Urban birdsongs: higher minimum song frequency of an urban colonist persists in a common garden experiment

Abstract

Environmental changes caused by urbanization and noise pollution can have profound effects on acoustic communication. Many organisms use higher sound frequencies in urban environments with low-frequency noise, but the developmental and evolutionary mechanisms underlying these shifts are less clear. We used a common garden experiment to ask whether changes in minimum song frequency observed 30 years after a songbird colonized an urban environment are a consequence of behavioral flexibility or canalized changes that occur early in development. We captured male juvenile dark-eyed juncos (Junco hyemalis thurberi) from two recently diverged populations (urban and mountain) soon after they reached independence (aged 25-40 days), raised them in identical indoor aviaries, and studied their songs at an age of three years. We found that the large population difference in minimum frequency observed in the field persisted undiminished in the common garden despite the absence of noise. We also found some song sharing between the common garden and natal field populations, indicating that early song memorization before capture could contribute to the persistent song differences in adulthood. These results are the first to show that frequency shifts in urban birdsong are maintained in the absence of noise by genetic evolution and/or early life experiences..

Rapid evolutionary divergence of a songbird population following recent colonization of an urban area

“…KCNQ4 has also been found to be involved in highfrequency hearing in echolocating bats (Eriksson & Wiktelius, 2011). A significantly higher minimum frequency in the vocal signalling of the UCSD juncos with respect to natural habitats has been previously reported (Cardoso & Atwell, 2010Reichard et al, 2020;Slabbekoorn et al, 2007), arguably as a strategy to reduce masking by anthropogenic low-frequency noise. Importantly, both genes showed high levels of divergence with respect to pinosus, as evidenced by F ST values.…”

“…This population belongs to the subspecies thurberi and inhabits elevations above 1500 m, a montane habitat with a more extreme temperature regime than the milder Mediterranean climate of the UCSD campus (Unitt, 1984; Yeh & Price, 2004). Studies on UCSD juncos published to date have focused on the evolution of social signalling traits during colonization of a novel environment (Price, Yeh & Harr, 2008; Reichard et al, 2020; Yeh, 2004); the role of plasticity in population persistence during the early stages of colonization (Price et al, 2008; Yeh & Price, 2004); patterns of morphological and genetic variation in comparison with other California populations, using both microsatellites (Rasner et al, 2004) and MHC (major histocompatibility complex) loci (Whittaker et al, 2012); and hormonal changes underlying shifts in phenotypic and life‐history traits during adjustments to urban environments (Atwell et al, 2012, 2014; Fudickar et al, 2017). Based on phenotypes of overwintering nonresident birds and proximity to potential sources, Yeh (2004) proposed that the population of UCSD juncos had probably originated from the thurberi population in the nearby mountains as a result of overwintering birds remaining to breed.…”

Rapid evolutionary divergence of a songbird population following recent colonization of an anthropogenic habitat

“…KCNQ4 has also been found to be involved in high-frequency hearing in echolocating bats (Eriksson & Wiktelius 2011). A significantly higher minimum frequency in the vocal signaling of the UCSD juncos with respect to natural habitats have been previously reported (Cardoso & Atwell 2010Reichard et al 2020;Slabbekoorn et al 2007), arguably as a strategy to reduce masking by anthropogenic low-frequency noise. Importantly, both genes showed high levels of divergence with respect to pinosus , as evidenced by F ST values.…”

“…This population belongs to the subspecies thurberi and inhabits elevations above 1,500 m, a montane habitat with a more extreme temperature regime than the milder Mediterranean climate of the UCSD campus (Unitt 1984;Yeh & Price 2004). Studies published to date have focused on the evolution of social signaling traits during colonization of a novel environment (Priceet al 2008;Reichard et al 2020;Yeh 2004); the role of plasticity in population persistence during the early stages of colonization (Price et al 2008;Yeh & Price 2004); patterns of morphological and genetic variation in comparison with other California populations, using both microsatellites (Rasner et al 2004) and MHC loci (Whittaker et al 2012) and hormonal changes underlying shifts in phenotypic and life-history traits during adjustments to urban environments Atwell et al 2014;Fudickar et al 2017). Based on phenotypes of over-wintering non-resident birds and proximity to potential sources, Yeh (2004) proposed that the population of UCSD juncos had likely originated from the thurberi population in the nearby mountains as a result of overwintering birds remaining to breed.…”

Constant Resting Frequency and Auditory Midbrain Neuronal Frequency Analysis of Hipposideros pratti in Background White Noise

“…However, the observed adjustments in the frequency domain are quite variable, depending on both the frequency spectrum of the noise and the species studied. For example, low-frequency background noise usually increases the minimum frequency of the acoustic signals in birds ( Reichard et al, 2020 ). Water flow noise also increases the call frequency in frogs ( Shen and Xu, 2016 ), even without the Lombard effect ( Zhao et al, 2018 ).…”