I am broadly interested in the evolution of biotic interactions, and the consequences of these interactions for the evolution of lineages and clades. Species interactions encompass many of the major problems in evolutionary ecology, and my work targets three specific areas of active inquiry in the field: mechanisms of speciation and diversification in coevolving interactions; the use of phylogenetic and network approaches to ask questions about the evolution of specialists and generalists; and understanding the evolution of the transition between mutualism and parasitism.

Speciation and diversification in coevolving mutualisms

Much of my work has focused on the spectacular co-radiation of endemic leafflower trees (Phyllanthaceae: Phyllanthus s. l.: Glochidion) and their pollinating leafflower moths (Lepidoptera: Gracillariidae: Epicephala) on oceanic archipelagoes in the South Pacific as a model for asking questions about the diversification of intimately associated clades. Like fig wasps and yucca moths, leafflower moths in Asia actively pollinate the flowers of their host plants, but their larvae consume a subset of the host’s seeds. Out of the three hundred described Glochidion from the Asia-Pacific region, I focus on the endemic radiation of 25 species which have radiated on the oceanic islands of Southeastern Polynesia (Cook Islands and French Polynesia). These 25 species show a wide range of floral and ecological diversity, grow from coral cays at sea level to cloud forests at 1500 m elevation, and are all endemic to single archipelagos and often single islands.

I discovered that Epicephala moths have co-colonized remote Pacific islands and pollinate Glochidion trees there in a similar manner to that previously reported from Asia (Hembry et al. 2012), and that despite being intimately associated, phylogenies of host Glochidion and their pollinating Epicephala are far from congruent (Hembry et al. 2013b). In fact, the monophyletic southeastern Polynesian Glochidion radiation has been colonized twice by Epicephala, with the second colonization spreading across at least 12 host species in three archipelagoes in a very short period of time (likely < 1 Ma). I also found that isolation on different islands or archipelagoes likely played a major role in the diversification of the older Epicephala lineage. The reciprocal specialization observed in mutualisms such as these on continents has been thought to constrain their diversification, but these findings indicate that in fact, patterns of interaction between intimately associated yet free-living taxa can be highly dynamic over short periods of evolutionary time.

Currently, I am using a suite of chemical ecology, population genomic, and transcriptomic approaches to examine incipient host race formation in Epicephala moth populations using different host Glochidion species on the islands of Tahiti and Mo’orea (Society Islands, French Polynesia). These islands are less than 1.8 Ma and have between them seven species of Glochidion, all but one of which are endemic. This work is supported by the US National Science Foundation, makes use of field stations run by the Institut de recherche pour le développement and the University of California, Berkeley, and is conducted in collaboration with a team of colleagues around the Pacific Basin, particularly Michael Eisen (UC Berkeley), Katrina Dlugosch (University of Arizona), Tomoko Okamoto (Gifu University), Issei Ohshima (Kyoto Prefectural University), and Jean-Yves Meyer (Délégation à la Recherche, Government of French Polynesia).

Evolution of specialists and generalists in ecological networks

Spatiotemporal variation in the patterns of interactions (networks) between species, and patterns of divergence within species in these networks, may provide insights into the evolutionary dynamics of ecological networks. As a result of the two temporally separated colonizations by leafflower moths, leafflower-leafflower moth networks on the Society Islands are less specialized and less modular in their topologies than those previously reported in continental regions of Asia (Hembry et al., in revision). Sharing of a single pollinator by multiple, sometimes sympatric, Glochidion species is known from several of the Society Islands, and putative hybrid trees are known from sites where two plants share the same pollinator. My ongoing work on incipient host race formation in Society Islands Epicephala (above) aims to determine the role of divergence and speciation in the evolutionary dynamics of ecological networks. I also am collaborating with colleagues Rafael Raimundo and Paulo Guimarães (Universidade de São Paulo) to quantitatively compare the structure of these small networks in order to test hypotheses about the factors driving geographic variation in specialization and modularity in this mutualism. Finally, I am pursuing these questions as a co-organizer (with Jimmy O’Donnell, Dominique Gravel, and Paulo Guimarães) of a recently funded Working Group at NIMBioS on “Spatiotemporal variation and dynamics in ecological networks” (see Delmas et al., preprint, as an example of our work).

Evolutionary ecology of the mutualism-parasitism transition

At the University of Arizona, I am developing leafflower moth species native to the United States as a tractable study system for understanding the evolutionary transition between mutualism and parasitism. Most leafflower moths are mutualists which benefit their host plants as pollinators, but some species do not pollinate their host plants and instead are simply non-pollinating seed predators. In the United States we have native, non-pollinating leafflower moths which have evolved from mutualistic ancestors but continue to be associated with native leafflower species (Phyllanthus spp.), primarily in the southwestern and southeastern states. This work is conducted in collaboration with Katrina Dlugosch (University of Arizona) and Noah Whiteman (UC Berkeley).

Pacific biogeography

Although often tiny and remote, Pacific islands have served as inspiration and testing grounds for major advances in evolutionary biology since Darwin, through Mayr’s work on speciation, MacArthur and Wilson’s theory of island biogeography, and the evolutionary ecology of adaptive radiation. Whereas most of this research has focused on the Hawaiian and Galápagos islands, I have primarily worked on the geologically analogous archipelagos of southeastern Polynesia, which have been comparatively neglected by evolutionary biologists. In a major rearing survey of internally-feeding insects on Glochidion trees across southeastern Polynesia, I uncovered a major role for conserved specialized host associations—and therefore niche conservatism—in the assembly of a remote insular community (Hembry et al. 2013a). I am also synthesizing phylogeographic data from the Society Islands (French Polynesia) and other Pacific archipelagos to test models of diversification on hotspot archipelagos (Hembry and Balukjian 2016; Hembry, in revision).

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