Loss of transcriptional plasticity but sustained adaptive capacity after adaptation to global change conditions in a marine copepod

Reid S Brennan,Hans G Dam,Michael B Finiguerra,Hannes Baumann,James A Demayo,Melissa H Pespeni

doi:10.1038/s41467-022-28742-6

Abstract

Adaptive evolution and phenotypic plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earth’s oceans, however, we have much to learn about the interactions and costs of these mechanisms of resilience. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplants, we investigated the relationship between adaptation and plasticity in the marine copepod, Acartia tonsa, in future global change conditions (high temperature and high CO2). We found parallel adaptation to global change conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when global change-adapted animals were returned to ambient conditions or reared in low food conditions. However, after three successive transplant generations, global change-adapted animals were able to match the ambient-adaptive transcriptional profile. Concurrent changes in allele frequencies and erosion of nucleotide diversity suggest that this recovery occurred via adaptation back to ancestral conditions. These results demonstrate that while plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations adapted, limiting resilience to new stressors and previously benign environments.

Highlights

While the static conditions in the lab are a limitation of these studies as they do not necessarily represent the variable conditions found in the wild, experimental losses of plasticity under static conditions raise the concern that the strong selection driving rapid adaptation to global change may purge phenotypic plasticity from populations
Given the likely polygenic nature of adaptation to warming and acidification conditions and that polygenic traits tend to be genetically redundant[65,66], the identified adaptive genetic variation would be prone to false negatives due to the requirement that adaptation be parallel in all replicates
NDUFS2 is a nuclearencoded, core subunit of Complex 1 of the mitochondrial electron transport chain (ETC) that has been shown to be inhibited by heat stress[68,69]

Summary

Introduction

For short-lived species, these extreme conditions may be longer than their generation time and selection may drive rapid adaptation that reduces plasticity, resulting in populations that are less resilient when environments fluctuate in the future, which is expected under global change[1]. We identified plastic changes in gene expression for OWA and AM lines by comparing expression in the home environment after 20 generations to gene expression responses at the end of one generation in transplant conditions (AMAM vs AMOWA and OWAAM vs OWAOWA; Fig. 3a).

Results

Conclusion