Recurrent Extreme Climatic Events Are Driving Gorgonian Populations to Local Extinction: Low Adaptive Potential to Marine Heatwaves

Abstract

Extreme climatic events (ECEs), such as marine heatwaves (MHWs), are a major threat to biodiversity. Understanding the variability in ecological responses to recurrent ECEs within species and underlying drivers arise as a key issue owing to their implications for conservation and population recovery. Yet, our knowledge on such ecological responses is limited since it has been frequently gathered following "single-event approaches" focused on one particular event. These approaches provide snapshots of ecological responses but fall short of capturing heterogeneity patterns that may occur among recurrent ECEs, questioning current predictions regarding biodiversity trends. Here, we adopt a "multiple events" perspective to characterize the effects of recurrent ECEs on the ecological responses in Paramuricea clavata, a Mediterranean temperate coral threatened by MHWs. Through a common-garden experiment repeated three consecutive years with the same individuals from three populations, we assessed the respective roles of environmental (year effect), genetic (population effect), and phenotypic (population-by-environment interactions effect) components in the ecological response to recurrent heat stress. The environmental component (year) was the main driver underlying the responses of P. clavata colonies across experiments. To build on this result, we showed that: (i) the ecological responses were not related to population (genetic isolation) and individual (multilocus heterozygosity) genetic make-up, (ii) while all the individuals were characterized by a high environmental sensitivity (genotype-by-environment interactions) likely driven by in situ summer thermal regime. We confront our experimental results to in situ monitoring of the same individuals conducted in 2022 following two MHWs (2018, 2022). This confirms that the targeted populations harbor limited adaptive and plastic capacities to on-going recurrent ECEs and that P. clavata might face unavoidable population collapses in shallow Mediterranean waters. Overall, we underscore the need to consider the recurrence of ECEs to assess threats to biodiversity and to forecast its evolution.

Keywords: Mediterranean Sea; common‐garden experiment; ecological memory; genotype‐by‐environment interactions; habitat‐forming octocorals; mass mortality events.