Date of Award

2016

Degree Type

Dissertation

Degree Name

Ph.D.

Department

Great Lakes Institute for Environmental Research

First Advisor

Heath, Daniel

Second Advisor

Pitcher, Trevor

Keywords

carotenoids, Chinook salmon, colour polymorphisms, evolution, genetics, sexual selection

Rights

CC BY-NC-ND 4.0

Abstract

Carotenoids are responsible for the characteristic red eggs, skin and flesh of salmonids. Although carotenoids are thought to provide salmon with many benefits, carotenoid pigmentation has not evolved in all, or even the majority of fishes, thus highlighting our lack of understanding of the evolutionary costs and benefits associated with the pigment. In nature, Chinook salmon (Oncorhynchus tshawytscha) exhibit extreme variation in carotenoid utilization due to genetic polymorphisms that affect carotenoid deposition into the flesh, skin and eggs, consequently resulting in two colour morphs (red and white). Chinook salmon are thus an ideal model species to study carotenoid pigmentation evolution. Using red and white Chinook salmon, I examined the proximate (genetic) and ultimate (fitness) mechanisms involved in carotenoid pigmentation. By examining these mechanisms, my thesis also determined evolutionary processes responsible for maintaining this unique colour polymorphism. In my thesis, I first examined the proximate mechanisms responsible for carotenoid pigmentation using a genome-wide association study, where I identified 90 single nucleotide polymorphisms (SNPs) associated with carotenoid pigmentation. Several SNPs mapped to locations in the Atlantic salmon (Salmo salar) genome near candidate genes for pigmentation, including genes associated with carotenoid absorption, metabolism and binding. This work therefore showed that several genes throughout the genome are responsible for carotenoid colouration in Chinook salmon. Second, I examined the effects of maternal carotenoids on early life fitness in Chinook salmon. I determined that increased carotenoids in salmon eggs can increase predation risk, where using choice trials, I show that rainbow trout (O. mykiss) predators showed a significant bias for red eggs over white eggs. Additionally, I showed that increased carotenoids in salmon eggs does not lead to benefits on offspring performance, as I found no significant difference in offspring of red and white females (i.e., eggs) in survival, size and immune, stress and oxidative stress responses. My results indicate that high levels of carotenoids are not required in Chinook salmon eggs. After determining that colour morphs were not reproductively isolated (i.e., no genetic divergence), I examined pre- and post-spawning sexual selection in red and white Chinook salmon. Under experimental breeding trials that quantified colour assortative mating, I found that red females mated assortatively with red males, whereas white females did not mate based on colour. Next, I examined post-spawning processes (sperm competition and cryptic female choice (CFC)), where, first, I found that red males had marginally faster sperm relative to white males, suggesting that carotenoid storage may affect sperm performance. However, although sperm velocity was important for predicting in vitro fertilization success under competitive fertilization trials, CFC was also a key mechanism that affected fertilization. Overall, colour assortative mating was important for red and white Chinook salmon, however red and white females employ different strategies (pre- versus post-spawning) to bias paternity in favour of males that are the same colour as themselves. In conclusion, my thesis determined that salmon are red because of several genes that influence carotenoid pigmentation. However, salmon are not red because it increases offspring performance or reproductive fitness, in fact, I demonstrated that during early life carotenoids can pose a cost rather than a benefit. Therefore, my thesis demonstrates that not all salmon need to be red, and therefore this unique colour polymorphism can be stably maintained in nature. My thesis chapters show a pattern of interactions between natural and sexual selection that promote the maintenance of both phenotypes.

Available for download on Wednesday, February 07, 2018

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