Highlights d A marine heatwave caused massive loss of genetic diversity in underwater forests d Between 30% and 65% of average genetic diversity was lost across 800 km of coastline d Loss of genetic diversity was cryptic and not reflected in measures of forest cover d Marine heatwaves may compromise ability to respond to future climatic change
Extreme events are increasing globally with devastating ecological consequences, but the impacts on underlying genetic diversity and structure are often cryptic and poorly understood, hindering assessment of adaptive capacity and ecosystem vulnerability to future change. Using very rare "before" data we empirically demonstrate that an extreme marine heatwave caused a significant poleward shift in genetic clusters of kelp forests whereby alleles characteristic of cool water were replaced by those that predominated in warm water across 200 km of coastline. This "genetic tropicalisation" was facilitated by significant mortality of kelp and other co-occurring seaweeds within the footprint of the heatwave that opened space for rapid local proliferation of surviving kelp genotypes or dispersal and recruitment of spores from warmer waters. Genetic diversity declined and inbreeding increased in the newly tropicalised site, but these metrics were relative stable elsewhere within the footprint of the heatwave. Thus, extreme events such as marine heatwaves not only lead to significant mortality and population loss but can also drive significant genetic change in natural populations. Climate change is increasing the intensity and frequency of extreme events 1,2 with significant impacts to species and ecosystems on both evolutionary and contemporary time scales 3. Because extreme events, by definition, exceed normal environmental conditions, they drive significant mortality, range shifts and the transition to novel ecosystem states 4-6. However, in contrast to the ecological impacts of extreme climatic events which are often obvious and well documented, their impact on underlying patterns of genetic diversity and structure and the implications for adaptability to future change is obscure and often unknown 3,7-10 , particularly for marine systems. Marine heatwaves are extreme events defined as discrete periods of anomalously warm-water that exceed historical norms of ocean temperature 11 and are superimposed on a background of ocean warming. Marine heatwaves are increasing in frequency and duration globally 12 with significant consequences for coastal marine species, communities and the ecosystem services they provide 13-17. While we have an emerging understanding of how ocean warming may affect the genetics of marine species e.g. 18,19 , there are few empirical studies demonstrating the genetic impact of extreme marine heatwaves (but see 20,21. One of the most severe marine heatwaves ever recorded impacted ~ 2,000 km of coast off Western Australia in 2011 22 , where sea temperatures soared up to 5.5 °C above normal for several weeks Fig. 1 23,24. The heatwave precipitated widespread and significant local extinction and range contraction of entire marine communities 6,24,25 , shifts in ecological structure 6,26 and impacted fisheries 27 significantly compromising the vast ecosystem goods and services along this coastline 28. Marine forests, comprised of foundation species of kelps and seaweeds that underpin biodiversity throug...
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