Evolution of phenology in a salmonid population: a potential adaptive response to climate change

Abstract

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. Résumé :Si une accumulation d'observations indique que de nombreuses populations de poissons réagissent aux changements climatiques en modifiant le moment de leur migration, les données génétiques qui établissent le rôle de l'évolution dans ces modifications sont rares. Une des premières démonstrations de l'évolution du moment de la migration a été produite en suivant des allèles d'allozymes ayant fait l'objet de manipulations expérimentales pour marquer génétiquement des saumons roses (Oncorhynchus gorbuscha) à migration tardive. Nous élargissons ces recherches en utilisant des observations d'allèles marqueurs chez des alevins afin de démontrer que ces changements du moment de la migration ont été causés par une sélection directionnelle contre le phénotype à migration tardive durant la phase océanique du cycle de vie des salmonidés. L'évènement de sélection, qui semble avoir été provoqué par un réchauffement vernal précoce du milieu marin sublittoral et la baisse conséquente de la survie des alevins à migration tardive par rapport à celle des alevins à migration précoce, s'est traduit par une diminution du phénotype à migration tardive de plus de 50 % à environ 10 % de l'abondance totale des alevins en une seule génération. Ces changements dé-mographiques ont persisté durant les 13 générations subséquentes et donnent à penser qu'une tendance plus vaste vers un moment de migration plus précoce dans cette population pourrait refléter une adaptation à la hausse des températures de la surface de la mer. [Traduit par la Rédaction]

Single-nucleotide polymorphism data describe contemporary population structure and diversity in allochronic lineages of pink salmon (Oncorhynchus gorbuscha)

“…Similar responses to climate change have already been observed in both lineages with changes to migration timing thought to better match new environmental conditions. Kovach et al (2013) observed earlier migration timing in both lineages, and evidence for the genetic basis of the change in the odd-year lineage is accumulating (Kovach et al 2012, Manhard et al 2017).…”

Thermal exposure of adult Chinook salmon and steelhead: Diverse behavioral strategies in a large and warming river system

“…It is well established that adult salmonid migration timing and spawn timing are genetically heritable over generations [ 17 , 18 ] and that these traits reflect historical adaptation to river discharge and temperature patterns [ 19 , 20 ]. There is also accumulating evidence that recent phenological shifts in many salmonid populations have occurred in response to climate-driven warming and have been accompanied by genetic changes [ 21 – 23 ]. What is much less clear is whether population-level adaptation can keep pace with climate change, and this is currently a central question in salmonid conservation and management.…”

A bioenergetics evaluation of temperature‐dependent selection for the spawning phenology by Snake River fall Chinook salmon

“…Therefore, the biological limit of 4 kJ/g to sustain biological function under prevailing temperatures could not explain the end of the observed spawning migration. Other factors such as subsequent selection pressures and evolutionary feed‐backs resulting from the poor survival of eggs and fry as a consequence of late spawning are likely mechanisms that could explain the end of the spawning migration (Brannon, ; Manhard, Joyce, & Gharrett, ; Rand et al., ). The inability for energy use to explain the end of the observed spawning migration was not an unexpected result.…”