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Variation in personality shaped by evolutionary history, genotype, and developmental plasticity in response to feeding modalities in the Arctic charr

Cite this dataset

Dellinger, Marion et al. (2023). Variation in personality shaped by evolutionary history, genotype, and developmental plasticity in response to feeding modalities in the Arctic charr [Dataset]. Dryad. https://doi.org/10.5061/dryad.4f4qrfjk2

Abstract

Animal personality has been shown to be influenced by both genetic and environmental factors and shaped by natural selection. Currently, little is known about mechanisms influencing the development of personality traits. This study examines the extent to which personality development is genetically influenced and/or environmentally responsive (plastic). We also investigated the role of evolutionary history, assessing whether personality traits could be canalized along a genetic and ecological divergence gradient. We tested the plastic potential of boldness in juveniles of five Icelandic Arctic charr morphs (Salvelinus alpinus), including two pairs of sympatric morphs, displaying various degrees of genetic and ecological divergence from the ancestral anadromous charr, split between treatments mimicking benthic vs. pelagic feeding modalities. We show that differences in mean boldness are mostly affected by genetics. While the benthic treatment led to bolder individuals overall, the environmental effect was rather weak, suggesting that boldness lies under strong genetic influence with reduced plastic potential. Finally, we found hints of differences by morphs in boldness canalization through reduced variance and plasticity, and higher consistency in boldness within morphs. These findings provide new insights into how behavioural development may impact adaptive diversification.

README: Variation in personality shaped by evolutionary history, genotype, and developmental plasticity in response to feeding modalities in the Arctic charr

https://doi.org/10.5061/dryad.4f4qrfjk2

Marion Dellinger1,2; Sarah E. Steele2,3; Evert Sprockel1,4; Joris Philip1,5; Arnar Pálsson2; David Benhaïm1

1 Department of Aquaculture and Fish Biology, Hólar University, Iceland; 2 Institute of Life and Environmental Sciences, School of Engineering and Natural Sciences, University of Iceland, Iceland; 3 Canadian Museum of Nature, Canada; 4 HAS University, the Netherlands; 5 Scottish Centre for Ecology and the Natural Environment, University of Glasgow, Scotland

Research questions

In the present study, we examined what roles genotype, plasticity and canalization play in the development of personality in the Arctic charr. We focused on a widely studied aspect of animal personality, boldness – the individual propensity to take risks – that has recently been reported in the Arctic charr.
We hypothesised that:

  1. differences in ecological backgrounds lead to the evolution of different personality profiles between morphs (genotype)
  2. the early environment influences the developmental trajectories of personality traits (developmental plasticity of personality) within morphs
  3. the degree of evolutionary divergence influences the degree of developmental plasticity of personality and the magnitude of personality range between morphs, potentially via canalization.

To address this, juvenile full-sibs of AN, VS, VB, LB and PL Arctic charr morphs were reared in common garden in benthic vs. pelagic feeding modality treatments. We tested for differences in boldness repeatability, averages, and variances across morphs and treatments to characterise personality profiles.
If personality development is under genetic influence (1.), we expected mean boldness to be morph-specific, or at least population-specific (between lakes/rivers).
If personality development responds to environmental conditions, i.e., is plastic (2.), we expected differences in mean boldness between treatments, either overall or within morphs.
If a longer time since divergence leads to canalization of personality traits (3.), we expected reduced plasticity, lower boldness variance and higher boldness consistency (repeatability) in more diverged morphs.
Note that these predictions are not mutually exclusive.

Data acquisition

All fish were submitted twice to a Open Field Test (OFT) with shelter, with a 7-day interval between each replication (video-recorded at 30 frames per second). At the beginning of the test, the focal fish was placed in the closed shelter of the OFT arena. After 5 minutes acclimation, the shelter door was opened and the fish was free to explore the arena for 20 minutes. The fish were tracked from the obtained videos with Ethovision XT version 14 (Noldus Information Technology). The arena was divided into four virtual zones: the shelter zone covering the shelter area, overlapping with an entry zone; the border zone along the edges of the arena; the centre zone being the remaining part of the arena⁠. The fish barycentre was used to calculate behavioural variables presented in the Metadata. The associated dataset can be found under the name "RSPB-2023-2302_Data.xlsx".

Metadata

  • PCF = the unique ID of each individual fish
  • Trial.rep = the replication (either A or B) as OFT tests were repeated twice for each fish
  • Population = the morph (AN, VS, VB, LB, PL) to which the focal fish belongs
  • Trial.no = the number of the OFT trial, i.e. the order in which fish were tested. NB: one trial consisted of 4 arenas tested simultaneously, hence 4 fish having the same trial.no
  • Arena.no = the number of the arena in which the focal fish was tested during the trial
  • Date = the day at which the OFT test took place for the focal fish
  • Time.categories = the time slot (Early.morning, Late.morning, Early.afternoon, etc) when the OFT test was carried out for the focal fish
  • Family = the family (crossing) to which the focal fish belongs. NB: there are 3 families per morph in our design.
  • Color = the VIE colour tag code identifying the focal fish
  • Size = the size category (Small, Medium, Large, corresponding respectively to the 1st, 2nd and 3rd quantiles of the body size distribution of a family within a tank) associated to each focal fish
  • Tank = the tank replicate to which the focal fish belongs
  • Treatment = the feeding modality (Benthic or Pelagic) under which the focal fish was raised
  • T.before = temperature in the OFT arena at the beginning of the OFT trial (°C)
  • T.after = temperature in the OFT arena at the end of the OFT trial (°C)
  • T.average = the average temperature over the OFT trial, i.e., (T.before + T.after)/2 (°C)

    NB: T.after measurements were not available (NA) for the first OFT trial (Trial.no: 1). As the variation in temperature over the trials was usually very low (median increase of 0.6°C), we attributed a T.average value in each arena for this particular trial corresponding to the T.before value in each given arena.

  • FL = fork length of the focal fish, measured from the tip of the snout to the fork of the caudal fin (cm)

  • TL = total length of the focal fish, measured from the tip of the snout to the tip of the caudal fin lobes (cm)

  • m = weight of the fish (g)

Behavioural variables recorded for the focal fish in the OFT arena during the 20 minutes free phase:

  • Dtot = the total distance travelled (cm)
  • v = the mean swimming velocity (cm/s)
  • v.bl = the mean swimming velocity divided by the total length of the focal fish (i.e., v/TL, s^-1)
  • v.ang = absolute angular velocity (deg/s)
  • XXX.freq = the frequency of visits to the XXX zone
  • XXX.duration = the amount of time spent in the XXX zone (s)
  • Exit.time = the latency to exit the shelter for the first time (head and trunk visible, s)

Code/Software/Supplements

The code used to obtain boldness scores and analyse the data is available here under the name "RSPB-2023-2302_Accompanying_R_Script" both in .Rmd and in .html formats. Supplementary figures and tables associated to the main text can be found here under the name "RSPB-2023-2302_Supplements.pdf" as well as in the electronic supplementary material of the related article (https://doi.org/10.1098/rspb.2023.2302) through the following DOI: https://doi.org/10.6084/m9.figshare.c.6957270

Methods

Research questions

In the present study, we examined what roles genotype, plasticity and canalization play in the development of personality in the Arctic charr. We focused on a widely studied aspect of animal personality, boldness – the individual propensity to take risks – that has recently been reported in the Arctic charr.

We hypothesized that:

  1. differences in ecological backgrounds lead to the evolution of different personality profiles between morphs (genotype).

  2. the early environment influences the developmental trajectories of personality traits (developmental plasticity of personality) within morphs.

  3. the degree of evolutionary divergence influences the degree of developmental plasticity of personality and the magnitude of personality range between morphs, potentially via canalization.

To address this, juvenile full-sibs of AN, VS, VB, LB and PL Arctic charr morphs were reared in a common garden in benthic (feeding exclusively at the bottom) vs. pelagic (feeding exclusively in the water column) feeding modality treatments. We tested for differences in boldness repeatability, averages, and variances across morphs and treatments to characterize personality profiles.

If personality development is under genetic influence (1.), we expected mean boldness to be morph-specific, or at least population-specific (between lakes/rivers).

If personality development responds to environmental conditions, i.e., is plastic (2.), we expected differences in mean boldness between treatments, either overall or within morphs.

If a longer time since divergence leads to canalization of personality traits (3.), we expected reduced plasticity, lower boldness variance and higher boldness consistency (repeatability) in more diverged morphs.

Note that these predictions are not mutually exclusive.

Data acquisition

All fish were submitted twice to a Open Field Test (OFT) with shelter, with a 7-day interval between each replication (video-recorded at 30 frames per second). At the beginning of the test, the focal fish was placed in the closed shelter of the OFT arena. After 5 minutes of acclimation, the shelter door was opened and the fish was free to explore the arena for 20 minutes. The fish were tracked from the obtained videos with Ethovision XT version 14 (Noldus Information Technology). The arena was divided into four virtual zones: the shelter zone covering the shelter area, overlapping with an entry zone; the border zone along the edges of the arena; the centre zone being the remaining part of the arena⁠. The fish barycentre was used to calculate behavioural variables presented in the Metadata.

Metadata

  • PCF = the unique ID of each individual fish
  • Trial.rep = the replication (either A or B) as OFT tests were repeated twice for each fish
  • Population = the morph (AN, VS, VB, LB, PL) to which the focal fish belongs
  • Trial.no = the number of the OFT trial, i.e. the order in which fish were tested. NB: one trial consisted of 4 arenas tested simultaneously, hence 4 fish having the same trial.no
  • Arena.no = the number of the arena in which the focal fish was tested during the trial
  • Date = the day at which the OFT test took place for the focal fish
  • Time.categories = the time slot (Early.morning, Late.morning, Early.afternoon, etc) when the OFT test was carried out for the focal fish
  • Family = the family (crossing) to which the focal fish belongs. NB: there are 3 families per morph in our design.
  • Color = the VIE color tag code identifying the focal fish
  • Size = the size category (Small, Medium, Large, corresponding respectively to the 1st, 2nd and 3rd quantiles of the body size distribution of a family within a tank) associated to each focal fish
  • Tank = the tank replicate to which the focal fish belongs
  • Treatment = the feeding modality (Benthic or Pelagic) under which the focal fish was raised
  • T.before = temperature in the OFT arena at the beginning of the OFT trial (°C)
  • T.after = temperature in the OFT arena at the end of the OFT trial (°C)
  • T.average = the average temperature over the OFT trial, i.e., (T.before + T.after)/2 (°C)
    NB: T.after measurements were not available (NA) for the first OFT trial (Trial.no: 1). As the variation in temperature over the trials was usually very low (median increase of 0.6°C), we attributed a T.average value in each arena for this particular trial corresponding to the T.before value in each given arena.
  • FL = fork length of the focal fish, measured from the tip of the snout to the fork of the caudal fin (cm)
  • TL = total length of the focal fish, measured from the tip of the snout to the tip of the caudal fin lobes (cm)
  • m = weight of the fish (g)

Behavioural variables recorded for the focal fish in the OFT arena during the 20-minute free phase:

  • Dtot = the total distance travelled (cm)
  • v = the mean swimming velocity (cm/s)
  • v.bl = the mean swimming velocity divided by the total length of the focal fish (i.e., v/TL, s^-1)
  • v.ang = absolute angular velocity (deg/s)
  • XXX.freq = the frequency of visits to the XXX zone
  • XXX.duration = the amount of time spent in the XXX zone (s)
  • Exit.time = the latency to exit the shelter for the first time (head and trunk visible, s)

Funding

The Icelandic Centre for Research, Award: 228515-051, Icelandic Research Fund

The Icelandic Centre for Research, Award: 195615-051, Icelandic Research Fund

The Icelandic Centre for Research, Award: 184897-051, Icelandic Research Fund

European Union, Erasmus+ programme