Date Published: November 14, 2018
Publisher: Public Library of Science
Author(s): Lucy Magoolagan, Peter J. Mawby, Flora A. Whitehead, Stuart P. Sharp, Johan J. Bolhuis.
Song complexity and singing frequency in male birds are shaped by female choice; they signal male quality because song is costly to develop and produce. The timing of song learning and the development of the brain structures involved occur during a period when chicks are exposed to a number of potential stressors. The quality and quantity of song produced by adults may therefore reflect the level of stress experienced during early life, a theory known as the ‘developmental stress hypothesis’. We tested this hypothesis using song recordings and life-history data from an individually marked, long-term study population of wild dippers (Cinclus cinclus). The extent to which early life conditions predict adult song traits was investigated using natal brood size as a measure of sibling competition; the rate of provisioning by parents as a proxy for nutritional stress; and residuals of the linear regression between body mass and tarsus length as a measure of nestling condition. The syllable diversity in the songs of adult males was positively correlated with their body condition as nestlings, but there was no significant correlation with either provisioning rate or brood size. Provisioning rate did, however, predict song rate; males in relatively poor condition as nestlings or those raised in smaller broods which were fed more frequently by their parents sang at a higher rate in adulthood. These results support the developmental stress hypothesis and provide some of the first evidence from a wild bird of how the conditions experienced during early life impact adult song. Song traits may therefore provide females with information regarding both the current condition and developmental history of males.
In many bird species, males produce complex songs to defend their territories and attract a mate, and female choice is thought to be a major driver of the evolution of large song repertoires [1,2]. While several studies have shown that singing is not metabolically demanding [3,4], the development of the brain structures necessary for learning complex songs is thought to incur significant energetic costs . Furthermore, time spent learning and performing song is time taken away from other essential activities such as foraging  and increases exposure to predation . Females can therefore use song characteristics as measures of male quality [2,8,9], thereby gaining benefits such as proficient paternal care, territory defence, and ‘good genes’ for their offspring [2,10,11].
The conditions individuals experience during the early part of their lives have been shown to impact a range of life history variables and phenotypic traits in adulthood [37,38], including behavioural traits such as birdsong [19,39]. Our results demonstrate that song traits in male dippers are correlated with early life conditions and provide some of the first evidence from a wild bird population to support the developmental stress hypothesis [8,12]. This hypothesis proposes that song production and complexity may be compromised by exposure to stress during the nestling period as this is when the brain structures responsible develop [5,8,12]. Nestling body condition, which likely reflects nutritional stress, was positively correlated with syllable diversity, a proxy for repertoire size; this supports the findings of several experimental studies of captive birds in which the quality of nestling diet was manipulated [9,19,21]. The nestling phase is a critical period of growth for birds , and individuals in poorer condition at this time are presumably unable to invest as heavily in the development of the brain structures associated with song learning [5,41]. Such birds would be unable to learn and produce as many different syllables, hence syllable diversity may provide females with an honest signal of male quality [2,8,9]. Interestingly, versatility was found to vary with breeding stage but was not correlated with any of the measures of early life conditions. Solo and pre-breeding males sing with higher versatility than breeding males , suggesting that individuals are able to vary the use of their repertoires according to context even if the size of their repertoire is constrained by developmental stress. However, further research is needed to explore these ideas, in particular the analysis of songs recorded from the same males at different breeding stages.