Diversification of Fijian halictine bees: insights into a recent island radiation

Although bees form a key pollinator suite for flowering plants, very few studies have examined the evolutionary radiation of non-domesticated bees over human time-scales. This is surprising given the importance of bees for crop pollination and the effect of humans in transforming ecosystems via agriculture. In the Pacific, where the bee fauna appears depauperate, their importance as pollinators is not clear, particularly in Fiji where species diversity is even lower than neighbouring archipelagos. Here we explore the radiation of halictine bees in Fiji using phylogenetic analyses of mtDNA COI sequence data. Our analyses indicate the existence of several 'deep' clades whose divergences are close to the crown node, along with a highly derived 'broom' clade showing very high haplotype diversity, and mostly limited to low-lying agricultural regions. This derived clade is very abundant, whereas the more basal clades were relatively rare. Although nearly all haplotype diversity in Fijian Homalictus comprises synonymous substitutions, a small number of amino acid changes are associated with the major clades, including the hyper-diverse clade. Analyses of haplotype lineage accumulation show a steep increase in selectively neutral COI haplotypes corresponding to the emergence of this 'broom' clade. We explore three possible scenarios for this dramatic increase: (i) a key change in adaptedness to the environment, (ii) a large-scale extinction event, or (iii) a dramatic increase in suitable habitats leading to rapid population expansion. Using estimated mutation rates of mitochondrial DNA in other invertebrates, we argue that Homalictus first colonised the Fijian archipelago in the middle-late Pleistocene, and the rapid accumulation of haplotypes in the hyper-diverse clade occurred in the Holocene, but prior to recorded human presence in the Fijian region. Our results indicate that bees have not been important pollinators of Fijian ecosystems until very recent times. Post-Pleistocene climate change and anthropogenic effects on Fijian ecosystems are likely to have greatly transformed pollinator suites from the conditions when those ecosystems were first being assembled.