NSFGEO-NERC: Integrating individual personality differences in the evolutionary ecology of a seabird in the rapidly changing polar environment

Lead Research Organisation: University of Liverpool
Department Name: Earth, Ocean and Ecological Sciences

Abstract

To date, studies that have addressed the impacts of global changes have mainly focused on linking
climate variability and/or human disturbances to individual life history traits, population dynamics or
distribution. However, individual behavior and plasticity mediate these responses. The goal of this project
is to understand mechanisms linking environmental changes (climate & fisheries) - behavioral personality
type - plasticity in foraging behaviors - life history traits - population dynamics for a seabird breeding in
the southern ocean: the wandering albatross. This project will also forecast the population structure and
growth rate using the most detailed mechanistic model to date for any wild species incorporating
behaviors in an eco-evolutionary context. Specifically, the investigators will (1) characterize the life
history strategies along the shy-bold continuum of personalities and across environmental conditions; (2)
understand the link between phenotypic plasticity in foraging effort and personality; (3) characterize the
heritability of personality and foraging behaviors; (4) develop a stochastic eco-evolutionary model to
understand and forecast the distribution of bold and shy individuals within the population and the
resulting effect on population growth rate in a changing environment by integrating processes from goals
1, 2 and 3. To date, this has been hampered by the lack of long-term data on personality and life histories
in any long-lived species in the wild. For the first time ever, we have tested in a controlled environment
the response to a novel situation for ~1800 individuals for more than a decade to define individual
personality variation along the shy-bold continuum that we can relate to the life history traits over the
entire species life cycle using unique long-term individual mark-recapture data sets for this iconic polar
species. The novelty of this project thus lies in the combination of personality, foraging and demographic
data to understand and forecast population responses to global change using state-of-the-art statistical
analysis and eco-evolutionary modeling approaches.

Publications

10 25 50
 
Description Objective 1: Life history strategies
Our results indicate that personality covaries with individual vital rates in sex-specific fashion. Bolder females displayed higher survival rates, as well as higher breeding probability and breeding success. Bolder males, by contrast, displayed lower breeding probability, but no significant effects on breeding success were detected. Boldness had little effects on life- history outcomes in females; but bolder males had lower life-time reproductive success and life expectancy. These findings suggest that even if bolder females have higher breeding probability, the trade-offs between survival and reproduction, with non-breeding females having a higher survival rate, compensates for the lower breeding probability of shyer females resulting in a small effect of boldness on life-history outcomes. We extended these analyses to show support for the slow-fast continuum of life histories in females compared but not males.
These results show that personality is more correlated with life-history trade-offs in female wandering albatrosses, especially when considering only females that reproduce multiple times in their lifetime. This is consistent with the first analysis suggesting that those trade-offs obscure the effect of personality on life history outcomes in females. They also show that there are potentially different reproductive tactics in the population or that there may be an elevated cost of successful first reproduction in the wandering albatross, which are independent of individual personality.

Objective 2: Phenotypic plasticity in foraging behaviours
Bolder birds showed lower sensitivity to changes in wind conditions. Specifically, in strong winds, which are optimal for the dynamic soaring flight of albatrosses, all individuals increased investment in travel behaviour, indicative of explorative foraging. However, in weaker winds, behavioural responses diverged along the gradient of boldness, such that shyer individuals invested preferentially in search, indicative of exploitative foraging, while bolder individuals maintained investment in travel. This highlights that individual variation in plasticity may limit the capacity of bold individuals to adapt to challenging conditions.

This work was extended to look at how foraging success itself changed with intrinsic and extrinsic factors. Our results show that the chance of albatrosses attempting to feed, and feeding successfully, was dependent on the environment and age.

Objective 3: Heritability in personality and in foraging behaviours
There was moderate repeatability (0.44) and heritability of boldness (0.19) in the population, and uncovered sex and age effects. Males were shyer than females on average, and in both sexes, individuals became shyer with increasing age, as indicated by the declining response of older birds. The age-related decline was more pronounced in males; in early life, the responses of males and females to human approach are very similar. Boldness was two times larger in males than females and was driven by a higher additive genetic variance in males. The cross-sex genetic correlation in boldness was positive and significantly less than one. This implies that the evolution of sex differences in boldness is heavily constrained, so that any sexually-antagonistic selection on boldness would need to be very strong to drive the evolution of sexually dimorphic personality values.
The results of our simulations suggest that there is low power to detect significantly non-zero but low heritabilities with our data set. This is presumably because of the relatively weak connectedness of the pedigree. It would be difficult to know whether to treat heritability estimates with a lower bound of zero as a genuine biological effect - the trait is not heritable - or as a limitation of the data structure.

Objective 4: Stochastic eco-evolutionary model
Using a hyper-state eco-evolutionary model, we simulated different heritability values to assess its effect on the growth rate for both sexes. The growth rate is less affected by heritability of personality at low and intermediate values, but increases exponentially when heritability is >0.80 for males and >0.85 in females. Given the low empirical estimate of heritability found in this grant, we anticipate that selective pressure on personality will have little effect on the growth rate. However, personality may affect the population structure in complex ways as the selective pressures are opposite on males and females, maintaining personality in a population.
Exploitation Route The results from this grant have led to two newly funded grants - one NSF and on NERC. These projects will build on this work and explore two new directions. The NERC standard grant (PI S. Patrick) will explore individual differences in foraging and resource acquisition in a changing environment and link this to individual reproductive investment time series. The grant will also examine the heritability of the covariation between resource acquisition and allocation, focussing on the lifetime reproductive histories of 1000s of individual albatrosses. The NSF ORCC grant (PI S. Jenouvrier) will build on the results from the demographic models, looking at population level effects and the impact of climate on population trajectories in a changing environment.
Sectors Environment

 
Description Exploring Frontiers
Amount £100,000 (GBP)
Funding ID NE/X012492/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 02/2023 
End 01/2024
 
Description MSCA Global Fellowship
Amount € 278,824 (EUR)
Funding ID 101148550 
Organisation Marie Sklodowska-Curie Actions 
Sector Charity/Non Profit
Country Global
Start 09/2024 
End 09/2027
 
Description Resolving the life-history trade-off paradox: Measuring resource acquisition to reveal life-history trade-offs over different temporal scales
Amount £597,457 (GBP)
Funding ID NE/X000680/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2022 
End 09/2025
 
Description Collaboration with CNRS 
Organisation Centre d'Etudes Biologiques de Chizé
Country France 
Sector Public 
PI Contribution expertise - I have specialised expertise on individual foraging behaviour, personality and the inheritance of behavioural traits intellectual input - I have participated in a range of projects with these collaborators, including writing a new grant off the back of this collaboration access to data - I have made all data available to these collaborators and help to generate specific products that they need
Collaborator Contribution expertise - My collaborators here are experts in seabird biology - including foraging ecology and demographic processes. They also have database experts who are able to provide the data we need to this project intellectual input - All members of the team have provided valuable intellectual input, helping to formulate hypotheses, test predictions and interpret the results access to data - The data we need for this project is held by this collaborator and they provided these to us
Impact https://doi.org/10.1098/rspb.2022.2252 https://doi.org/10.1002/ecm.1522 https://doi.org/10.1098/rsbl.2022.0301 https://doi.org/10.1111/1365-2656.13968
Start Year 2021
 
Description NSF collaboration with Woods Hole Oceanographic Institute 
Organisation Woods Hole Oceanographic Institution
Country United States 
Sector Charity/Non Profit 
PI Contribution This partner is part of the collaborative NSF component of our grant. Myself and Jack Thorley, the PDRA on the grant, specialise in foraging behaviour and personality research. We have been helping to develop proxies for these traits which can be integrated into population models.
Collaborator Contribution This partner is part of the collaborative NSF component of our grant. This involves Stephanie Jenouvrier, Joanie van de Walle and Ruijiao Sun. We have biweekly meetings and they have contributed to the direction of the project, analytical techniques and the framing out the outputs.
Impact Outcomes - the development of individual based measure of foraging and personality traits
Start Year 2021