Historical biogeography and ecological opportunity in the adaptive radiation of native Hawaiian leafhoppers (Cicadellidae: Nesophrosyne)

Aim Our aims were to infer the roles of ecology and geology in the adaptive radiation, historical biogeography, and diversification dynamics of the native Hawaiian leafhoppers (Hemiptera: Cicadellidae: Nesophrosyne). Location The Hawaiian Archipelago. Methods A six gene molecular data set for 191 Nesophrosyne species was used to reconstruct relationships in absolute time with relaxed Bayesian methods. Dated phylogenetic hypotheses were used to reconstruct historical biogeography and host plant associations. Phylogenetic clustering methods were implemented to examine the structuring of Nesophrosyne species according to island. Lineage diversification dynamics were inferred using the -statistic and birth-death likelihood methods. Results Nesophrosyne split from a common ancestor with its sister genus 4.5million years ago (Ma), with a basal divergence in Hawaii 3.2Ma. Historical biogeographical reconstructions reveal a Kauai origin for the genus and complex island colonization patterns. Ancestral host plant associations reconstruct Urticaceae and Rubiaceae at the root, with host transitions resulting in host-specific clades. Only species endemic to Kauai are significantly clustered with respect to the whole phylogeny; however, species show significant terminal level clustering for the four main high islands. Diversification rates in Nesophrosyne show an initial burst in net speciation rate with a subsequent decline. Main conclusions Nesophrosyne colonized the Hawaiian Islands after the formation of Kauai. Host plant arrival times and insect-insect competition may have been important in shaping diversification patterns. The plant families Urticaceae and Rubiaceae played critical roles in the early diversification of Nesophrosyne. Island geography imposed significant barriers to gene flow, leading to extensive allopatric speciation and intra-island diversification. A high initial net speciation rate was associated with host plant transitions, and the formation and establishment of Nesophrosyne on multi-volcano islands (e.g. Oahu and Maui Nui). Net diversification rates exhibit a diversity-dependent decline, corresponding to the end phase of island formation.