Plumage manipulation alters associations between behaviour, physiology, the internal microbiome and fitness

Abstract

Signals often covary with physiological and behavioural traits to form an axis of integrated phenotypic variation associated with reproductive performance. This pattern of phenotypic integration could result from intrinsic between-individual differences that are causally related to signal production, physiology and behaviour. Alternatively, signal expression itself might generate feedback between physiology, behaviour and the experienced social environment, resulting in an integrated phenotype. We manipulated the plumage of female tree swallows, Tachycineta bicolor, to decouple the expression of a social signal from any pre-existing behavioural or physiological differences. We collected a time series of physiological samples, monitored nestbox visiting patterns with a sensor network and tracked reproductive performance. Relative to sham controls, dulled females' nests were visited more by conspecific females and less by males. Dulled females subsequently made fewer trips to other nestboxes and increased nestling provisioning. However, these changes in nestbox visiting patterns depended on both the focal female's pretreatment plumage and on the breeding stage. These differences resulted in an altered internal microbiome and glucose levels and, ultimately, dulled females produced more offspring. Moreover, dulled females produced larger clutches than control females in the year after the manipulation. Thus, signal variation alone – independent from any pre-existing differences – had a sustained causal effect on a suite of integrated traits. This finding suggests that dynamic feedback may play a role in coordinating an integrated signalling phenotype.