Host and geography together drive early adaptive radiation of Hawaiian planthoppers

Abstract

The interactions between insects and their plant host have been implicated in driving diversification of both players. Early arguments highlighted the role of ecological opportunity, with the idea that insects “escape and radiate” on new hosts, with subsequent hypotheses focusing on the interplay between host shifting and host tracking, coupled with isolation and fusion, in generating diversity. Because it is rarely possible to capture the initial stages of diversification, it is particularly difficult to ascertain the relative roles of geographic isolation versus host shifts in initiating the process. The current study examines genetic diversity between populations and hosts within a single species of endemic Hawaiian planthopper, Nesosydne umbratica (Hemiptera, Delphacidae). Given that the species was known as a host generalist occupying unrelated hosts, Clermontia (Campanulaceae) and Pipturus (Urticaceae), we set out to determine the relative importance of geography and host in structuring populations in the early stages of differentiation on the youngest islands of the Hawaiian chain. Results from extensive exon capture data showed that N. umbratica is highly structured, both by geography, with discrete populations on each volcano, and by host plant, with parallel radiations on Clermontia and Pipturus leading to extensive co‐occurrence. The marked genetic structure suggests that populations can readily become established on novel hosts provided opportunity; subsequent adaptation allows monopolization of the new host. The results support the role of geographic isolation in structuring populations and with host shifts occurring as discrete events that facilitate subsequent parallel geographic range expansion.

A holobiont view of island biogeography: unraveling patterns driving the nascent diversification of a Hawaiian spider and its microbial associates

“…However, sampling of additional sites, individuals, and species will be required to disentangle the historical sequence of events explaining the relationship between these sites. Our results are consistent with other population genetic studies on Hawaiʻi Island showing strong differentiation and potential speciation of lineages on the different volcanoes within the island (Funk & Wagner 1995; Holland & Cowie 2007; Muir & Price 2008; Croucher et al 2012; Goodman et al 2019; Eldon et al 2019; Blankers et al 2018). Interestingly, spiders on the mainland would not show this isolation by volcano pattern, because they do efficiently disperse by ballooning; here, our data, in contrast, suggest that the species does not efficiently balloon anymore in this island system (Gillespie et al 2012).…”

“…Sampling of additional sites, individuals, and species will be required to disentangle the historical sequence of events explaining the relationship between these sites. Our results are consistent with other population genetic studies on Hawai’i Island showing strong differentiation and potential speciation of lineages on the different volcanoes within the island (planthoppers, Goodman et al 2019; flies, Eldon et al 2019; crickets, Blankers et al 2018).…”

“…Island showing strong differentiation and potential speciation of lineages on the different volcanoes within the island (planthoppers, Goodman et al 2019;flies, Eldon et al 2019;crickets, Blankers et al 2018).…”

“…Even on the youngest island of Hawai’i, the volcanoes are arranged chronologically, from approximately 430,000 years old (Kohala), to the active flows of Kīlauea, with population structure of local flora and fauna generally shaped by progressive colonization of the newly emerged volcanoes (e.g. Blankers et al 2018; Eldon et al 2019; Goodman et al 2019).…”

“…Even on the youngest island of Hawaiʻi, the volcanoes are arranged chronologically, from approximately 430,000 years old (Kohala), to the active flows of Kīlauea, with population structure of local flora and fauna generally shaped by progressive colonization of the newly emerged volcanoes (e.g. Simon 1987; Wagner & Funk, 1995; Blankers et al 2018; Eldon et al 2019; Goodman et al 2019). Stick-spiders in the genus Ariamnes (Theridiidae) have diversified rapidly across the landscapes in the Hawaiian archipelago (Gillespie & Rivera 2007) and exhibit repeated diversification into ecomorphs adapted to specific microhabitats such as the “gold” ecomorph that is are entirely cryptic on the underside of leaves (Gillespie & Rivera 2007; Gillespie et al .…”