Extreme climate shifts pest dominance hierarchy through thermal evolution and transgenerational plasticity

Dominance hierarchy, the dominance ranking of members in a community, is determined by the relative population fitness of coexisting species. Climate change can shift dominance hierarchies depending on how species respond to changing climate, but ecological mechanisms underlying such shifts remain largely unknown. Specifically, dominance hierarchy shifts under climate change have rarely been linked to eco-evolutionary responses to thermal extremes, which we consider in this study. We conducted an 8-year field survey to link extreme high-temperature events to the shift in dominance hierarchy of two worldwide cereal aphid species (Rhopalosiphum padi and Sitobion avenae), which may respond rapidly through evolutionary or plastic responses to thermal extremes due to their short generation duration, clonal structure and high thermal sensitivity. To further understand the mechanism involved in this change in species' dominance, we characterised aphid heat tolerance and demography of the two species sourced from relatively mild (Xinxiang) and hot (Wuhan) locations in a common garden design and compared the same measures in up- and down-selected lines of the two aphid species. We found that accumulation of extreme high-temperature events (EHTs) affected per capita growth rate of S. avenae but not R. padi, driving a shift in annual relative dominance of these two common species in wheat fields. Furthermore, evidence from common garden tests and artificial thermal selection revealed that evolutionary and plastic changes in thermal tolerance under EHTs were species-dependent; R. padi evolved higher heat tolerance without reducing fitness while S. avenae did not evolve heat tolerance but showed detrimental transgenerational plastic changes under thermal extremes. Rhopalosiphum padi may take over the dominant position of S. avenae in a warmer future, due to a higher evolutionary potential of heat tolerance and less detrimental plasticity following selection. Field surveys and laboratory experiments together point to a shift in species dominance related to interspecific differences in species' evolutionary rates and transgenerational plasticity of thermal traits during selection events associated with extreme climatic conditions. This study highlights that eco-evolutionary dynamics can contribute to community responses to natural thermal extremes. A free Plain Language Summary can be found within the Supporting Information of this article.