The evolutionary origins of ritualized acoustic signals in caterpillars

Abstract

Animal communication signals can be highly elaborate, and researchers have long sought explanations for their evolutionary origins. For example, how did signals such as the tail-fan display of a peacock, a firefly flash or a wolf howl evolve? Animal communication theory holds that many signals evolved from non-signalling behaviours through the process of ritualization. Empirical evidence for ritualization is limited, as it is necessary to examine living relatives with varying degrees of signal evolution within a phylogenetic framework. We examine the origins of vibratory territorial signals in caterpillars using comparative and molecular phylogenetic methods. We show that a highly ritualized vibratory signal--anal scraping--originated from a locomotory behaviour--walking. Furthermore, comparative behavioural analysis supports the hypothesis that ritualized vibratory signals derive from physical fighting behaviours. Thus, contestants signal their opponents to avoid the cost of fighting. Our study provides experimental evidence for the origins of a complex communication signal, through the process of ritualization.

Figure 1. Vibratory communication signals in the masked birch caterpillar, Drepana arcuata.

(a) Caterpillars build and occupy silken leaf shelters (scale bar, 2.5 mm). (b) When approached by an intruder, the resident produces three types of vibratory signals: anal scraping (green) is performed by pulling the abdominal segment forward while at the same time scratching a sclerotized 'oar' against the leaf surface; mandible drumming (blue) and mandible scraping (orange) are produced by rapidly hitting and laterally scraping opened mandibles against the leaf surface, respectively.

Figure 2. Structure and function of the terminal abdominal segment in a representative species that possesses anal prolegs (Tethea or) and one that lacks anal prolegs but possesses anal oars (Drepana arcuata).

(a, d) Schematic of T. or and D. arcuata illustrating the overall body plan of each species. (b, f) (top panels) Schematic of identified setae on the terminal segment in T. or and D. arcuata; labels refer to names of setae according to Stehr (D=dorsal, SD=subdorsal, V=ventral, SV=subventral, L=lateral, PP=posterior proctor); (bottom panels) scanning electron micrographs showing posterior views of the right anal proleg in T. or and the homologous region with stridulatory oar in D. arcuata. PP1 setae are marked with arrows, and colours correspond to setae labelled in the top panel. Scale bars, 200 μm (T. or) and 100 μm (D. arcuata). (c, e) Video frames of the terminal abdominal segments in each species, illustrating one complete crawling cycle in T. or and one complete anal scraping movement in D. arcuata. Arrows show the progression of movement. Scale bars, 3 mm (T. or) and 1.5 mm (D. arcuata).

Figure 3. Bayesian tree showing ancestral and derived states of the terminal (anal) segment.

Anal prolegs present (orange), absent (green); anal oars present (red), absent (blue). Posterior probabilities are shown above branches. Pie charts are maximum likelihood probabilities of ancestral states at four selected nodes. The common ancestor of Drepaninae and Thyatirinae (Node B) had a 99.9% probability of possessing anal prolegs. Anal oars were probably gained at Node C and were subsequently lost multiple times.

Figure 4. Representative territorial encounters in a species that do not signal with their abdomen (Tethea or, left panel), and one that uses abdominal 'oars' to signal (Drepana arcuata, right panel).

(a) Video frames illustrating a typical encounter between a resident and intruder, whereby the intruder enters the leaf shelter (1), the resident then approaches the intruder while hitting, pushing or mandible scraping (T. or; scale bar, 9 mm), or uses ritualized signals (D. arcuata; scale bar, 7 mm) (2) and the intruder turns to leave (3). (b) Laser vibrometer traces of the cues and signals on the leaf during such an encounter. Numbers correspond to frames in a. Relative amplitudes are equal between species. The box encloses part of the trace that is enlarged in the coloured segment below, which shows the vibrations generated by the resident when the two individuals are close together. Colours correspond to cues or signals in c. (c) Transition diagrams showing the probability of one type of behaviour following another. Asterisks denote significantly more probable transitions (D. arcuata, n=13; T. or, n=7; P<0.05). MS, mandible scraping; AS, anal scraping; MD, mandible drumming.