Why do different oceanic archipelagos harbour contrasting levels of species diversity? The macaronesian endemic genus Pericallis (Asteraceae) provides insight into explaining the ‘Azores diversity Enigma’

What does explain the ADE-like pattern for Pericallis?

A key difference between Pericallis diversity patterns in the two archipelagos concerns the relationship between morphological and molecular (AFLP) data. We observe isolation by distance (IBD) for AFLP data in both archipelagos (Table 4). In the Canary Islands AFLP data showed some congruence with current taxonomic treatments although with sharing of genetic material evident between taxa. In the Azores, three AFLP groups were defined, broadly corresponding to the central group, São Miguel, and Santa Maria (thus two genetic SIEs are defined; Fig. 3a), a pattern that was incongruent with the recognised subspecies. These findings are similar to Schaefer et al. [10] who observed genetically differentiated SIEs in a suite of apparently widespread Azorean endemic lineages.

A smaller proportion of the AFLP variation was explained by between-island differences in the Canaries than in the Azores (Table 3), and there was greater sharing of genetic material between islands in the Canaries than between Santa Maria, São Miguel and the Central island group in the Azores. Thus, AFLP data suggest a stronger geographical signal in the Azores than in the Canaries, and the AFLP pattern in the Azores is at odds with the pattern observed with morphology whereas AFLP data and morphology are broadly congruent in the Canaries. Several factors may explain the differences. The generally smaller population sizes in the Azores than in the Canaries, partly influenced by anthropogenic factors such as habitat destruction, may have led to stronger genetic structuring. While populations in Santa Maria and, to a lesser extent, São Miguel may be large, those in the central group of the Azores are typically comprised of less than 100 individuals; in the Canaries, populations are often extensive. Geographic isolation between populations is a second factor that may explain the greater geographical structuring of AFLP data in the Azores. Colonization of a new island is the result of a combination of dispersal and establishment. Pericallis achenes are wind dispersed (anemochorous) that likely facilitates long distance dispersal to islands [38], yet the predominant dispersal syndromes observed in different island floras appear to be highly idiosyncratic [39]. Geographic distance is critical in the process of colonization and therefore, greater geographic distance between islands may facilitate inter-island diversification [35]. In the Canaries, the maximum distance between two neighbouring islands on which herbaceous Pericallis occur is ~60 km. In the Azores, the distances between Santa Maria and São Miguel (~80 km) and between São Miguel and the central group (~120 km) are both greater, and this is likely to promote greater genetic differentiation by geographic isolation (Fig. 1; [40, 41]). Within the Azorean central island group, wherein all except one accession are placed in the same genetic cluster, the islands are generally in closer proximity than in the Canaries (minimum distance: 6–19 km) and this may explain the lack of differentiation between populations on these islands. Terceira is a notable exception; at 39 km from São Jorge it is more isolated than the islands of Tenerife and La Gomera in the Canaries (28 km). The lack of differentiation of Terceira populations from other central sub-archipelago populations was also observed in genetic diversity analyses of the endemic Picconia azorica [42], but the island has been found to harbour distinct genetic lineages in other taxa [10].

In the Canaries, molecular and morphological diversity were both correlated with geographical distance and climatic variation (Table 4). However, geographical distance and climate were themselves correlated (r?=?0.21, P?=?0.001 for geographic distance vs PC1; r?=?0.3, P?=?0.001 for geographic distance vs. PC2). Thus, morphologically differentiated clusters in the Canarian lineage tend to be both geographically isolated and climatically differentiated (Fig. 2d). The group may therefore be considered to be an example of a classic island adaptive radiation, within which geographical isolation and ecological differentiation have acted in concert in the diversification of the group [43, 44]. In a review of molecular phylogenies of island lineages, Baldwin et al. [45] concluded that inter-island allopatry was an important driver of diversification in the Canaries given that closely related taxa often occupy apparently similar habitats but on different islands. Our results for Canarian Pericallis suggest that the closely related and recently diverged taxa occupy broadly similar habitats but there is some evidence for bio-climatically differentiation between taxa that may have further contributed to their diversification. Other putative examples of ‘inter-island allopatry’ in the Canaries may also involve ecological differentiation (e.g. Gonosperminae, [46]; Lotus, [47] or Bystropogon [48]).

In the Azores, morphology showed no correlation with geographical distance but was correlated with climate when the possible noise caused by geographical distance was taken into account in the partial dbRDA (Table 4). In contrast, AFLP data were not correlated with climate when geographical distance was taken into account. Thus, molecular patterns appear to reflect island isolation and genetic drift (inter-island allopatry) whereas the morphological patterns reflect ecological differentiation. The latter has involved shifts between climatic zones that have occurred within islands or island groups at least twice in parallel in the central group and in São Miguel. Therefore, in contrast to the Canaries, the effects of geographic isolation and ecological differentiation in Azorean Pericallis are uncorrelated.

The independent origins of the high altitude subsp. caldeirae ‘morphotype’ on separate islands in the central group and São Miguel may reflect underlying phenotypic plasticity, i.e. the property of a genotype to express distinct phenotypes in different environments [49]. The role of phenotypic plasticity in diversification is widely debated (see [50] and references therein). However, phenotypic plasticity provides opportunities for diversification, including ecological adaptation and speciation [50]. The maintenance of morphological differences in spite of limited genetic differentiation between taxa could also reflect strong ecological selection on few loci of large effect that are not detected by the AFLP analyses due to limited genome coverage [51–54]. Recent studies have also provided evidence for ecological divergence correlating with epigenetic changes in DNA methylation [55]. The potential role of epigenetics in generating phenotypic plasticity in the diversification of recently evolved oceanic island lineages has yet to be explored and may be significant.

Incongruence between molecular and morphological patterns may reflect a more general pattern in the Azorean flora. For example, Euphorbia stygiana subsp. stygiana shows geographical structuring of molecular data yet morphological differences to support this have not been identified [10]. Molecular studies of the Azorean Ammi lineage [10] and Azorean Juniperus [56] have demonstrated geographically structured patterns that are incongruent with morphology. It is important to note that although our sampling ensured a broad distributional range and included almost all known Pericallis populations in both archipelagos, the number of samples with both morphological and genetic data was limited (Additional file 4: Table S1). Therefore, future studies with an increased number of individuals per population may help further explain the patterns.