Evolutionary Consequences of Artificial Light at Night

Overview

How does artificial light at night affect the evolution of circadian rhythms? Field and lab tests in an Australian field cricket system.

Life on Earth evolved under a regular oscillating cycle of daylight and darkness. However, recent urban sprawl and the associated increase in artificial light at night (ALAN) have disturbed these natural light cycles. ALAN is one of the most important urban stressors as no species has an evolutionary history of exposure. Despite known impacts on animal behaviour and physiology, we have little understanding of how ALAN might act as an agent of natural selection and driver of evolutionary change (Hopkins et al. 2018). This project will evaluate evolutionary consequences of ALAN by testing whether long-term exposure causes genetic changes in circadian rhythms for key fitness traits. Focusing on acoustic signalling and mating behaviour in a highly tractable field cricket study system (Figure 1), the student will combine fieldwork, behaviour assays, and genomics to test evolutionary impacts of ALAN and identify their genetic causes (Figure 2).

Methodology

This project uses fieldwork, behavioural experiments, and genetics to test how ALAN changes circadian rhythms in fitness traits and disset the genetic basis of those changes.

1. Quantify circadian behaviours in the wild for Australian cricket populations with different evolutionary histories of ALAN

(a) Perform bioacoustic recordings from replicate wild populations historically exposed (or not) to ALAN.
(b) Use a comparative approach taking advantage of the two sister species indicated shown in Figure 2.
(c) Analyse wild recordings to establish circadian patterns of in calling and ALAN levels in nature, and examine ecological and environmental factors that interact with them (Dominoni et al. 2013).

II. Using established experimental evolution populations and a laboratory-based high-throughput phenotyping system, test whether ALAN exposure selects for altered circadian rhythms in signalling, communication, and reproductive behaviour, and quantify fitness.

(a) Establish laboratory populations using offspring from generation 0 and generation 10 of an ongoing experimental evolution study.
(b) Test whether evolution under ALAN alters circadian phenotypes and the properties of the endogenous circadian clock (Dominoni et al. 2013).
(c) Using a time-shift experiment, test whether evolution under ALAN alters photosensitivity.
(d) In circadian rhythm experiments, record calling effort and song characteristics of males (who ordinarily sing to attract females on a circadian cycle), and perform open field tests to assess locomotion, mating behaviour, and reproductive fitness (Rayner et al. 2020).

III. Test and validate the genetic basis of evolved changes to circadian rhythms combining RNAseq and RNAi validations.

(a) Photosensitivity plasticity experiment: quantify and characterise gene expression changes activated by exposure to ALAN.
(b) Evolutionary genomics experiment: compare ALAN-induced expression profiles in experimentally evolved vs. control cricket populations (cf. Pascoal et al. 2018).
(c) Identify candidate circadian rhythm genes (contrast ALAN vs. no ALAN treatments) and test whether their expression has responded to selection (contrast evolved vs. control populations) (Zhang et al. 2021)
(d) Perform RNAi with phenotyping to functionally validate hits (Takekata et al. 2012).

Project Timeline

Year 1

Y1—Months 0-6: Kick-off meeting, PhD training, reading group, experimental design, fieldwork
Y1—Months 7-12: Analyse field data, training on laboratory behavioural assays, begin phenotyping study

Year 2

Y2—Months 0-6: Finish phenotyping study
Y2—Months 7-12: Perform wet lab work for gene expression study, secondment to Glasgow

Year 3

Y3—Months 0-6: Perform RNAi validations and analyse resequencing data
Y3—Months 7-12: Further analysis and manuscript and chapter writing, conference presentations

Year 3.5

Y4—Months 0-6: Submit thesis, work on papers

Training
& Skills

The studentship provides an opportunity to develop skills in cutting-edge research techniques consistent with NERC’s identified priority areas. For example, numeracy will be developed through engagement with bioinformatics in analysis of genomics data, and statistical and experimental design associated with the circadian rhythm and high-throughput phenotyping experiments. Exposure to best practice for fieldwork, lab behavioural work, and advanced genomic analyses will provide the student both breadth and depth of advanced skills for a career in the biosciences. The student will be encouraged and supported in identifying external training opportunities such as bioinformatics courses (e.g. through the St Andrews Bioinformatics Unit), and they will be encouraged to independently develop their own specialties and interests related to the project. Fieldwork training will be facilitated by the supervisors and postdoctoral researchers associated with their research groups, and the student will be embedded within a highly collegiate postgraduate environment at St Andrews that offers both formal and informal mentoring, access to seminars and more informal discussion groups. The student and supervisors will take advantage of the physical proximity of St Andrews and Glasgow to facilitate progress meetings and laboratory exchange visits, thus widening the student’s network of contacts, colleagues and collaborators, and a secondment to the University of Melbourne will provide valuable international context for the programme of research.

References & further reading

Dominoni DM, Helm B, Lehmann M, Dowse HB, Partecke J (2013) Clocks for the city: circadian differences between forest and city songbirds. Proceedings of the Royal Society of London B 280:20130593

Hopkins GR, Gaston KJ, Visser ME, Elgar MA, Jones TM (2018) Artificial light at night as a driver of evolution across urban-rural landscapes. Frontiers in Ecology and the Environment 16:472-479.

Pascoal S, Liu X, Fang Y, Paterson S, Ritchie MG, Rockliffe N, Zuk M, Bailey NW (2018) Increased socially mediated plasticity in gene expression accompanies rapid adaptive evolution. Ecology Letters 21:546-556.

Takekata H, Matsuura Y, Goto SG, Satoh A, Numnata H (2012) RNAi of the circadian clock gene period disrupts the circadian rhythm but not the circatidal rhythm in the mangrove cricket. Biology Letters 8:488-491.

Rayner JG, Schneider WT, Bailey NW (2020) Can behaviour impede evolution? Persistence of singing effort after morphological song loss in crickets. Biology Letters 16:20190931.

Zhang X, Rayner JG, Blaxter M, Bailey NW (2021) Rapid parallel adaptation despite gene flow in silent crickets. Nature Communications 12:50.

Further Information

Nathan W Bailey, School of Biology, University of St Andrews, Fife KY16 9TH

E: nwb3@st-andrews.ac.uk
T: +44 (0) 1334 463367

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