Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise

Abstract

Ornaments used in courtship often vary wildly among species, reflecting the evolutionary interplay between mate preference functions and the constraints imposed by natural selection. Consequently, understanding the evolutionary dynamics responsible for ornament diversification has been a longstanding challenge in evolutionary biology. However, comparing radically different ornaments across species, as well as different classes of ornaments within species, is a profound challenge to understanding diversification of sexual signals. Using novel methods and a unique natural history dataset, we explore evolutionary patterns of ornament evolution in a group - the birds-of-paradise - exhibiting dramatic phenotypic diversification widely assumed to be driven by sexual selection. Rather than the tradeoff between ornament types originally envisioned by Darwin and Wallace, we found positive correlations among cross-modal (visual/acoustic) signals indicating functional integration of ornamental traits into a composite unit - the courtship phenotype. Furthermore, given the broad theoretical and empirical support for the idea that systemic robustness - functional overlap and interdependency - promotes evolutionary innovation, we posit that birds-of-paradise have radiated extensively through ornamental phenotype space as a consequence of the robustness in the courtship phenotype that we document at a phylogenetic scale. We suggest that the degree of robustness in courtship phenotypes among taxa can provide new insights into the relative influence of sexual and natural selection on phenotypic radiations.Author SummaryAnimals frequently vary widely in ornamentation, even among closely related species. Understanding the patterns that underlie this variation is a significant challenge, requiring comparisons among drastically different traits - like comparing apples to oranges. Here, we use novel analytical approaches to quantify variation in ornamental diversity and richness across the wildly divergent birds-of-paradise, a textbook example of how sexual selection can profoundly shape organismal phenotypes. We find that color and acoustic complexity, along with behavior and acoustic complexity, are positively correlated across evolutionary time-scales. Positive covariation among ornament classes suggests that selection is acting on correlated suites of traits - a composite courtship phenotype - and that this integration may be partially responsible for the extreme variation we see in birds-of-paradise.

Habitat structure drives the evolution of aerial displays in birds

“…This study provides an emblematic example of the power of sensory drive in predicting the direction of evolution of otherwise highly unpredictable sexual traits. Also, by revisiting a pattern predicted for decades, but never tested before – that ‘high‐flying […] displays are most characteristic of birds of the open country' (Armstrong, , p. 257) – we offer a contribution to the ongoing efforts to disentangle the evolutionary drivers of complex avian gestural displays (Ligon et al, ; Miles et al, ; Miles & Fuxjager, , ; Soma & Garamszegi, ). Such efforts had shown that biogeographical, phenotypic, environmental and life‐history factors all influence sexual display evolution in passerines at the family level.…”

“…While these case studies belong in the sensory drive realm (Cummings & Endler, ) and may be indicative of an evolutionary link between habitat and display, a phylogenetic comparative approach is the most appropriate way to uncover such a link (Harvey & Pagel, ). Phylogenetic comparative evidence accumulated to date suggests that (micro)habitat may influence aspects of avian and saurian displays such as repertoire size (Ligon et al, ; Miles & Fuxjager, ; Ord, Blumstein, & Evans, ) and repetition pattern (Ord & Martins, ; but see Perez et al, ). However, the role of habitat as a force that determines which elements of display repertoires should evolve – rather than how many elements – has yet to be demonstrated.…”

“…Recent phylogenetic comparative analyses have shed light on the evolution of passerine displays at the family level, with multiple factors influencing their evolution. For instance, latitude (Icteridae; Miles, Cheng, & Fuxjager, ), display height (Paradisaeidae; Ligon et al, ; Miles & Fuxjager, ), body size and brood parasitism (Estrildidae; Soma & Garamszegi, ) all have been found to influence some aspect of gestural displays in passerine families. Such diversity of clade‐specific evolutionary forces might lead one to believe that the structure of passerine sexual displays is all but unpredictable.…”

“…This analysis constitutes, both taxonomically and geographically, the most comprehensive test of sensory drive to date, as far as we are aware. By testing our hypothesis at the order level, we aim to uncover an overarching factor that might influence the evolution of passerine displays as a whole, in addition to the idiosyncratic forces that have been found to act within specific clades (Ligon et al, ; Miles et al, ; Miles & Fuxjager, ; Soma & Garamszegi, ). This would represent a significant step towards unravelling the evolution of gestural displays across the animal kingdom.…”

Niche partitioning as a selective pressure for the evolution of theDrosophilanervous system

“…The utilization of forest openings are well studied in avian biology, where males often construct and clear elaborate arenas to perform intricate visual displays for females (i.e. the genus Parotia or six-plumed birds of paradise) [38]. However, to our knowledge, the visual capabilities across vertebrate animal species has never been compared to examine evolutionary investments in the nervous system that correlate with visual courtship.…”