Phylogeny and evolution ofStaphyliniformia andScarabaeiformia: forest litter as a stepping stone for diversification of nonphytophagous beetles

Abstract

AbstractThe beetle seriesStaphyliniformia exhibits extraordinary taxonomic, ecological and morphological diversity. To gain further insight into staphyliniform relationships and evolution, we reconstructed the phylogeny ofStaphyliniformia usingDNAsequences from nuclear28SrDNAand the nuclear protein‐coding geneCADfor 282 species representing all living families and most subfamilies, a representative sample ofScarabaeiformia serving as a near outgroup, and three additional beetles as more distant outgroups. Under bothBayesian inference (BI) and maximum likelihood inference (MLI), the major taxa withinStaphyliniformia are each monophyletic: (i)Staphylinoidea, (ii)Hydrophiloidea s.l., and the contained superfamilies (iii)Hydrophiloidea s.s.and (iv) Histeroidea, althoughStaphylinoidea andHydrophiloidea s.l. are not strongly supported byMLIbootstrap. Scarabaeiformia is monophyletic under both methods of phylogenetic inference. However, the relative relationships ofStaphylinoidea, Hydrophiloideas.l.andScarabaeiformia differ betweenBIandMLI: underBI,Staphyliniformia andScarabaeiformia were sister groups; underMLI,Hydrophiloideas.l.andScarabaeiformia were sister groups and these together were sister toStaphylinoidea. The internal relationships inScarabaeiformia were similar under both methods of phylogenetic inference, withCetoniinae,Dynastinae + Rutelinae,Hybosoridae,Passalidae,Scarabaeidae andScarabaeinae recovered as monophyla. Histeridae comprised two major clades: (1)Abraeinae,Trypanaeine andTrypeticinae; and (2)Chlamydopsinae,Dendrophilinae,Haeteriinae,Histerinae,Onthophilinae,Saprininae andTribalinae. The relationships among early‐divergentHydrophiloidea differed betweenBIandMLI, and overall were unresolved or received only moderate to low nodal support. The staphylinoid familiesAgyrtidae,Hydraenidae andPtiliidae were recovered as monophyletic; the latter two were sister taxa, andStaphylinidae + Silphidae was also monophyletic. Silphidae was placed withinStaphylinidae in close relation to a subset ofTachyporinae. Pselaphinae andScydmaeninae were both recovered withinStaphylinidae, in accordance with recent analyses of morphological characters, although not always with recently proposed sister taxa. None of the four major groups ofStaphylinidae proposed byLawrence andNewton (1982) was recovered as monophyletic. Certain highly specialized staphyliniform habits and morphologies, such as abdominal defensive glands and reduced elytra, have arisen in parallel in separate lineages. Further, our analyses support two major transitions to an aquatic lifestyle withinStaphyliniformia: once withinStaphylinoidea (Hydraenidae), and once withinHydrophiloideas.l.(Hydrophiloideas.s.). On a smaller scale, the most common transition is from litter to subcortical or to periaquatic microhabitats and the next most common is from litter to carrion and to fungi. Overall, transitions to periaquatic microhabitats were the most numerous. The broad picture inStaphyliniformia seems to be a high level of evolutionary plasticity, with multiple possible pathways to and from many microhabitat associations, and litter as a major source microhabitat for diversification. InScarabaeiformia, the most common transitions were from litter to foliage, with flowers to litter, litter to flowers, and litter to dung being next, and then litter to roots, logs or carrion. Litter is again the largest overall source microhabitat. The most common transitions were to foliage and flowers. It thus seems that the litter environment presents ecological and evolutionary opportunities/challenges that facilitate entry ofStaphyliniformia andScarabaeiformia into ‘new’ and different ecological adaptive zones.