Dissertation/Thesis Abstract

Genetic and Developmental Analysis of Evolved Stickleback Gill Raker Reduction
by Glazer, Andrew Michael, Ph.D., University of California, Berkeley, 2015, 183; 10186673
Abstract (Summary)

Much is known about the genetic and developmental basis of mutant phenotypes in the laboratory. However, much less is known about the mechanisms that control naturally evolved phenotypes in the wild. Are specific types of genes or mutations preferred? How are developmental programs modified to generate altered phenotypes? Finally, in cases where the same phenotype has evolved in independent lineages (convergent evolution), are the same genes or mutations used?

The threespine stickleback fish (Gasterosteus aculeatus) is an emerging model organism in which the approaches and tools of developmental biology, genetics, and genomics can be applied to understand evolutionary changes. Marine sticklebacks have repeatedly colonized and adapted to new freshwater environments throughout the Northern Hemisphere. Freshwater sticklebacks have evolved many changes in their skeleton relative to marine fish. For example, freshwater sticklebacks have evolved changes to their defensive armor in response to decreased predation and changes in bones used for feeding in response to differences in diet. Despite their phenotypic differences, marine and freshwater sticklebacks can be bred in the lab. Crosses between marine and freshwater sticklebacks can be used to decipher the genetic basis of their evolved phenotypic differences.

In chapter 2 of this thesis, I present the results of a large quantitative genetic study of stickleback skeletal evolution. I mapped regions of the genome, known as quantitative trait loci (QTL), affecting a wide range of skeletal traits. Over 100 QTL were mapped, and a meta-analysis of their properties was performed. Using these QTL, several general questions in evolutionary genetics were addressed. First, I explored the dominance of the QTL. The dominance of a QTL is a genetic property that might affect likelihood of being used during adaptation.

In chapter 3 of this thesis, I focus on one skeletal trait, gill raker number. Gill rakers are periodically patterned bones in a fish’s throat important for feeding. In response to a change in diet in freshwater populations, hundreds of freshwater stickleback populations have independently evolved a reduction in gill raker number. This phenomenon is known as gill raker reduction. I found that heritable marine/freshwater differences in gill raker number were present early in development. The gill raker number differences were due to a difference in the spacing between adjacent gill rakers. The marine/freshwater number and spacing differences were present at the earliest detectable point of gill raker specification. This result suggests that gill raker reduction is caused by an early-acting change to a lateral inhibition process controlling raker bud spacing. Next, I performed linkage mapping in F2 fish from crosses with three independently derived freshwater populations. These results suggest that even highly polygenic adaptive traits can have a predictable developmental genetic basis.

In chapter 4 of this thesis, I present an economical method that uses next-generation sequencing to perform genome-wide genotyping of hundreds of multiplexed samples. This method was used to genotype two large marine by freshwater F2 crosses of over 350 fish each. The resulting maps significantly improved the stickleback genome assembly by making over 100 changes to the order and orientation of the scaffolds that compose the genome assembly. In the revised genome assembly, 95% of the assembly was anchored to a chromosome, compared to 87% in the original assembly. To assess linkage map quality, I mapped quantitative trait loci (QTL) controlling lateral plate number. Plate number mapped as expected to a 200 kilobase genomic region containing Ectodysplasin. In addition, plate number mapped to a chromosome 7 QTL overlapping a previously identified modifier QTL. Finally, I examined gill raker length. I found that the two freshwater populations convergently evolved shorter gill rakers relative to marine fish. I mapped eight QTL controlling gill raker length in the two crosses. However, none of the QTL were overlapping between the two crosses. Thus, the convergent evolution gill raker length reduction has a surprisingly non-parallel genetic basis.

In chapter 5 of this thesis, I present additional experiments to determine the genetic basis of evolved reduction in gill raker number. Using the genotyping method developed in chapter 4, I mapped QTL controlling raker number and spacing in two large marine by freshwater F2 crosses of over 350 fish each. Overlapping QTL on chromosomes 4, 16, and 20 were found in both crosses. In addition, 14 unique modifier QTL were mapped. Together these results indicate that a combination of similar and different genetic basis underlies the convergent evolution of gill raker number. (Abstract shortened by ProQuest.)

Indexing (document details)
Advisor: Miller, Craig
Commitee: Harland, Richard, Rokhsar, Daniel, Wake, Marvalee
School: University of California, Berkeley
Department: Molecular & Cell Biology
School Location: United States -- California
Source: DAI-B 78/11(E), Dissertation Abstracts International
Subjects: Biology, Genetics, Evolution and Development
Keywords: Evolution, Fgf20, Gill raker, QTL, Skeleton, Stickleback
Publication Number: 10186673
ISBN: 978-1-369-88263-6
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