Plasticity and associated epigenetic mechanisms play a role in thermal evolution during range expansion

Janne Swaegers* (Corresponding Author), Simon De Cupere, Noah Gaens, Lesley T Lancaster, José A Carbonell, Rosa A Sánchez Guillén, Robby Stoks

*Corresponding author for this work

Research output: Contribution to journalLetterpeer-review

Abstract

Due to global change, many species are shifting their distribution and are thereby confronted with novel thermal conditions at the moving range edges. Especially during the initial phases of exposure to a new environment, it has been hypothesized that plasticity and associated epigenetic mechanisms enable species to cope with environmental change. We tested this idea by capitalizing on the well-documented southward range expansion of the damselfly Ischnura elegans from France into Spain where the species invaded warmer regions in the 1950s in eastern Spain (old edge region) and in the 2010s in central Spain (new edge region). Using a common garden experiment at rearing temperatures matching the ancestral and invaded thermal regimes, we tested for evolutionary changes in (thermal plasticity in) larval life history and heat tolerance in these expansion zones. Through the use of de- and hypermethylating agents, we tested whether epigenetic mechanisms play a role in enabling heat tolerance during expansion. We used the phenotype of the native sister species in Spain, I. graellsii, as proxy for the locally adapted phenotype. New edge populations converged toward the phenotype of the native species through plastic thermal responses in life history and heat tolerance while old edge populations (partly) constitutively evolved a faster life history and higher heat tolerance than the core populations, thereby matching the native species. Only the heat tolerance of new edge populations increased significantly when exposed to the hypermethylating agent. This suggests that the DNA methylation machinery is more amenable to perturbation at the new edge and shows it is able to play a role in achieving a higher heat tolerance. Our results show that both (evolved) plasticity as well as associated epigenetic mechanisms are initially important when facing new thermal regimes but that their importance diminishes with time.Climate change is confronting species with new conditions, yet it remains a key uncertainty of what processes underlie successful responses to cope with novel thermal regimes. Plasticity is considered to be especially important during the initial phases of exposure to a new environment, while evolution is assumed to act in the longer term. The many range expansions whereby species encounter new thermal conditions provide powerful ‘natural experiments’ to study these processes ‘in action’. We capitalized on the range expansion of a damselfly from France into a warmer region in Spain. This allowed to compare French core populations that are the source of the expansion with new edge populations and with old edge populations. The latter has been the longest exposed to the new thermal regime. We used the phenotype of the native sister species in Spain as a proxy for the locally adapted phenotype. Using a common garden experiment at rearing temperatures matching the ancestral and invaded thermal regimes, we tested how plasticity and evolution contribute to larval life history and heat tolerance changes in these expansion zones. New edge populations became more similar to the phenotype of the native species through plastic thermal responses in life history and heat tolerance while old edge populations (partly) evolved a faster life history and higher heat tolerance toward the phenotype of the native species (i.e., at both rearing temperatures). Our results also suggest that epigenetic mechanisms (i.c., DNA methylation) are able to play a role in achieving a higher heat tolerance in new edge populations. Our results provide unique insights into how populations adapt to new environments and support the theory that both (evolved) plasticity as well as associated epigenetic mechanisms are initially important when facing new thermal regimes but that their importance diminishes with time whereby evolution gets more important.
Original languageEnglish
Article numberqrac007
Number of pages13
JournalEvolution Letters
Early online date31 Jan 2023
DOIs
Publication statusE-pub ahead of print - 31 Jan 2023

Keywords

  • thermal plasticity
  • thermal evolution
  • range expansion
  • DNA methylation
  • warming

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