Phylogenomic relationships of bioluminescent elateroids define the ‘lampyroid’ clade with clicking Sinopyrophoridae as its earliest member

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 of Sinopyrophorus Bi & 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 clicking Sinopyrophorus and 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.

Click Beetle Mitogenomics with the Definition of a New Subfamily Hapatesinae from Australasia (Coleoptera: Elateridae)

“…For example, Kundrata et al [ 14 ] recovered Negastriinae and Cardiophorinae at the deepest split of click beetles and Elaterinae as a derived lineage [ 64 ], but Kundrata et al [ 20 ] conversely presented Elaterinae as a sister to other subfamilies and Negastriinae and Cardiophorinae as terminal lineages. Now, transcriptomics robustly supports the second alternative [ 22 , 25 , 26 ], and we also recover such relationships with our dataset using mitochondrial genomes ( Figure 2 and Figures S6 and S7 ).…”

“…There are several subfamilies of click beetles for which are not available mitogenomes, and in some cases even any molecular data. These are Neotropical Campyloxeninae, European neotenic Omalisinae, and several small lineages as Physodactylinae, Subprotelaterinae, Hemiopinae, Oestodinae, Tetralobinae, Thylacosterninae, and Lissominae [ 2 , 13 , 14 , 15 , 16 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ]. We considered the earlier recovered molecular relationships of the later five and they have never been recovered in relationships to our focal taxa Hapatesus (Hapatesinae) and Eudicronychus (Eudicronychini).…”

“…In such a way, we avoided problematic alignments of length variable loop regions of 18S and 28S rRNA genes. Besides, we now have an opportunity to validate the inferred topology with earlier phylogenomic topologies which are based on >4000 orthologs [ 26 ]. Additionally, we encountered in our data strong base compositional and mutational rate heterogeneity which may violate the stationarity assumption of the widely used site-homogeneous models of nucleotide substitution [ 68 , 69 ] and may negatively affect the reconstruction of phylogenetic relationships.…”

“…Later studies using transcriptomic data and whole-genome shotgun sequencing robustly supported earlier inclusion of Drilini (in Agrypninae), Plastocerinae, and Omalisinae within Elateridae [ 25 ]. Additionally, genomic data indicated the close relationships of clicking and non-clicking elateroids, and a family Sinopyrophoridae was proposed for an elaterid-like sister group of bioluminescent, soft-bodied fireflies and glowworm beetles (Lampyridae, Phengodidae, Rhagophthalmidae [ 26 ]). Simultaneously, these analyses have shown that further data are needed to propose a robust phylogeny that can serve as a basis for the natural classification of click beetles.…”

The Fossil Record of Elateridae (Coleoptera: Elateroidea): Described Species, Current Problems and Future Prospects

“…The click-beetles (Elateridae) are the major family in Elateroidea, comprising more than 10,000 described species worldwide [ 1 ]. Despite the efforts of numerous studies using morphological or molecular data, the classification and phylogenetic relationships within the family remain far from fully understood [ 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 ]. Taking this into consideration, further development of click-beetle systematics and understanding their evolution would certainly benefit from integrating modern molecular-based methods and morphology with fossils into a combined phylogenetic approach.…”