Out of Hawaii: the origin and biogeography of the genus Scaptomyza (Diptera: Drosophilidae)

Abstract

The Hawaiian Archipelago is the most isolated island system on the planet and has been the subject of evolutionary research for over a century. The largest radiation of species in Hawaii is the Hawaiian Drosophilidae, a group of approximately 1000 species. Dispersal to isolated island systems like Hawaii is rare and the resultant flora and fauna shows high disharmony with mainland communities. The possibility that some lineages may have originated in Hawaii and subsequently 'escaped' to diversify on continental landmasses is expected to be rarer still. We present phylogenetic analysis of 134 partially sequenced mitochondrial genomes of Drosophilidae (approx. 1.3 Mb of sequence total) to address major aspects of adaptive radiation and dispersal in Hawaii. We show that the genus Scaptomyza, a group that accounts for approximately one-third of the species-level diversity of Drosophilidae in the Hawaiian Islands, originated in Hawaii, diversified there, and subsequently colonized a number of island and continental landmasses elsewhere on the globe. We propose that a combination of small body size, rapid generation time and unique ecological and physiological adaptations have allowed this genus to effectively disperse and diversify.

New Guinea highland origin of a widespread arthropod supertramp

“…They reveal colonization of Australasia/Oceania out of Eurasia followed by a colonization sequence in the opposite direction in recent geological time, as well as repeated transgressions of Wallace's line ( Filardi & Moyle 2005;Jønsson & Fjeldså 2006). The evolution of megadiverse drosophilid clades in Hawaii and their unexpected subsequent colonization of continental areas and remote islands suggested by O'Grady & DeSalle (2008) is evidence that, for arthropods, even more complex biogeographic scenarios are possible. Polynesian spiders in the family Thomisidae have probably colonized Oceania twice: once from Eurasia and once from the New World (Garb & Gillespie 2006).…”

Are islands the end of the colonization road?

“…More than a third of the studies show evidence of reverse colonization, revealing continental lineages nested within island clades (shown in bold in Table 1). The clearest examples included birds (bananaquit [30], flycatchers [31], monarch flycatchers [10], parrots [32], Darwin's finches [33], catbirds [34] and orioles [35]), lizards [11,36], frogs [9,37], short-faced bats [38], drosophilid flies [39] and turtles [40]. Only a few of these studies explicitly discussed the phenomenon of reverse colonization [10,11,39].…”

“…The West Indian archipelago is probably favorable for reverse colonization because it is sufficiently close to mainland America to produce a dynamic interaction between continents and islands (but see Box 2). However, two of the examples of reverse colonizations [10,39], which involve crossing water gaps of between 2000 and 4000 km, demonstrate that longdistance reverse colonizations are also possible. One of these studies [39] showed that two species of Scaptomyza (Drosophilidae) from Gough Island in the south Atlantic Ocean are nested phylogenetically within a clade of Hawaiian species, and suggested that their ancestors dispersed out of the Hawaiian Islands to continental regions as eggs Figure 1.…”

“…However, two of the examples of reverse colonizations [10,39], which involve crossing water gaps of between 2000 and 4000 km, demonstrate that longdistance reverse colonizations are also possible. One of these studies [39] showed that two species of Scaptomyza (Drosophilidae) from Gough Island in the south Atlantic Ocean are nested phylogenetically within a clade of Hawaiian species, and suggested that their ancestors dispersed out of the Hawaiian Islands to continental regions as eggs Figure 1. World map showing cases of over-water colonizations (dark arrows) and over-water reverse colonizations (orange arrows) from studies of molecular phylogenies of terrestrial animal clades inhabiting both continents and islands (as described in Table 1).…”

Ancient diversification of Hyposmocoma moths in Hawaii

“…It represents one of the most spectacular and species-rich endemic radiations in the archipelago, second in numbers only to the Hawaiian Drosophilidae, which are largely restricted to relatively mesic habitats in the current high islands 12 . In contrast, Hyposmocoma occur on virtually every emergent landmass in the archipelago, and each species appears to be endemic to a single island.…”