The evolution and genomic basis of beetle diversity

Abstract

The order Coleoptera (beetles) is arguably the most speciose group of animals, but the evolutionary history of beetles, including the impacts of plant feeding (herbivory) on beetle diversification, remain poorly understood. We inferred the phylogeny of beetles using 4,818 genes for 146 species, estimated timing and rates of beetle diversification using 89 genes for 521 species representing all major lineages and traced the evolution of beetle genes enabling symbiont-independent digestion of lignocellulose using 154 genomes or transcriptomes. Phylogenomic analyses of these uniquely comprehensive datasets resolved previously controversial beetle relationships, dated the origin of Coleoptera to the Carboniferous, and supported the codiversification of beetles and angiosperms. Moreover, plant cell wall-degrading enzymes (PCWDEs) obtained from bacteria and fungi via horizontal gene transfers may have been key to the Mesozoic diversification of herbivorous beetles—remarkably, both major independent origins of specialized herbivory in beetles coincide with the first appearances of an arsenal of PCWDEs encoded in their genomes. Furthermore, corresponding (Jurassic) diversification rate increases suggest that these novel genes triggered adaptive radiations that resulted in nearly half of all living beetle species. We propose that PCWDEs enabled efficient digestion of plant tissues, including lignocellulose in cell walls, facilitating the evolution of uniquely specialized plant-feeding habits, such as leaf mining and stem and wood boring. Beetle diversity thus appears to have resulted from multiple factors, including low extinction rates over a long evolutionary history, codiversification with angiosperms, and adaptive radiations of specialized herbivorous beetles following convergent horizontal transfers of microbial genes encoding PCWDEs.

The morphological evolution of the Adephaga (Coleoptera)

“…1) was postulated by Beutel & Roughley (1988) for the first time, and since then was confirmed by numerical analyses of morphological characters (e.g. Beutel & Haas, 2000;Beutel et al, 2006Beutel et al, , 2013 and also recent phylogenomic studies (Baca et al, 2017a;McKenna et al, 2019). The monophyly of the aquatic families ('Hydradephaga') was recovered only with analyses of the nuclear ribosomal and mitochondrial genes (Shull et al, 2001;Hunt et al, 2007;López-López & Vogler, 2017).…”

“…Currently, a sister-group relationship with Dytiscoidea ( Fig. 1) is supported by cladistic analyses of large morphological datasets (Beutel et al, 2006(Beutel et al, , 2013 as well as molecular data (McKenna et al, 2015(McKenna et al, , 2019Baca et al, 2017a). This implies that maxillae inserted at the anteroventral margin of the head capsule and movable in all directions (char.…”

“…According to recent analyses of large molecular datasets, Adephaga are probably the sister group of a clade comprising the two small beetle suborders, Archostemata and Myxophaga McKenna et al, 2015;Che et al, 2017;Zhang et al, 2018;McKenna et al, 2019), which are associated with wood or with riparian or hygropetric habitats, respectively. Presently, the lifestyle of the last common ancestor of Adephaga is still equivocal.…”

“…Beutel et al, 2006;McKenna et al, 2015;Baca et al, 2017a), although a sister-group relationship between Trachypachidae and tiger beetles was recently suggested based on analyses of mitochondrial genomes (López-López & Vogler, 2017). From a morphological perspective, this is highly unlikely and also in conflict with analyses of other molecular datasets (McKenna et al, 2015(McKenna et al, , 2019Baca et al, 2017a;Zhang et al, 2018).…”

“…The size of the molecular datasets and taxon sampling increased rapidly (e.g. Balke et al, 2005Balke et al, , 2008López-López & Vogler, 2017;Zhang et al, 2018;McKenna et al, 2019). Baca et al (2017a) analysed 305 ultra-conserved element loci for 18 representatives of all adephagan families except Aspidytidae, with a main focus on the aquatic groups.…”