Significant differences in maternal carotenoid provisioning and effects on offspring fitness in Chinook salmon colour morphs

J Evol Biol. 2018 Dec;31(12):1876-1893. doi: 10.1111/jeb.13383. Epub 2018 Oct 27.

Abstract

In oviparous species, maternal carotenoid provisioning can deliver diverse fitness benefits to offspring via increased survival, growth and immune function. Despite demonstrated advantages of carotenoids, large intra- and interspecific variation in carotenoid utilization exists, suggesting trade-offs associated with carotenoids. In Chinook salmon (Oncorhynchus tshawytscha), extreme variation in carotenoid utilization delineates two colour morphs (red and white) that differ genetically in their ability to deposit carotenoids into tissues. Here, we take advantage of this natural variation to examine how large differences in maternal carotenoid provisioning influence offspring fitness. Using a full factorial breeding design crossing morphs and common-garden rearing, we measured differences in a suite of fitness-related traits, including survival, growth, viral susceptibility and host response, in offspring of red (carotenoid-rich eggs) and white (carotenoid-poor eggs) females. Eggs of red females had significantly higher carotenoid content than those of white females (6× more); however, this did not translate into measurable differences in offspring fitness. Given that white Chinook salmon may have evolved to counteract their maternal carotenoid deficiency, we also examined the relationship between egg carotenoid content and offspring fitness within each morph separately. Egg carotenoids only had a positive effect within the red morph on survival to eyed-egg (earliest measured trait), but not within the white morph. Although previous work shows that white females benefit from reduced egg predation, our study also supports a hypothesis that white Chinook salmon have evolved additional mechanisms to improve egg survival despite low carotenoids, providing novel insight into evolutionary mechanisms that maintain this stable polymorphism.

Keywords: carotenoid pigmentation; common garden; gene expression; genetic polymorphisms; infectious hematopoietic necrosis virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animal Feed
  • Animal Nutritional Physiological Phenomena
  • Animals
  • Carotenoids / administration & dosage*
  • Female
  • Fish Diseases / immunology
  • Fish Diseases / virology
  • Genetic Fitness*
  • Humans
  • Infectious hematopoietic necrosis virus
  • Maternal Nutritional Physiological Phenomena
  • Ovum
  • Pigmentation / genetics*
  • Pigmentation / physiology*
  • Real-Time Polymerase Chain Reaction / veterinary
  • Rhabdoviridae Infections / immunology
  • Rhabdoviridae Infections / veterinary
  • Rhabdoviridae Infections / virology
  • Salmon / growth & development
  • Salmon / physiology*

Substances

  • Carotenoids

Associated data

  • GENBANK/NM_001124246.1
  • GENBANK/AY685220
  • GENBANK/AF498320.1
  • GENBANK/DQ778946.1
  • GENBANK/DQ778949.1
  • GENBANK/DQ778945.1
  • GENBANK/AY788890
  • GENBANK/GT897808
  • GENBANK/AF076620
  • GENBANK/CA058263
  • GENBANK/GT897806
  • GENBANK/CB515644
  • GENBANK/U34718.1
  • GENBANK/AY523661
  • GENBANK/AF178053
  • GENBANK/X65263
  • GENBANK/CB506793
  • GENBANK/AY870265
  • GENBANK/X99303
  • GENBANK/AF329700
  • GENBANK/CB498619
  • GENBANK/NM_001124436
  • GENBANK/AY495372.1
  • GENBANK/U35064.1
  • GENBANK/U89945.1
  • GENBANK/DQ139342.1
  • GENBANK/AF469663.1
  • GENBANK/AF281338.1
  • GENBANK/NM_0011605591
  • GENBANK/CA057296
  • GENBANK/FJ265710
  • GENBANK/FJ265715
  • Dryad/10.5061/dryad.33m546g