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Predicting adaptability to environmental change: do animals inherit information about their environment from their parents?

Dr Elizabeth Duncan (SOB), Dr Christopher Hassall (SoB), Dr Steven Sait (SoB)

Contact email: e.j.duncan@leeds.ac.uk

All animals live in variable environments where conditions can change rapidly. In cases where environmental change is predictable, such as seasonal changes in temperature and precipitation, animals are adapted to cope with this variation. However, unpredictable and abrupt changes in the environment, or those moving beyond the boundaries previously experienced, can have profound effects on species, either facilitating rapid phenotypic change as animals become adapted but also, perhaps more importantly, increasing extinction risk for at-risk species that fail to adapt or move.  Understanding how and why some animals become adapted to rapid changes in the environment and some don’t, therefore facing risk of extinction, is a key question in ecology, evolution and conservation biology.

The responses of a population to environmental change are thought to be associated with genetic diversity in the population.  Higher levels of genetic diversity provide more variation in phenotypes, some of which may be better adapted to the new or fluctuating environmental conditions.  But we now know that that variation in ecologically relevant traits can occur through epigenetic mechanisms, such as DNA methylation, in the absence of genetic variation.  These epigenetic marks don’t alter the DNA sequence permanently, and the effects may be transient, lasting for a single generation, or remarkably may be passed between generations.  Transgenerational inheritance of these marks would allow for adaptive changes to the genome that are longer lasting but not permanent.  This kind of transient variation may be advantageous in fluctuating environments where permanent genetic adaptation may, in the long-term, be maladaptive as environments continue to change or fluctuate [1]

The amount of epigenetic variation (such as DNA methylation) in a population and the potential for this information to be passed between generations may predict species resilience to fluctuating environments.  This mechanism would facilitate rapid adaptation in response to environmental change in some species, while other species may have low levels of epigenetic variation or may not be able to pass that information to the next generation, leaving them susceptible to extinction.  In this project you will test this hypothesis using a combination of field and laboratory based experiments focussed on invertebrate species.

Invertebrates (and insects in particular) are the most abundant and species rich group of animals on the planet.  They have critical roles in all terrestrial and many aquatic ecosystems.  Invertebrates are critical for ecological functions including pollination, pest control, resource processing, and act as a food source for other animals [2]. Ambient temperature is particularly important for ectotherms such as invertebrate and many invertebrate species are potentially highly vulnerable to the impacts of climate change and have a high risk of extinction [3].  Invertebrates are ideal animals to test our hypothesis as they have a short generation time, have conserved epigenetic machinery, and are responsive to environmental variation.  In this project we will focus on invertebrates that are tractable in the laboratory setting as well as being available for study in their natural habitat.

We have identified a number of invertebrate species where environmental information may be encoded epigenetically (e.g. the pest moth Plodia interpunctella [4], its biocontrol agent parasitoid wasp Ventaria canescens [5], the keystone shrimp Gammarus pulex, and the hoverfly Episyrphus balteatus). The first stage of this project will be to determine whether these species have increased epigenetic variation in fluctuating versus stable environments and whether this variation is passed from parent to offspring. To do this we will use cutting edge techniques to measure DNA methylation (such as RRBS [6,7] or epiRAD-seq [8]).  The second stage of this project will be to determine whether these species have high levels of epigenetic variation at a population level in their natural habitat and whether this correlates with species fitness and an increased resilience to fluctuating environments.

In this project we will use a unique approach to address the novel hypothesis that transmission of epigenetic information predicts resilience to environmental change.  This project will be based in the School of Biology at the University of Leeds and combines the skills of all three of the supervisors to amalgamate laboratory-based studies with population studies of epigenetic variation and field studies.

Applicant background

Necessary background for students: First class undergraduate degree in biology, zoology, ecology, or genetics and/or a masters qualification in a related area. Some experience in molecular techniques is highly desirable but not essential.

References

1.         Duncan, E.J., Gluckman, P.D., and Dearden, P.K. (2014). Epigenetics, plasticity, and evolution: How do we link epigenetic change to phenotype? Journal of experimental zoology. Part B, Molecular and developmental evolution 322, 208-220.

2.         Holderegger, R., Kamm, U., and Gugerli, F. (2006). Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landscape Ecology 21, 797-807.

3.         Dunn, R.R. (2005). Modern Insect Extinctions, the Neglected Majority Extinciones Modernas de Insectos, la Mayoría Desatendida. Conservation Biology 19, 1030-1036.

4.         Triggs, A.M., and Knell, R.J. (2012). Parental diet has strong transgenerational effects on offspring immunity. Functional Ecology 26, 1409-1417.

5.         Jones, T.S., Bilton, A.R., Mak, L., and Sait, S.M. (2015). Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species. Ecology and Evolution 5, 459-465.

6.         Chatterjee, A., Lagisz, M., Rodger, E.J., Zhen, L., Stockwell, P.A., Duncan, E.J., Horsfield, J.A., Jeyakani, J., Mathavan, S., Ozaki, Y., et al. (2016). Sex differences in DNA methylation and expression in zebrafish brain: a test of an extended 'male sex drive' hypothesis. Gene 590, 307-316.

7.         Chatterjee, A., Stockwell, P.A., Rodger, E.J., Duncan, E.J., Parry, M.F., Weeks, R.J., and Morison, I.M. (2015). Genome-wide DNA methylation map of human neutrophils reveals widespread inter-individual epigenetic variation. Scientific reports 5, 17328.

8.         Schield, D.R., Walsh, M.R., Card, D.C., Andrew, A.L., Adams, R.H., and Castoe, T.A. (2016). EpiRADseq: scalable analysis of genomewide patterns of methylation using next-generation sequencing. Methods in Ecology and Evolution 7, 60-69.

Related undergraduate subjects:

  • Biology
  • Ecology
  • Zoology