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

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.

求偶相关的装饰特征往往在不同物种间存在显著差异，这反映了配偶偏好功能与自然选择施加的约束之间的进化互作。因此，阐明驱动装饰特征多样化的进化动力学，一直是进化生物学领域长期存在的核心挑战。然而，跨物种比较截然不同的装饰特征，以及在同一物种内比较不同类别的装饰特征，对于理解性信号的多样化而言是一项极为艰巨的难题。本研究借助全新的研究方法与一套独特的自然历史数据集，以被广泛认为是由性选择驱动产生剧烈表型多样化的类群——极乐鸟（birds-of-paradise）——为研究对象，探究其装饰特征的进化模式。与达尔文和华莱士最初设想的装饰类型间权衡关系不同，我们发现跨模态（视觉/声学）信号之间存在正相关，这表明装饰性特征已整合为一个复合单元——即“求偶表型”。此外，鉴于系统鲁棒性——功能重叠与相互依存——能够促进进化创新这一观点已获得广泛的理论与实证支持，我们提出：极乐鸟之所以能够在求偶表型的性状空间中实现广泛辐射演化，正是源于我们在系统发育尺度上所观测到的求偶表型鲁棒性。我们认为，不同类群的求偶表型所具备的鲁棒性程度，能够为阐明性选择与自然选择对表型辐射的相对影响提供全新的研究视角。