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 fi refl y fl ash 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 fi ghting behaviours. Thus, contestants signal their opponents to avoid the cost of fi ghting. Our study provides experimental evidence for the origins of a complex communication signal, through the process of ritualization.
In seeking hypotheses to explain the evolutionary origin of vibratory signalling, we performed a survey of literature that included preliminary morphological9,10 or behavioural11,12 descriptions of drepanid caterpillars. We observed a range of morphologies and behaviours associated with the anal segment across species. Most interestingly, it was noted that many species lacked anal prolegs, whereas others possessed a pair of fully functional prolegs. Prolegs are unsegmented legs located on abdominal segments 3–6 and 10 in most caterpillars13,14 and are used for locomotion. This observation of morphological variation in the anal segment led to our hypothesis that the ritualized anal scraping signal seen in D. arcuata was co-opted from crawling. Specific predictions that would support this hypothesis include the following: (1) structures and movements in species that use their anal segment for crawling will be homologous to the modified forms found in anal scraping species; (2) the possession of anal prolegs will be the basal condition when mapped onto a phylogeny; and (3) anal scraping signals will possess modifications characteristic of ritualized signals when compared with cues associated with crawling. To test these predictions, we studied the morphological, behavioural and associated vibratory characteristics of the anal segment in distantly related species. We then constructed a molecular phylogeny onto which walking and talking with the anal segment were mapped.