Recent warming reduces the reproductive advantage of large size and contributes to evolutionary downsizing in nature

Body size is a key functional trait that is predicted to decline under warming. Warming is known to cause size declines via phenotypic plasticity, but evolutionary responses of body size to warming are poorly understood. To test for warming-induced evolutionary responses of body size and growth rates, we used populations of mosquitofish ( Gambusia affinis ) recently established (less than 100 years) from a common source across a strong thermal gradient (19–33°C) created by geothermal springs. Each spring is remarkably stable in temperature and is virtually closed to gene flow from other thermal environments. Field surveys show that with increasing site temperature, body size distributions become smaller and the reproductive advantage of larger body size decreases. After common rearing to reveal recently evolved trait differences, warmer-source populations expressed slowed juvenile growth rates and increased reproductive effort at small sizes. These results are consistent with an adaptive basis of the plastic temperature–size rule, and they suggest that temperature itself can drive the evolution of countergradient variation in growth rates. The rapid evolution of reduced juvenile growth rates and greater reproduction at a small size should contribute to substantial body downsizing in populations, with implications for population dynamics and for ecosystems in a warming world.Funding provided by: Division of Environmental BiologyCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000155Award Number: 1457333Funding provided by: Division of Environmental BiologyCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000155Award Number: 1457112Funding provided by: Royal Society of New ZealandCrossref Funder Registry ID: Award Number: 16-UOA-02