Epigenetics of local adaptation

Overview

Climate change poses a profound threat to biodiversity. However, this threat can be mitigated through a better understanding of how organisms adapt to changes in their local environmental conditions. One understudied route to such rapid adaptation is through epigenetic modifications affecting the expression of genes adjusting an individual organism’s traits to its prevailing environment1,2. This project uses a “natural laboratory” of wild field crickets in the mountains of northern Spain to investigate such epigenetic mechanisms of local adaptation. The student will test how DNA methylation and non-coding RNA control how crickets cope with manipulated altitudinal environmental variation. The project integrates these experimental approaches with quantitative genetic approaches to determine whether intergenerational epigenetic effects can facilitate rapid adaptation to environmental change.

This studentship will capitalise on an existing long-term study of 10 natural populations of field crickets in the mountains of northern Spain (see www.wildcrickets.org). We have established methods for quantifying behaviour, performance, and relative fitness using a genetically based pedigree and 24/7 tracing and performance-monitoring of individuals through a novel network of 150 video-cameras. The student will join the WildCrickets team to experimentally translocate crickets between altitudes, addressing two main objectives:

1. MECHANISM: 1a. Determine the epigenetic modes underpinning physiological and behavioural adjustments to altitude, 1b. test their intergenerational effects, and 1c. validate their causal roles in physiology and behaviour using RNA-interference.
2. EVOLUTION: 2a. Estimating the strength of selection on epigenetic markers and their additive genetic variation in the wild. 2b. Test if epigenetics underpin indirect genetic effects.

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Image Captions

Fig. 1 High altitude meadow in Asturias, Spain
Fig 2. Tagged adults outside burrow

Methodology

This project combines fieldwork in Spain, experimental environmental manipulations, epigenetic manipulations, and quantitative genetic approaches to test the role of epigenetics in local adaptation to altitude. We recently found evidence for genetic isolation among 10 populations of the cricket Gryllus campestris distributed across high and low altitudes in the mountains of northern Spain. At high altitudes, the adult season is much shorter, and this affects key life-history traits such as the date of adult emergence and adult lifespan.

1. MECHANISM: The student will breed crickets from each altitude for a quantitative genetic analysis. F1 eggs will be reciprocally translocated between the 2 altitudes (a procedure we have successfully piloted). Individuals will be sampled longitudinally in early-life and adult developmental stages and bisulfite sequencing will be used to identify potential candidate genes related to epigenetic altitude adaptation, as well as noncoding RNAs (lncRNA, miRNA, piRNA, siRNA)3. Using this approach, the epigenetic changes associated with the physiological and behavioural responses to altitudinal conditions will be investigated (obj. 1a). The experiment will be repeated for a second season to estimate the non-genetic, intergenerational epigenetic effects (obj. 1b). To validate epigenetic mechanisms this identifies, the causal role of candidate genes and RNAs can be investigated with RNA-interference through injections, a method already developed in field crickets4 (obj. 1c).

2. EVOLUTION: A complementary project linking the mechanistic epigenetic basis of local adaptation to altitude to the evolutionary dynamics of local adaptation will run concurrently. The aim is to understand how epigenetic variants are selected in the wild. Using data from the above quantitative genetic and epigenetic experiments, we will estimate additive genetic variation for epi-marking itself (obj. 2a) and by resequencing candidate genes whose epigenetic modifications are linked to altitude adaptation and a control set of housekeeping genes, we will use a population genomic approach to interrogate patterns of selection that have operated upon those genes in different populations. The aim is to test whether candidate genes subject to epigenetic modification show heightened signatures of selection in different altitudes. Lastly, the student will test the presence of indirect genetic effects and the extent to which they could arise through epigenetic modifications altering gene expression (obj. 2b).

Project Timeline

Year 1

Y1 – Months 1-6: Core skills training. The student will join the WildCrickets field work in Spain to setup the breeding design for obtaining the F1 generation of nymphs developing at manipulated altitudinal conditions.
Y1 – Months 7-12: Epigenetics pilot (evaluate overall DNA-methylation and noncoding RNA landscapes).

Year 2

Y2 – Months 1-6: Field work to collect samples and to continue the breeding design for obtaining the F2 generation that will be used to investigate intergeneration epigenetic effects. The student will also conduct the RNA-interference experiment by injecting eggs.
Y2 – Months 7-12: Secondment to St Andrews to conduct a candidate gene study. The student will also initiate a quantitative genetic study as part of their core training using life-history data that is already available. In the meantime, samples for epigenetic markers will be processed in the Glasgow Polyomics centre.

Year 3

Y3 – Months 1-6: Analyses to investigate modes of epigenetic inheritance using the F1 and F2 generations. Quantitative genetic analyses for investigating indirect genetic effects.
Y3 – Months 7-12: Finalising data analyses. Chapter and manuscript writing. Conference presentations.

Year 3.5

Y4 – Months 1-6: Submit thesis and work on papers.

Training
& Skills

The studentship provides an opportunity to receive training from a diverse team of internationally recognized experts to develop skills in cutting-edge research techniques consistent with NERC’s mission. For example, numeracy will be developed through engagement with statistical quantitative genetics analyses and we will also work with the student to develop new theory to extend the quantitative genetic framework to include epigenetic modes of heritable biological variation. Best practice for lab technique plus proficiency in quantitative and epigenomic analyses will equip the student with skills that can be applied in other settings or systems during their future career. We will encourage the student to identify relevant external workshops in molecular evolution and local adaptation and enable them to pursue sub-specialities of their own interest. Fieldwork training will be facilitated by the PIs, and the student will be embedded within a highly collegiate postgraduate environment at Glasgow that offers both formal and informal mentoring, access to seminars and more informal discussion groups. The student and supervisors will take advantage of the DTP scheme to arrange for a secondment to St Andrews and visits to Exeter, to facilitate knowledge exchange through institutional seminars or workshops, thus widening the network of potential contacts, colleagues and collaborators for the student.

The project will benefit from matured genomic resources including an annotated genome, gene expression data, a genome browser (www.chirpbase.org), and bioinformatic pipelines in closely-related cricket species, and includes a secondment to co-supervisor Bailey’s lab at the University of St Andrews. The Polyomics centre in Glasgow has established pipelines for epigenomic analyses. We will collaborate intensively with Paul Shiels (Glasgow), an expert on epigenomics.

References & further reading

1. Suzuki, M. M. & Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9, 465–476 (2008).
2. Jablonka, E. & Lamb, M. J. The Changing Concept of Epigenetics. Ann Ny Acad Sci 981, 82–96 (2002).
3. Villagra, C. & Frías-Lasserre, D. Epigenetic Molecular Mechanisms in Insects. Neotrop Entomol 1–28 (2020) doi:10.1007/s13744-020-00777-8.
4. Barry, S. K. et al. Injecting Gryllus bimaculatus Eggs. J Vis Exp (2019) doi:10.3791/59726.

WildCrickets: www.wildcrickets.org.

Further reading
5. Boonekamp, J. J., Mulder, E. & Verhulst, S. Canalisation in the wild: effects of developmental conditions on physiological traits are inversely linked to their association with fitness. Ecology Letters 67, 1 (2018).
6. Boonekamp, J.J., Rodriguez-Munoz, R., Hopwood, P., Zuidersma, E., Mulder, E., Wilson, A., Verhulst, S. & Tregenza, T. (2020) Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets. bioRxiv.
7. Rodríguez‐Muñoz, R., Boonekamp, J.J., Liu, X.P., Skicko, I., Pedersen, S.H., Fisher, D., Hopwood, P. & Tregenza, T. (2019) Comparing individual and population measures of senescence across 10 years in a wild insect population. Evolution 73 (2), 293-302.

Further Information

For IAPETUS2 applications to the University of Glasgow please use the dedicated application portal: https://www.gla.ac.uk/scholarshipApp (you will still need to submit your administrative details to the IAPETUS2 website as well).

Jelle Boonekamp, College of Medical, Veterinary & Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ. Email: jelle.boonekamp@glasgow.ac.uk

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