Multiple colonizations of the Pacific by Peperomia (Piperaceae): Complex patterns of long-distance dispersal and parallel radiations on the Hawaiian Islands

Abstract

Aim: Our understanding of the biogeographical history of the flora of the Pacific is hampered by limited geographical sampling, and the evolutionary history for many species-rich lineages in the Pacific remain poorly known. Here, we examine the spatial and temporal context of the evolutionary history of Peperomia (Piperaceae) in the Pacific, where it is one of the largest angiosperm groups (c. 100 species) and a ubiquitous part of wet forests. We focus on the native taxa on the Hawaiian Islands (25 species) where they represent a hotspot of diversity for the genus in the Pacific. Location: Islands of the Pacific, with focus on the Hawaiian Islands. Taxon: Peperomia (Piperaceae). Methods: Phylogenetic analyses of Pacific taxa were performed using full chloroplast genomes for 115 accessions of Peperomia, including 42 Pacific species (∼40% of the diversity in the Pacific). To examine the timing of colonization and diversification of Peperomia in the Pacific, we implemented a Bayesian relaxed-clock model for the Piperales, using multiple fossils in a fossilized-birth death framework. Results: The Hawaiian Islands (and the Pacific) have been colonized by four separate Peperomia lineages originating from the Neotropics. Endemic Hawaiian taxa are derived from independent radiations from two different ancestors, and represent the first documented case of multiple radiations among species-rich plant groups on the Hawaiian Islands. While extant Peperomia originated in the Eocene (∼54.2 million years old, Ma), most lineages in the Pacific are young and originated in the Pliocene (5.33–2.58 Ma), consistent with the ages of the major islands in the Pacific. Main conclusions: The multiple colonizations and radiations of Peperomia in the Pacific attest to the efficacy of their epizoochorous mode of dispersal. The diversification of two clades in parallel on the Hawaiian Islands suggests that the effect of niche-preemption from the earlier-arriving clade on the diversification of the later-arriving lineage has been weak. Ecological release due to the paucity of large native vertebrate herbivores and the relatively open understoreys of Hawaiian wet forests may have allowed both lineages to flourish, and suggests a context-dependent role of niche-preemption in the assembly of oceanic island biotas.