Additive genetic and environmental variation interact to shape the dynamics of seasonal migration in a wild bird population

Paul Acker* (Corresponding Author), Francis Daunt, Sarah Wanless, Sarah J Burthe, Mark A Newell, Michael P Harris, Robert L Swann, Carrie Gunn, Tim I Morley, Jane M Reid

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Dissecting joint micro-evolutionary and plastic responses to environmental perturbations requires quantifying interacting components of genetic and environmental variation underlying expression of key traits. This ambition is particularly challenging for phenotypically discrete traits where multiscale decompositions are required to reveal non-linear transformations of underlying genetic and environmental variation into phenotypic variation, and when effects must be estimated from incomplete field observations. We devised a joint multistate capture-recapture and quantitative genetic animal model, and fitted this model to full-annual-cycle resighting data from partially-migratory European shags (Gulosus aristotelis) to estimate key components of genetic, environmental and phenotypic variance in the ecologically critical discrete trait of seasonal migration versus residence. We demonstrate non-negligible additive genetic variance in latent liability for migration, resulting in detectable micro-evolutionary responses following two episodes of strong survival selection. Further, liability-scale additive genetic effects interacted with substantial permanent individual and temporary environmental effects to generate complex non-additive effects on expressed phenotypes, causing substantial intrinsic gene-by-environment interaction variance on the phenotypic scale. Our analyses therefore reveal how temporal dynamics of partial seasonal migration arise from combinations of instantaneous micro-evolution and within-individual phenotypic consistency, and highlight how intrinsic phenotypic plasticity could expose genetic variation underlying discrete traits to complex forms of selection.

Original languageEnglish
Pages (from-to)2128-2143
Number of pages16
JournalEvolution
Volume77
Issue number10
Early online date21 Jun 2023
DOIs
Publication statusPublished - 1 Oct 2023

Bibliographical note

We thank everyone who contributed to long-term field data collection, particularly Raymond Duncan, Sarah Fenn, Hannah Grist, Calum Scott, Jenny Sturgeon, Moray Souter, John Anderson, and Harry Bell; and thank NatureScot for allowing work on the Isle of May National Nature Reserve, and Isle of May Bird Observatory Trust for supporting the longterm ringing of shags. We thank Stefanie Muff for helpful discussions, and Rita Fortuna and Thomas R. Haaland for useful comments on a manuscript draft. The current study was funded by Natural Environment Research Council (NERC; awards NE/M005186/1, NE/R000859/1, and NE/R016429/1 as part of the UK-SCaPE program delivering National Capability), Norwegian Research Council (SFF-III grant 223257, FRIPRO grant 313570), NTNU and University of Aberdeen. Analyses were performed using the IDUN cluster of NTNU

Data Availability Statement

All data and code used in this study are available from Dryad at https://doi.org/10.5061/dryad.pk0p2ngtg

Supplementary material is available online at Evolution.

Keywords

  • alternative tactics
  • capture-recapture animal model
  • cryptic genetic variation
  • gene by environment interaction
  • partial migration
  • quantitative genetic threshold trait

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