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Evolving communication systems in response to altered sensory environments

Periodic Reporting for period 4 - CITISENSE (Evolving communication systems in response to altered sensory environments)

Reporting period: 2023-07-01 to 2023-12-31

How animal communication systems evolve is a fundamental question in ecology and evolution and crucial for our understanding of adaptation and speciation. In the project CITISENSE we make use of the process of urbanisation to address how communication signals adapt to changes in the sensory environment. In the project we
focus on the impact of noise and light pollution on acoustic communication of a Neotropical species of frog, namely the tungara frog. Males of this species gather at night in small puddles that are formed after heavy rains and call to attract females. Their call does however also attract predatory bats and parasitic midges and their call behaviour therefore needs to be balanced between mate attraction and survival. Males can either alter their call behaviour directly, in response to immediate change to their environment, or indirectly, via selection, in which males that have the best match with their local sensory environment are better at attracting females or avoiding predators and parasites. Our central aim is to unravel the evolutionary and ecological processes that have led to divergence in sexual signalling behaviour between urban and forest populations of our focal frog species, addressing the following objectives:

1) How do senders adjust their acoustic signals to altered sensory environments?

2) How do signals evolve in response to direct (via sender) and indirect (via receivers) selection pressures?

3) What are the evolutionary consequences of signal divergence?

4) Can we predict how species adapt their signals to the sensory environment?

The outcome of our project has revealed that tungara frogs adjust their sexual signals directly via changes in the sensory environment, namely by calling louder when exposed to artificial light at night. These plastic responses are adaptive, as both predatory bats and females in search of mates were found to avoid males calling from light-polluted areas. Frogs from urban and forest populations also seem to have adjusted their physiology and behaviour indirectly in response to either experience or selection. Urban males were found to adjust their hormone levels in response to noise and light, whereas forest males seemed indifferent of their sensory environment. Males and female behaviour were found to differ depending on the sensory environment as well as their origin. Males that could acoustically interact with a rival were found to call most vigorously when tested under sensory conditions they were familiar with. Likewise, female preferences for a particular male were highest when tested under local sensory conditions. Lastly, we found male acoustic traits, such as call rate or complexity to have low heritability estimates, making it difficult to predict how sexual signals evolve in response to urban sensory conditions. The fact that male phenotypic expression appears to depend also on the phenotype of its nearest rival(s) makes it even harder to predict the outcome of any evolutionary process, despite the fact that we found the selective pressures on urban and forest frogs to differ starkly across all life-history phases. Our results have consequences for understanding how organisms adapt to human altered environments, as the interplay between direct plastic responses, combined with ecological interactions and indirect responses imposed by these interactions reduce our predictability.
In the first part of the project we have exposed urban and forest male frogs to urban and forest sensory conditions under both field- and lab-conditions, assessed selective pressures on calling males during field playbacks, setup a common garden breeding experiment and made a start with genomic analyses of urban and forest populations. In the second part of the project we assessed female preferences and rival responses in relation to urban sensory conditions and continued our genomic analyses to relate acoustic and morphological traits to genomic variation.

Major achievements are: 1) our results that calling males were found to directly respond to increased light pollution, both by increasing their call amplitude and testosterone levels and by decreasing their corticosterone levels. Furthermore, we found 2) females and predatory bats to avoid light-polluted areas, thereby explaining why urban males have adjusted their calling, as louder and possibly more complex calls should compensate for reduced mating opportunities, while not running the risk of attracting more predators. Finally, we found 3) that urban and forest populations have not diverged genetically, but have both undergone a period of population decline dated back several hundred years ago. This bottleneck event may have reduced the genetic diversity and thereby the evolutionary potential to respond to contemporary changes in the environment, such as urbanization and pollution.

These major achievements have been disseminated via scientific and public outreach events and by publishing in peer-reviewed journals.
We have developed and tested a state-of-the-art automated sender-receiver system that allows to run experimental evolution experiments under real field conditions. Combining heritability estimates of various acoustic traits our setup can let artificially-created acoustic phenotypes evolve in urban and forest sensory conditions by tracking their mating success and survival. We expect to publish the development of this novel tool open source and anticipate it to be useful in when studying complex mechanisms underlying adaptive signalling in response to environmental change.
Preparations of a field playback of frog sounds in Parque National Soberania, Panama.