only shallow divergence between populations on either side. It is remarkable that the ‘Sahul sunbird’ appears to maintain a range all the way from Sulawesi to Australia, while the ‘Wakatobi sunbird’ seems to have diverged in a small archipelago nested in this range. Buton is only 27 km from the Wakatobi Islands, while the stretch of islands between Sulawesi and New Guinea contains deep-water barriers up to 100 km wide (this largest barrier is that between Misool and Seram). This striking pattern appears to conform with the ‘taxon cycle’ ( Wilson, 1959, 1961; Ricklefs & Bermingham, 2002), whereby taxa become less dispersive as they age. In this framework, the ‘Sahul sunbird’ would occupy an early stage in the taxon cycle, leading to a dispersive lifestyle and a relatively recent colonization of the Sahul Shelf (or perhaps a back-colonization of Sulawesi) across Lydekker’s Line. This would be in keeping with previous hypotheses that the olive-backed sunbird colonized the Sahul Shelf from Wallacea quite recently ( Schodde, 1977). The ‘Wakatobi sunbird’ would occupy a later stage of the taxon cycle, maintaining a sedentary lifestyle in a small range. The ‘Wakatobi sunbird’ may thus represent a biological species, at it would have maintained its genetic and phenotypic divergence during this recent colonization wave. In other bird families that are widespread in this region, populations on small oceanic islands have been subject to selection for reduced dispersal ability, leading to a pattern of widespread continental species and isolated island relatives ( Pedersen et al., 2018; Le Pepke et al., 2019). We have found evidence that this might also be the case in sunbirds, as the ‘Wakatobi sunbird’ exhibited a significantly lower dispersal index than the ‘Sahul sunbird’ populations of Sulawesi, its land-bridge islands and Menui. Since the earliest days of biogeography ( Wallace, 1880), small, isolated ‘oceanic’ islands like the Wakatobi Islands have been known to harbour disproportionate numbers of endemic species. Birds on smaller islands are subject to different evolutionary processes than those on continents, exhibiting lower effective population sizes and losing fewer deleterious mutations to natural selection ( Leroy et al., 2021).

This study also demonstrates the somewhat stochastic nature of island colonization, as we have found that the sunbirds of Runduma colonized this island (located over 50 km east of the main Wakatobi Archipelago) from an entirely different direction than the white-eyes of the island. These are among the only two small passerines on Runduma that are not island specialists or human commensals. The ‘Wakatobi sunbird’ arrived on this tiny island from the Wakatobi Islands: CJ_W03 was the only haplotype found on Runduma, and is shared with Hoga, Tomia, Binongko and Lintea ( Fig. 3). Runduma’s white-eye population, on the other hand, is most closely related to that of mainland south-east Sulawesi ( O’Connell et al., 2019c). Despite their evolutionary importance, many small islands in the Indo-Pacific have received little ornithological attention until recently ( Monkhouse et al., 2018; O’Connell et al., 2020; Sin et al., 2021).

The black sunbird was already known to be subject to Wallace’s Line, as Sulawesi represents the western extent of its range. Cheke et al. (2001) hypothesized that the black sunbird might be part of a superspecies, with its sister species on the other side of Wallace’s Line. Unlike the ‘Sahul sunbird’, our work indicates that Leptocoma sunbirds have speciated across Lydekker’s Line, based on the strength of divergence between populations in Sulawesi and PNG. Where the ‘Sahul sunbird’ exhibits a similar population throughout Australia and PNG, the black sunbird exhibits noticeable structure on this scale. That the Bismarck Islands hold an endemic taxon illustrates once again the importance of small and isolated islands in generating biodiversity.