Periodic Reporting for period 3 - SongNeuroGen (Species discrimination in birds: A behavioural-neurogenomics approach to auditory learning)
Reporting period: 2022-11-01 to 2024-04-30
Many species of animals use mating traits, such as songs, pheromones, and other signals, to find mates. Thus, producing and preferring appropriate traits is essential for successful reproduction. Acquiring correct traits is a major challenge when they are learned, since this risks mistakenly learning from co-occurring species. Cross-species learning, in turn, can reduce the individual’s chances of mating and erode species differences in mating traits. We know surprisingly little about how cross-species learning is avoided. The overall problem addressed in my project is how and why juvenile songbirds avoid learning the songs of other species.
How individuals avoid mating with members of other species is of theoretical and practical importance. From a theoretical perspective, mating between species can be costly to the affected individuals, leading to evolutionary responses, and, if it is widespread, can lead to the extinction of one of the species. From a practical perspective, human-induced changes to geographic ranges are driving novel instances of contact between formerly isolated species. An understanding of how animals avoid mating with individuals from other species will provide important insights into the outcome of such range shifts.
My project has three main aims, focused on understanding the causes and consequences of early song discrimination in a widespread songbird species, the pied flycatcher. AIM 1: Songbirds can recognize their own species’ songs from a very young age, an ability that influences what songs they are likely to learn and prefer as adults. The first aim of the project is to determine why and how this ability has evolved using a large-scale experiment at multiple populations throughout the European range of the pied flycatcher. This experiment measures the responses of nestling birds to playbacks of songs to test two main hypotheses for the evolution of early song discrimination. AIM 2: The second aim of the project progresses beyond the earliest stages of learning to determine the key periods throughout an individual’s development when they are sensitive to song exposure. Akin to language learning in human children, songbirds are particularly sensitive during certain life stages early in life. Determining when these stages occur will provide insights into how likely individuals are to learn the songs of their own versus other species and, since song learning in birds is our principal model system for understanding language learning in humans, these insights will have broad impacts. AIM 3: The third aim of the project is to determine how species differences in song perception arise in the brain. The songbird auditory system develops to be specifically responsive to the types of sounds produced by members of the same species, making them particularly likely to memorize the songs of their own species. However, we know very little about how and when the auditory system develops species-specific differences. To address this gap, we will use gene expression to assess auditory responses of juvenile pied flycatchers and closely related collared flycatchers to the songs of their own and other species to determine the key brain regions and genes driving species differences.
How individuals avoid mating with members of other species is of theoretical and practical importance. From a theoretical perspective, mating between species can be costly to the affected individuals, leading to evolutionary responses, and, if it is widespread, can lead to the extinction of one of the species. From a practical perspective, human-induced changes to geographic ranges are driving novel instances of contact between formerly isolated species. An understanding of how animals avoid mating with individuals from other species will provide important insights into the outcome of such range shifts.
My project has three main aims, focused on understanding the causes and consequences of early song discrimination in a widespread songbird species, the pied flycatcher. AIM 1: Songbirds can recognize their own species’ songs from a very young age, an ability that influences what songs they are likely to learn and prefer as adults. The first aim of the project is to determine why and how this ability has evolved using a large-scale experiment at multiple populations throughout the European range of the pied flycatcher. This experiment measures the responses of nestling birds to playbacks of songs to test two main hypotheses for the evolution of early song discrimination. AIM 2: The second aim of the project progresses beyond the earliest stages of learning to determine the key periods throughout an individual’s development when they are sensitive to song exposure. Akin to language learning in human children, songbirds are particularly sensitive during certain life stages early in life. Determining when these stages occur will provide insights into how likely individuals are to learn the songs of their own versus other species and, since song learning in birds is our principal model system for understanding language learning in humans, these insights will have broad impacts. AIM 3: The third aim of the project is to determine how species differences in song perception arise in the brain. The songbird auditory system develops to be specifically responsive to the types of sounds produced by members of the same species, making them particularly likely to memorize the songs of their own species. However, we know very little about how and when the auditory system develops species-specific differences. To address this gap, we will use gene expression to assess auditory responses of juvenile pied flycatchers and closely related collared flycatchers to the songs of their own and other species to determine the key brain regions and genes driving species differences.
AIM 1: From 2020-2022, we have conducted a large-scale, song playback experiment across breeding populations of pied flycatchers throughout Europe. I organized a collaboration involving researchers studying 7 European populations. In total, we performed nearly 400 playback experiments, assessed the behavioral responses of nearly 2000 individual nestling birds to songs, and conducted over 5000 behavioral observations. The results of these experiments definitively demonstrate that nestling songbirds have heightened behavioral responses to songs typical of their local population.
AIM 2: Over two years, we brought 27 juvenile pied flycatchers into captivity and reared them over winter, controlling their exposure to songs and recording the songs they produce throughout development. We are currently relating song exposure to song production over different life stages to understand when juveniles are particularly sensitive to hearing songs.
AIM 3: I have performed song playbacks to stimulate gene expression in the auditory systems of nestling pied and collared flycatchers. One group of each species heard their own species’ songs and a second group heard the songs of the other species. We are currently conducting RNA sequencing of three important auditory brain regions. The RNA sequencing results are expected by the end of the summer 2022.
AIM 2: Over two years, we brought 27 juvenile pied flycatchers into captivity and reared them over winter, controlling their exposure to songs and recording the songs they produce throughout development. We are currently relating song exposure to song production over different life stages to understand when juveniles are particularly sensitive to hearing songs.
AIM 3: I have performed song playbacks to stimulate gene expression in the auditory systems of nestling pied and collared flycatchers. One group of each species heard their own species’ songs and a second group heard the songs of the other species. We are currently conducting RNA sequencing of three important auditory brain regions. The RNA sequencing results are expected by the end of the summer 2022.
The results of AIM 1 will change our understanding of the interaction between cultural and genetic evolution, since juvenile birds are tuned at an extremely young age to the songs of their local population and independently of prior song exposure. Population-specific songs, called dialects, arise due to social transmission of songs, which leads to ongoing song evolution within and across populations. Early perceptual tuning to local song forms implies a remarkable co-evolution between song variants and the underlying auditory brain regions. For AIM 2, captive rearing of pied flycatchers has been performed previously, but never with the aim of understanding song development and almost nothing is known about how and when experience early in life impacts adult songs. The results of these experiments will provide critical insights into the limits of song learning across species, an important model system for memory formation more generally. Finally, AIM 3 will establish how genetic differences between species influence species-specific responses. Over 4500 species of songbirds, over half of all bird species, are thought to learn their songs, meaning that these results will provide novel insights into the emergence and maintenance of species differences in an incredibly species-rich group.