Non-adaptive Radiation Promotes Phenotypic Diversification and Convergent Evolution of Aposematic Mimicry in a Highly Diverse Genus of Megaloptera

Abstract

Evolutionary radiations are considered key processes underlying the origin of biodiversity. Notably, the mechanisms driving these radiations can vary across organisms and often involve a complex interplay of abiotic and biotic factors. Empirical studies on evolutionary history are crucial for validation of multiple hypothesis regarding the mode of evolutionary radiations. Within the aquatic insect order Megaloptera, the genus Protohermes is the most speciose clade with 90 described species, accounting for around 22% of the total ordinal diversity. Protohermes species are featured by the limited dispersal ability, primarily occurring across the Oriental region, and a range of diversified phenotypes, e.g., highly divergent genital characters, and mimetic coloration alongside shifts in biological rhythm—from nocturnal to diurnal activities. Here we infer the spatiotemporal mode of diversification and associated driving factors of the Protohermes radiation as a test case for exploring the processes and potential mechanisms of evolutionary radiations. We present the first time-calibrated phylogeny of Protohermes using genome-scale data of ultraconserved elements (UCEs) and mitochondrial genes with a comprehensive taxon sampling. Our results reveal a mid-Cretaceous stem age of Protohermes, followed by a recent and steady diversification during the Neogene. Estimation of historical biogeography suggests the genus likely originated from a broad range including the Himalayas-Hengduan Mountains + Indochina + Borneo, with the first two areas serving as the center of early diversification. Our results further suggest that vicariance events, likely attributed to the Cenozoic Himalayan orogeny as well as climate change in East Asia, triggered speciation that coincided with the accumulation of genital divergence. Further enhancement of genital and phenotypic diversification may have been promoted by secondary contacts of allopatric or parapatric lineages following the build-up of species richness, likely facilitating species coexistence and lineage accumulation. We argue that the current species diversity of Protohermes likely resulted from a non-adaptive radiation. Our results highlight the role of geographic vicariance and sexual selection in driving the species and phenotypic diversification in insects.