Evolution of Phenology in a Salmonid Population: a Potential Adaptive Response to Climate Change
Accumulating evidence has indicated that many fish populations are responding to climate change through shifts in migration time, but genetic data identifying the role of evolution in these shifts are rare. One of the first demonstrations of evolution of migration time was produced by monitoring allozyme alleles that were experimentally manipulated to genetically mark late-migrating pink salmon (Oncorhynchus gorbuscha). Here, we extend that research by using observations of the marker alleles in fry to demonstrate that these changes in migration time were caused by directional selection against the late-migrating phenotype during the oceanic phase of the salmonid life cycle. The selective event, which appeared to be driven by early vernal warming of the nearshore marine environment and consequent decreased survival of late-migrating fry relative to earlymigrating fry, decreased the late-migrating phenotype from more than 50% to approximately 10% of the total fry abundance in only one generation. These demographic changes have persisted over the subsequent 13 generations and suggest that a larger
trend toward earlier migration time in this population may reflect adaptation to warming sea-surface temperatures.
A primary mechanism by which animal populations can respond to environmental change is by shifting the timing of life history events, known as phenology, to track optimal environmental conditions in time (Bradshaw and Holzapfel 2006, 2008; Bellard et al. 2012). Phenology is of critical importance for migratory fish, such as Pacific salmon (Oncorhynchus spp.), which must initiate an array of physiological, morphological, and behavioral changes at precise times during their life cycle (reviewed by Groot and Margolis 1991). The precision with which salmonids time migration can constrain gene flow between seasonally distinct spawning segments, thereby enabling local adaptation of phenology (Quinn et al. 2000; Fillatre et al. 2003; Gharrett et al. 2013). Evidence of local adaptation of phenology in salmonids has been provided by comparisons of seasonally distinct groups of Chinook salmon (Oncorhynchus tshawytscha) that spawn in the same river, which demonstrated significant genetic divergence at three circadian clock genes, but not at neutral markers (O’Malley et al. 2013). The tight coupling of salmonid ecology and phenology, along with the generally high heritability of phenological traits in salmonids (median h2 = 0.51; Carlson and Seamons 2008), suggests that salmonid populations may respond to periodic environmental fluctuations or persistent climatic trends through contemporary evolution of phenology.