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Symbiosis can benefit hosts in numerous ways, but less is known about whether interactions with hosts benefit symbionts—the smaller species in the relationship. To determine the fitness impact of host association on symbionts in likely mutualisms, we conducted a meta-analysis across 91 unique host-symbiont pairings under a range of spatial and temporal contexts. Specifically, we assess the consequences to symbiont fitness when in and out of symbiosis, as well as when the symbiosis is under suboptimal or varying environments and biological conditions (e.g., host age). We find that some intracellular symbionts associated with protists tend to have greater fitness when the symbiosis is under stressful conditions. Symbionts of plants and animals did not exhibit this trend, suggesting that symbionts of multicellular hosts are more robust to perturbations. Symbiont fitness also generally increased with host age. Lastly, we show that symbionts able to proliferate in- and outside host cells exhibit greater fitness than those found exclusively inside or outside cells. The ability to grow in multiple locations may thus help symbionts thrive. We discuss these fitness patterns in light of host-driven factors, whereby hosts exert influence over symbionts to suit their own needs.

 

Hoffmann and Bridle [ 1. ] describe two processes that the framework introduced by Vinton et al. [ 2. ] did not explicitly consider. These two processes, reversibility of plastic responses and time lags in sensitivity of responses to the environment, can affect how plasticity impacts evolution. These processes are easily incorporated into our framework by adding stage structure and lagged environmental drivers. In Vinton et al. [ 2. ], when discussing the costs of plasticity, we primarily focused on energetic impacts on fitness, and the role of environmental predictability. Hoffmann and Bridle [ 1. ] are correct that differential impacts of plasticity across an individual’s lifetime might determine its response to different types of environmental change. 

To forecast extinction risks of natural populations under climate change and direct human impacts, an integrative understanding of both phenotypic plasticity and adaptive evolution is essential. To date, the evidence for whether, when, and how much plasticity facilitates adaptive responses in changing environments is contradictory. We argue that explicitly considering three key environmental change components – rate of change, variance, and temporal autocorrelation – affords a unifying framework of the impact of plasticity on adaptive evolution. These environmental components each distinctively effect evolutionary and ecological processes underpinning population viability. Using this framework, we develop expectations regarding the interplay between plasticity and adaptive evolution in natural populations. This framework has the potential to improve predictions of population viability in a changing world.