Is phenotypic plasticity use-it-or-lose-it? Exploring genetic assimilation of salinity-plastic traits across threespine stickleback (Gasterosteus aculeatus) populations

Abstract

Understanding the response of phenotypically plastic traits to novel environments is critical to predicting evolutionary dynamics. 'Simpson-Baldwin dynamics' refer to the expected evolutionary response of a plastic trait to a constant novel environment: an initial increase in plasticity followed by a long-term decline. While theoretically well-supported, demonstrating Simpson-Baldwin dynamics has proven elusive in natural populations - and the mechanisms underlying a predicted long-term loss of plasticity remain obscure, with no clear evidence of a universal cost to plasticity. By lab-rearing diverse, wild-caught threespine stickleback (Gasterosteus aculeatus) populations under a range of salinities and recording the plasticity of morphological, physiological and fitness-related traits, we provide evidence of Simpson-Baldwin dynamics and insights into the underlying mechanisms. Following freshwater colonisation, populations showed a short-term increase or maintenance of salinity tolerance breadth - while a subsequent loss of salinity tolerance occurred in most, but not all, populations over the longer term. Despite variability amongst physiological and morphological responses to increased salinity across populations, we find that resolution of generalist-specialist trade-offs may drive plasticity loss: less-plastic populations grew faster in freshwater. Our findings establish that Simpson-Baldwin dynamics can apply to plastic traits in natural populations, although the underlying mechanisms may be variable, even within species.

Keywords: Phenotypic plasticity; Simpson-Baldwin dynamics; genetic assimilation; salinity tolerance; specialist-generalist trade-off; threespine stickleback.