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We understand very little about the timing and origins of bioluminescence, particularly as a predator avoidance strategy. Understanding the timing of its origins, however, can help elucidate the evolution of this ecologically important signal. Using fireflies, a prevalent bioluminescent group where bioluminescence primarily functions as aposematic and sexual signals, we explore the origins of this signal in the context of their potential predators. Divergence time estimations were performed using genomic-scale datasets providing a robust estimate for the origin of firefly bioluminescence as both a terrestrial and as an aerial signal. Our results recover the origin of terrestrial beetle bioluminescence at 141.17 (122.63–161.17) Ma and firefly aerial bioluminescence at 133.18 (117.86–152.47) Ma using a large dataset focused on Lampyridae; and terrestrial bioluminescence at 148.03 (130.12–166.80) Ma, with the age of aerial bioluminescence at 104.97 (99.00–120.90) Ma using a complementary Elateroidea dataset. These ages pre-date the origins of all known extant aerial predators (i.e. bats and birds) and support much older terrestrial predators (assassin bugs, frogs, ground beetles, lizards, snakes, hunting spiders and harvestmen) as the drivers of terrestrial bioluminescence in beetles. These ages also support the hypothesis that sexual signalling was probably the original function of this signal in aerial fireflies. 

Abstract Bioluminescence has been hypothesized as aposematic signalling, intersexual communication and a predatory strategy, but origins and relationships among bioluminescent beetles have been contentious. We reconstruct the phylogeny of the bioluminescent elateroid beetles (i.e. Elateridae, Lampyridae, Phengodidae and Rhagophthalmidae), analysing genomic data ofSinopyrophorusBi & Li, and in light of our phylogenetic results, we erect Sinopyrophoridae Bi & Li,stat.n. as a clicking elaterid‐like sister group of the soft‐bodied bioluminescent elateroid beetles, that is, Lampyridae, Phengodidae and Rhagophthalmidae. We suggest a single origin of bioluminescence for these four families, designated as the ‘lampyroid clade’, and examine the origins of bioluminescence in the terminal lineages of click beetles (Elateridae). The soft‐bodied bioluminescent lineages originated from the fully sclerotized elateroids as a derived clade with clickingSinopyrophorusand Elateridae as their serial sister groups. This relationship indicates that the bioluminescent soft‐bodied elateroids are modified click beetles. We assume that bioluminescence was not present in the most recent common ancestor of Elateridae and the lampyroid clade and it evolved among this group with some delay, at the latest in the mid‐Cretaceous period, presumably in eastern Laurasia. The delimitation and internal structure of the elaterid‐lampyroid clade provides a phylogenetic framework for further studies on the genomic variation underlying the evolution of bioluminescence.