The Hawaiian psyllids (Psylloidea, Triozidae) feeding on Metrosideros (Myrtaceae) constitute a remarkable radiation of more than 35 species. This monophyletic group has diversified on a single, highly polymorphic host plant species, Metrosideros polymorpha. Eleven Metrosideros-feeding species included in the Insects of Hawaii by Zimmerman are redescribed, and an additional 25 new species are described. Contrary to previous classifications that placed the Metrosideros-feeders in two genera, Trioza Foerster, 1848 and Kuwayama Crawford, 1911, all 36 named species are placed in Pariaconus Enderlein, 1926; and the relationship of this genus to other Pacific taxa within the family Triozidae, and other Austro-Pacific taxa feeding on host plants in Myrtaceae is clarified. The processes of diversification in Pariaconus include shifts in galling habit, geographic isolation within and between islands, and preferences for different morphotypes of the host plant. Four species groups are recognized: the bicoloratus and minutus groups are free-living or form pit galls, and together with the kamua group (composing all of the Kauai species) form a basal assemblage; the more derived closed gall species in the ohialoha group are found on all major islands except Kauai. The diversification of Pariaconus has likely occurred over several million years. Within island diversification is exemplified in the kamua group, and within species variation in the ohialoha group, but species discovery rates suggest this radiation remains undersampled. Mitochondrial DNA barcodes are provided for 28 of the 36 species. Genetic divergence, intraspecific genetic structure, and parallel evolution of different galling biologies and morphological traits are discussed within a phylogenetic framework. Outgroup analysis for the genus Pariaconus and ancestral character state reconstruction suggest pit-galling may be the ancestral state, and the closest outgroups are Palaearctic-Australasian taxa rather than other Pacific Metrosideros-feeders.

Gall biology, jumping plant lice, mitochondrial DNA barcode, morphology, parallel evolution, Pariaconus , species radiation, taxonomic revision, Triozidae

The Hawaiian Islands are renowned for exemplary species radiations (e.g. Magnacca and Danforth 2006, Rubinoff 2008, Givnish et al. 2009, Lerner et al. 2011, Bennett and O’Grady 2012, Goodman et al. 2014, Magnacca and Price 2015), as well as extraordinary and varied processes of species diversification and evolution (Rivera et al. 2002, Mullen et al. 2007, Rubinoff and Schmitz 2010, Wessel et al. 2013, Gillespie 2016). The primary characteristics of the Hawaiian archipelago that are considered important in speciation processes are: a) multiple islands, b) each island with a geographically concentrated heterogeneity of habitats, c) islands occurring in various degrees of isolation and age in relation to one another, and d) the extreme remoteness of the archipelago. Archipelagos with heterogeneity of habitats and varying geological ages are also found in other island systems, but the extreme isolation of the Hawaiian Islands is unique and may ultimately influence patterns of diversification in ways not found elsewhere (Gillespie et al. 2012, Shaw and Gillespie 2016).

The Hawaiian Islands are home to several endemic psyllid lineages that represent multiple independent colonizations, yet an enduring puzzle is why all of these lineages are from a single psyllid family. The native psyllid fauna is composed entirely of species from the family Triozidae; a single Liviidae specimen (collected in 1925) of an undetermined Paurocephala Crawford, 1913 species (Crawford 1927) remains unconfirmed (Zimmerman 1948). Adjacent continental and Pacific island regions are home to all eight psyllid families (notably Aphalaridae, Carsidaridae, and Psyllidae; Hodkinson 1983, 1986, 1988, Yang and Raman 2007), including the Marquesas and Austral Islands to the south of the Hawaiian Islands. The question therefore remains: why have none of these other psyllid families colonized the Hawaiian archipelago? Perhaps triozid psyllids are somehow more successful colonizers of remote islands. Other Pacific archipelagos are located within 1000 km distance of habitable landmasses (via many small islands), whereas the Hawaiian Islands are more than 3000 km from another landmass, which makes dispersal ability a critical factor (Hembry et al. 2013). However, it is difficult to reason how dispersal ability alone could discriminate between psyllid families. The colonization of remote landmasses containing few familiar host plants could be facilitated by an ability to survive on suboptimal or unfamiliar hosts (Roderick and Percy 2008, Percy 2011), and although the majority of psyllids are mono- or oligophagous (feeding on one or a few plant species within the same genus), the family Triozidae includes the largest number of psyllid species exhibiting atypically broad host preference (Ouvrard et al. 2015). An ancestral preadaptation to expanded host ranges (Janz et al. 2006, Janz and Nylin 2008) may be an advantage allowing successful colonization that may then cycle back to specialization given ecological opportunity (e.g. vacant niches, proximity of alternate hosts) (Percy et al. 2004). This scenario could explain both the imbalance in colonization potential of the different psyllid families and the observed pattern of within archipelago host specialization after establishment. There are also examples from introduced species of host range expansions post colonization of a new region, e.g. Trioza eugeniae Froggatt, 1901, which is associated with Syzygium (Myrtaceae) in its native Australian range, but in California where it is introduced it occurs on cultivated Metrosideros (Percy et al. 2012).

Many of the Hawaiian triozid species have been ascribed to endemic genera rather than placed within more widespread and established generic groupings; exceptions include taxa placed in Kuwayama Crawford, 1911 and Trioza Foerster, 1848, two highly artificial genera found in old and new world regions (Hodkinson 1983, 1986, 1988). The practice of erecting endemic Hawaiian genera does, however, often reflect unusual morphology as well as ambiguous affinities to genera elsewhere. The absence of such conspicuous morphological characters distinguishing Metrosideros-feeding species in the Hawaiian Islands is notable, and this is partly responsible for the placement of these taxa in Kuwayama and Trioza. Trioza, in particular, is a large, poorly defined, polyphyletic genus into which many disparate species have been placed (Burckhardt and Ouvrard 2012, Ouvrard et al. 2015). Kuwayama is also considered problematic and currently includes unrelated taxa from the American continent and Hawaiian Islands. Although both Enderlein (1926) and Crawford (1918) recognized the artifice of placing Hawaiian taxa in Kuwayama, it was Enderlein (1926) who removed three of the Metrosideros-feeding species to a separate, endemic genus, Pariaconus Enderlein, 1926; not based on unique differences, but rather on an absence of distinct affinities with other taxa in Kuwayama (Enderlein 1926). Despite the absence of distinct morphological synapomorphies, endemic generic status for the Metrosideros-feeding species is clearly supported by this study. Pariaconus is not close to the type species of Trioza, Trioza urticae (Linné, 1758), nor to the type species of Kuwayama, Kuwayama medicaginis (Crawford, 1910). However, closer taxonomic affinities outside the Hawaiian Islands remain to be clarified with yet further outgroup sampling.

All Hawaiian psyllid lineages appear to exhibit high host specificity that has been conserved during in situ diversification (e.g. Pariaconus on Metrosideros (Myrtaceae), Swezeyana Caldwell, 1940 on Planchonella (Sapotaceae), Hevaheva Kirkaldy, 1902 on Melicope (Rutaceae), Megatrioza Crawford, 1915 on Pritchardia (Arecaceae)) (Zimmerman 1948, Nishida et al. 1980, Uchida and Beardsley 1988). Pariaconus is an endemic Hawaiian genus with more than 35 species found on a single host plant (Metrosideros polymorpha) (Table 1) and species discovery rates suggest this number will continue to increase. This pattern of within host diversification is atypical for psyllids, as well as for other phytophagous insects (Joy and Crespi 2007). The rarity of speciose radiations on a single host plant is thought to be due, in part, to processes such as competitive exclusion between closely related species (Percy 2003b, 2011, Després and Cherif 2004, Gold et al. 2009). A much more common process associated with speciation in phytophagous insects, including psyllids, is switching to different host plants (Tilmon 2008, and chapters therein, Ouvrard et al. 2015), and a high degree of host specialization in psyllids appears to constrain most switching to closely related plant species with much rarer saltationary leaps to unfamiliar hosts (e.g. Burckhardt and Basset 2000, Percy et al. 2004, Ouvrard et al. 2015). The question is therefore whether diversification in Pariaconus evolved via atypical evolutionary processes, or whether typical evolutionary pathways have been co-opted in atypical ways.

In order to understand how the Pariaconus radiation has evolved and persisted on M. polymorpha, it is crucial to appreciate the ecological background over which the speciation processes have played out. Except in the very driest regions, M. polymorpha is the dominant native shrub in the Hawaiian Islands (Mueller-Dombois 1987, 1992, Dawson and Stemmermann 1999). There are currently eight M. polymorpha varieties recognized, but these inadequately represent the complex morphological variation observed within and between islands (Percy et al. 2008, Harbaugh et al. 2009, Wright and Ranker 2010, Stacy et al. 2014, 2016). In growth habit, the variation includes statuesque trees (~20 m) and low growing shrubs (< 1 m). Habitats may be wet or dry forest, bogs, or almost soil-less lava flows a few years old (Stacy et al. 2014, 2016). Studies of the morphological variation (e.g. leaf pubescence and thickness), including common garden and genetic studies, have concluded that the diversity of phenotypes is controlled by complex genome-environment interactions, as well as population dynamics (Cordell et al. 1998, Gruner et al. 2005, Wright and Ranker 2010, Stacy et al. 2014). Indeed, the presence of different morphotypes growing side by side in the same environment but exhibiting little or no genetic variation for neutral markers is one of the most striking features of this polymorphic plant species (Percy et al. 2008, Wright and Ranker 2010, Stacy et al. 2016).

The patterns of diversity observed in Pariaconus would not be markedly different from other radiations (e.g. those found in the Atlantic island archipelago of the Canary Islands; Percy 2003a, 2003b) if the variation found in M. polymorpha was represented by 20 or more distinct species with speciation occurring primarily via a process of switching between hosts. The Canary Islands, although less remote, share many attributes with the Hawaiian Islands, e.g. five major islands formed in an age progressive series over a volcanic hot spot, with similar degrees of habitat heterogeneity and inter-island distances (Neall and Trewick 2008, Bogaard 2013). In the Hawaiian Islands, the high degree of polymorphism in M. polymorpha may be promoting psyllid speciation processes akin to the effect of multiple host plants. However, understanding the diversification processes is further complicated by shifts in galling biology, and shifts to galling different plant organs.

When considering the origins of Hawaiian Pariaconus, Crawford (1918) thought “the original immigrant to be one inhabiting leaf galls”, and although originally describing different Pariaconus taxa in separate genera, he also stated, “as new species evolved from this, some have retained the gall-making habit … others have taken to living free in the nymphal stages, while still others have gone off to other plants making leaf galls or living free”, in other words he contemplated the scenario that all the Metrosideros-feeders, and even all Hawaiian Triozidae could be a monophyletic group. This illustrates Crawford’s ambiguous approach to the concept of monophyly. He apparently saw no conflict in simultaneously considering evolutionary shifts in situ within the Hawaiian Islands, but at the same time ascribing these island species to different genera based on superficial morphological affiliations with continental groups. Indeed, Crawford noted, when assigning three newly described Hawaiian Metrosideros-feeding species to Kuwayama, that “it seems certain that the species placed in this genus do not represent a common origin at all, but independent or parallel evolution toward the same end” (Crawford 1918). He goes on, “the three species seem almost certainly to have been derived from some Trioza species, probably T. ohiacola [P. ohiacola], or an ancestral type proceeding it”. He is apparently confirming here that he views taxonomic groupings as artificial and more for convenience than necessarily representative of evolutionary origins.

Multiple shifts in galling biology on the same plant species have rarely been documented. One of the few known systems is the gall-inducing Asphondylia Loew, 1850 (Cecidomyiidae) flies found on Larrea tridentata (Joy and Crespi 2007) where diversification has involved numerous shifts between different plant organs (leaves, buds, flowers, and stems) of the same host-plant species, thereby ecologically partitioning the host plant, with additional temporal as well as spatial separation. In a study of oak-gall wasps, Cook et al. (2002) found speciation more likely to involve shifts to galling different plant organs if the host oaks were more closely related (within taxonomic sections) than when host shifts involved oaks in different sections. Another study looking at Eurosta Loew, 1873 (Tephritidae) gall flies on Solidago where sympatric speciation has involved shifting between leaves and stems has suggested gall makers are more likely to speciate sympatrically than non-gall makers (Craig et al. 1994). These findings are consistent with patterns observed in the Metrosideros-psyllid system and thus help to frame hypotheses that may explain diversity in Hawaiian Pariaconus. However, analysis of the processes of speciation in Pariaconus may be additionally complicated by the underlying complexity inherent in the mosaic of plant phenotypes, and the frequent co-occurrence of alternate Metrosideros morphotypes.

The objectives of this study are, a) to describe the diversity of species feeding on Metrosideros in the Hawaiian Islands, b) to identify patterns of diversity within and between islands across the archipelago, c) to test putative outgroup affiliations, and d) to better understand the origins and evolution of Pariaconus.