IAP-24-003

How development shapes the pace-of-life of animals

Explanations for most biological phenomena are framed within standard, ‘gene-centric’ evolutionary theory that assumes that genes determine the phenotypic traits of living organisms, i.e., how they look and behave (Fig. 1A) [1]. But this theory does not consider the fact that when individuals grow up, developmental processes can ‘bias’ the direction of evolution so that their phenotypes can no longer be linked to genes [2-4,5-7]. A new, ‘development-centric’ theory of evolution (Fig. 1B) [2] is still controversial because it takes genes as only one of many resources that construct phenotypes [3,4]. But as an alternative conceptual framework. However, it can help increase our understanding of unexplained biological phenomena [2-4,5-7].

Biologists have recently adopted a more holistic, organismal approach to understanding animal phenotypes, suggesting that traits related to life-history speed (ranging from a less-fecund, longer-developing ″slow″ pace to a more-fecund, shorter-developing ″fast″ pace), physiology (e.g., body size, energy allocation strategy) and behaviour (e.g., dispersal, aggression) have coevolved to form a ‘pace-of-life syndrome’ (POLS) [8]. However, empirical observations reject the gene-centric assumptions of current POLS theory [9-11]. Here, we will, for the first time, apply development-centric theory to explain the existence of POLSs. We can then resolve why current POLS theory fails to predict which animals along the POLS continuum are most resilient to environmental change [8,12,13]. More broadly, we can reveal the potential that development-centric theory has to transform the field of evolutionary science [3].

The aim of this project is to test new POLS predictions using a development-centric, state-of-the-art life-history model in the laboratory to (i) explain why POLSs exist, (ii) how they evolve, and (iii) how they can be used to predict animal responses to environmental change.

The project starts with a meta-analysis on predicting the population responses to climate change from a development-centric perspective (paper 1).

We will then conduct laboratory experiments, where 12 populations will be kept at a low density and 12 at a high density at 24C [7]. Each population is in a 10-mm diameter, 25 mm high glass tube [7]. Densities are kept low (or high) by transferring 20% (or 80%) of the current population to a new tube every week [7]. All populations will have ad lib access to filter paper disks (232 mm) soaked in 40 mg yeast/ml water to ensure an even food distribution [14]) (Fig. 2). After 1, 3, and 10 generations (mite life-history evolves within a few generations [7]) (Fig. 2), we will use our protocols [15] to conduct 10x replicated, life-history assays by raising 10 individual eggs to adulthood from each population on a 2.5-fold yeast dilution series (1, 2.56, 6.4, 16, 40 mg/ml [16]), representing a population density gradient [14]. We will daily measure survival, growth, reproduction, dispersal expression (Fig. 1B: life stage d) [16], adult male morphs (Fig. 1B, life stages f & g; males mitigate food stress by developing into scramblers: [5]), and test the effect of population density on these variables, and their variation, using generalised linear mixed models (GLMMs) (with treatments as fixed factors, population tube as random factor).

The results will show if a POLS exists (paper 2). After 10 generations, we will simulate environmental change by increasing temperature to 28C for ⅓ of populations (which impacts development, reproduction, plasticity [14]) and switching ⅓ of all populations to a new food type (oats [15]), while leaving the final ⅓ undisturbed (Fig. 2). We will then conduct the same assays and analyses as before to determine whether the POLS evolves in response, and if low and high density-adapted populations respond differently to environmental change (also testing WP1 predictions) (paper 3; and paper 4 on whether density-dependent selection can maintain a male dimorphism).

Risk of experiments failing is minimised as the PA has worked with R. robini for over 15 years.

Dr Anja Guenther from the Max Planck Institute for Evolutionary Genetics, who is a POLS expert, will be involved as external advisor.

Year 1

– Conduct a meta-analysis.
– Start writing paper 1.
– Design and start long-term experiment.

Year 2

– Finish long-term experiment and analyse data.
– Conduct any additional life history experiments.
– Attend national conference to present first findings and network
– Finish paper 1; start writing paper 2.

Year 3

– Conduct any additional life history experiments.
– Write papers 3 and 4.

Year 3.5

Submit papers to peer-reviewed, high-impact journals.
– Attend international conference to present findings.
– Thesis completion.

The prospective student should have a background in population biology, life history theory and/or behavioural ecology. A strong interest in running experiments in the laboratory with small organisms is essential and any experience therein desirable. University modules and the supervisory team will provide the necessary data analysis and software training. Additional training will be identified to meet the needs throughout the studentship.