Arrival of the fittest: examining the underlying mechanisms of morphological plasticity in an adaptive radiation

Overview

Phenotypic plasticity currently drives contentious debate in evolutionary biology (1,2,3). This debate deals with the role of environmental cues in generating biodiversity, species, and ultimately the utility of the standard Darwinian synthesis (or its extension) (2). While plasticity is a topic of much empirical research with growing relevance to environmental change, we still lack a general understanding of the underlying mechanisms of plasticity in evolutionary systems. This project will draw on mechanistic knowledge from bone biology to fill this gap, specifically focusing on how bones interact with and interpret the stimuli that instruct their growth and produce adaptive variation.

Our previous research has identified variation in the magnitude of bone plasticity between related species of African cichlids. Cichlids are an exemplary system for evolutionary biologists in that they are derived from a recent common ancestor but exhibit vast amounts of adaptive skeletal variation. This variation appears to be controlled by a few mutations on a common genetic background. So far we have combined plasticity experiments with QTL mapping approaches to identify a number of candidate ‘plasticity genes’ in the craniofacial skeleton. These genes include members of signalling pathways previously implicated in bone development (Wnts, BMPs, FGFs), and structural genes including rootletin – a key component of the primary cilia and representative of a potential mechanism for bone mechanosensory function (3). These findings provide a strong basis for understanding the molecular and cellular mechanisms involved in plasticity and their contribution to evolution.

The PhD candidate will answer three key questions:
1) What mechanisms underly differences in the magnitude of plasticity?
2) Does the amount of bone plasticity rely on evolved differences among species?
3) Do parents induce plastic responses in bone through the environments they choose?

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Image Captions

Cichlid craniofacial diversity

Methodology

To address these questions, we will conduct a series of lab rearing experiments in a range of cichlids (~15 species). These will focus on inducing plastic responses in head morphology and its associated bones using established protocols that vary the position, size, and hardness of food to mimic natural ‘biting’ and ‘suction’ modes of feeding (1). These experiments will be used in conjunction with a range of lab techniques to understand plasticity mechanisms.
Question 1) will be addressed by assessing gene expression in a subset of cichlids (4 species) undergoing plasticity experiments. Targeting candidate genes for plastic qPCR will be performed on the bony elements of the oral jaws. This will occur at three phases, 2 weeks, 1 month, and 2 months following the initiation of foraging experiments. We predict that our candidate genes will show significant responses to treatment through the duration of the experiment. However, to go beyond gene expression to understand the cellular basis of plasticity the project will use novel approaches. Specifically, this will involve culturing cichlid bone cells in vitro and exposing them to nanovibrational stimulation (i.e ‘Nanokicking’) developed by Dalby (4). This technique programmes cells for bone growth (osteogenesis) and would be akin to plastic responses induced in vivo. The resolution afforded by this approach will allow us to observe the activity of cellular mechanisms using fluorescence staining.
Question 2) will build on our knowledge of cichlid morphology. Previous study has determined that divergence primarily involves relative lengthening and shortening of the jaws among species (1). Ecological generalists are found at the midpoint of morphospace, while specialists are at the extremes. Theory predicts that plasticity would be reduced in extreme phenotypes. We will test this prediction in the lab by using morphometric approaches across species exposed to different foraging modes couple with assays of gene expression. Question 3) will complement this lab work by testing the effect of parental care on bone growth and shape. Specifically, the student would experimentally alter the parental care environment and compare outcomes in offspring.

Project Timeline

Year 1

– Rearing of cichlids under different foraging treatments
– Collection of material for qPCR gene expression assays
– Establishment of in vitro cell culture protocols

Year 2

– Measurement of gene expression from fish and from in vitro cell cultures
– Measurement of plasticity in morphometric variation
– Initiation of writing for a first paper

Year 3

– Lab work for material collected from experimental fish
– completion of data collection
– Analysis of data and writing of chapters

Year 3.5

– Final editing and writing of chapters

Training
& Skills

The candidate will learn a broad range of transferable skills that will enhance his or her prospects and prepare them for a career in academia or industry. These skills include fish husbandry, data management and manipulation, fluorescent microscopy, molecular biology and genetic techniques, morphometrics and multivariate statistics. The student would also gain an understanding of functional morphology in skeletal systems and bone biology. We will take advantage of the close proximity of the supervisors to ensure frequent meetings, and the candidate will also profit from exposure to the extended networks of the collaborating team.

References & further reading

1. Parsons KJ, Concannon M, Navon D, Wang J, Ea I, Groveas K (2016) Foraging environment determines the genetic architecture and evolutionary potential of trophic morphology in cichlid fishes. Mol. Ecol. 25, 6012-6023.
2. Laland K. N., Uller T., Feldman M. W., Sterelny K., Müller G. B., Moczek A., Jablonka E. & Odling-Smee F.J.2015The extended evolutionary synthesis: its structure, assumptions and predictions. Proc. R. Soc. B 282, 20151019.
3. D Navon, I Male, ER Tetrault, B Aaronson, RO Karlstrom, RC Albertson 2020. Hedgehog signaling is necessary and sufficient to mediate craniofacial plasticity in teleosts. Proceedings of the National Academy of Sciences 117 (32), 19321-19327.
4. Robertson SN, et al. (2018) Control of cell behaviour through nanovibrational stimulation: nanokicking. Phil. Trans. Roy. Soc. A: Math. Phys. Eng. Sci., 376(2120), 20170290

Further Information

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

Email: Kevin.Parsons@glasgow.ac.uk
https://sites.google.com/site/kevinparsonslab/home
https://www.gla.ac.uk/researchinstitutes/biology/staff/matthewdalby/

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