Diversification and evolution of Hawaiian Megalagrion damselflies (Pinapinao, Odonata: Coenagrionidae)

Hawaiʻi's pinapinao (Megalagrion McLachlan) comprises a radiation of 23 endemic damselfly species within Coenagrionidae. Despite being a unique study system for understanding geology's impacts on evolutionary processes among Odonata, the understanding of these damselflies' temporal, geographic and phylogenetic origins remains incomplete. Testing macroevolutionary hypotheses has been hampered by conflicting topologies. To resolve these uncertainties, we performed phylogenetic analyses including divergence time estimation with 90 nuclear loci (>50 kbp) and 2 mitochondrial loci (>1 kbp), sampling representatives from 37 genera within core Coenagrionidae and 90% of Megalagrion species, including multiple island populations. We used ancestral range estimations, diversification analyses, agent-based simulation modelling and ancestral state reconstruction to infer the group's origin and biogeography and assess traits' roles in diversification. Our findings indicate Megalagrion's ancestor diverged from core Coenagrionidae in the early Eocene (~51 MA) and diversified in the early Miocene (~19 MA), suggesting Megalagrion's MRCA predates Kauaʻi's emergence by 7–21 MY. Diversification analyses suggest a low rate after Megalagrion diverged from Coenagrionidae followed by a sudden increase around 19 MA, and simulation modelling supports extinction playing a significant role. Extant Megalagrion diversity is largely explained by ecological diversification into at least five clades with distinct breeding habitats that likely evolved on Northwestern Hawaiian Islands that are now-sunken seamounts. Speciation continued as descendants dispersed to current Hawaiian Islands as islands emerged. Species breeding in seeps further diversified within the island of Kauaʻi. Our results highlight including geologic changes over time in evolutionary studies and increase understanding of diversification patterns, biogeography and adaptive radiation on islands.

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