Invertebrate and avian predators as drivers of chemical defensive strategies in tenthredinid sawflies

Abstract

BackgroundMany insects are chemically defended against predatory vertebrates and invertebrates. Nevertheless, our understanding of the evolution and diversity of insect defenses remains limited, since most studies have focused on visual signaling of defenses against birds, thereby implicitly underestimating the impact of insectivorous insects. In the larvae of sawflies in the family Tenthredinidae (Hymenoptera), which feed on various plants and show diverse lifestyles, two distinct defensive strategies are found: easy bleeding of deterrent hemolymph, and emission of volatiles by ventral glands. Here, we used phylogenetic information to identify phylogenetic correlations among various ecological and defensive traits in order to estimate the relative importance of avian versus invertebrate predation.ResultsThe mapping of 12 ecological and defensive traits on phylogenetic trees inferred from DNA sequences reveals the discrete distribution of easy bleeding that occurs, among others, in the genus Athalia and the tribe Phymatocerini. By contrast, occurrence of ventral glands is restricted to the monophyletic subfamily Nematinae, which are never easy bleeders. Both strategies are especially effective towards insectivorous insects such as ants, while only Nematinae species are frequently brightly colored and truly gregarious. Among ten tests of phylogenetic correlation between traits, only a few are significant. None of these involves morphological traits enhancing visual signals, but easy bleeding is associated with the absence of defensive body movements and with toxins occurring in the host plant. Easy bleeding functions through a combination of attributes, which is corroborated by an independent contrasts test indicating a statistically significant negative correlation between species-level integument mechanical resistance and hemolymph feeding deterrence against ants.ConclusionsOur analyses evidence a repeated occurrence of easy bleeding, and no phylogenetic correlation including specific visual signals is significant. We conclude that the evolution of chemically-based defenses in tenthredinids may have been driven by invertebrate as much as by avian predation. The clear-cut visual signaling often encountered in the Nematinae would be linked to differential trends of habitat use by prey and predators. Further studies on (prey) insect groups should include visual signals and other traits, as well as several groups of natural enemies, to better interpret their relative significance and to refine our understanding of insect chemical defenses.

Morphological phylogenetics of the Tenthredinidae (Insecta : Hymenoptera)

“…Boevé et al (2013) assembled a dataset comprising 100+ tenthredinid taxa, but only a dozen outgroup taxa to explore the evolution of larval chemical defenses. Furthermore, many genera are represented by more than one terminal (Monophadnus by no less than nine), so in total 64 tenthredinid genera are included (Boevé et al 2013 : fig. 3).…”

“…Two studies have recently been published by Boevé et al (2013) and Malm and Nyman (2015), the first to include a (Fig. 1A-E); (1) distinctly converging ventrally, reaching medially of lateral margins of clypeus (Fig.…”

“…Schulmeister 2003a; Klopfstein et al 2013;Malm and Nyman 2015), sometimes not (Heraty et al 2011;Ronquist et al 2012). Significantly, all analyses except Boevé et al (2013) failed to retrieve the Tenthredinidae as monophyletic, even with a small taxon sample (e.g. Heraty et al 2011); usually, representatives of the genus Athalia fall outside the family.…”

Toxic Peptides Occur Frequently in Pergid and Argid Sawfly Larvae

“…[33]). The fact that previously only four species from two sawfly families were known to contain toxic peptides, was not representative of their actual occurrence in nature but a strong underestimation of the actual number of species containing such peptides.…”

The larva and prepupa of Eupareophora exarmata (Thomson, 1871) (Hymenoptera, Tenthredinidae)

“…Some additional COI sequences representing broad diversity of Tenthredinidae, Cimbicidae, Diprionidae, and Heptamelus , and which were at least 1000 bp long, were downloaded from NCBI nucleotide database (http://www.ncbi.nlm.nih.gov/nucleotide). The downloaded sequences were published previously by Prous et al 2011, Boevé et al 2013, Wei et al 2015a, Wei et al 2015b, Malm and Nyman 2014, and Song et al 2015. Only the downloaded COI sequence of Eupareophora parca was shorter than others (KF528474; 862 bp), because this was the only Eupareophora sequence publicly available.…”