A systems approach to animal communication

Abstract

Why animal communication displays are so complex and how they have evolved are active foci of research with a long and rich history. Progress towards an evolutionary analysis of signal complexity, however, has been constrained by a lack of hypotheses to explain similarities and/or differences in signalling systems across taxa. To address this, we advocate incorporating a systems approach into studies of animal communication--an approach that includes comprehensive experimental designs and data collection in combination with the implementation of systems concepts and tools. A systems approach evaluates overall display architecture, including how components interact to alter function, and how function varies in different states of the system. We provide a brief overview of the current state of the field, including a focus on select studies that highlight the dynamic nature of animal signalling. We then introduce core concepts from systems biology (redundancy, degeneracy, pluripotentiality, and modularity) and discuss their relationships with system properties (e.g. robustness, flexibility, evolvability). We translate systems concepts into an animal communication framework and accentuate their utility through a case study. Finally, we demonstrate how consideration of the system-level organization of animal communication poses new practical research questions that will aid our understanding of how and why animal displays are so complex.

Keywords: degeneracy; evolvability; modularity; multimodal; redundancy; robustness.

Figure 1.

A heuristic example of the concepts and potential implementation of systems terminology based upon a recent study of animal communication [32]. Male barn swallows (centre), Hirundo rustica erythrogaster, communicate with conspecific males (left; intrasexual) and females (right; intersexual) using multimodal/multicomponent displays that encompass acoustic song (top; blue lines) and visual colour patches (red circle; red lines). Coloured lines with arrows indicate receivers (males and females) that respond to specific display components. Redundancy is seen in the repeated notes of the male's song. Degeneracy is seen in that two distinct display components (song and breast feather reflectance) overlap in function: territoriality (not highlighted) and female attraction [32]. Pluripotentiality is demonstrated by the dual function of song in both intra- and intersexual communication, and the similar dual function of breast feather colour (not highlighted) [32].

Figure 2.

Building on the geometric framework of Smith & Evans [83], a heuristic graphical representation of a response surface highlighting interactions between vibratory and visual signal components of the courtship display of the wolf spider, Schizocosa crassipes [37]. Empirical data demonstrate that females respond to variation in brush size only in the presence, versus absence, of vibratory signalling [37]. This geometric visualization bears similarity to the multidimensional response surface methodology [e.g. 1], but rather than linking fitness to trait values to measure evolutionary responses to selection, here we plot behavioural responses as a function of trait (signal) values [84].

Figure 3.

Signalling phenotype networks adapted from Wilkins et al. [32], illustrating the traits predicting (a) within-nest paternity and (b) internest distance in the barn swallow, Hirundo rustica erythrogaster. Triangles, colour variables; squares, morphological traits; and circles, song components. Lines connecting shapes represent Spearman's correlations and shape colours are graded by importance of rotated principal components (for details, see [32]). The best predictor of paternity (a surrogate for mate choice) was a factor with high loadings for wing length (RWL), tail feather length (TS), and per cent complex syllables (%T). The best predictor of internest distance (a surrogate for competition) was a factor with high loadings for the darkness of undertail contour feathers (VChr) and syllable repertoire size (Rep). The factor loading highly for a triad of song traits—warble tempo (WTmp), trill tempo (RTmp), and trill length (RL)—was the only strong predictor of both intra- and intersexual selection measures.