Parallel developmental genetic features underlie stickleback gill raker evolution

Andrew M Glazer,Phillip A Cleves,Angela Y Lam,Craig T Miller,Priscilla A Erickson

doi:10.1186/2041-9139-5-19

Abstract

BackgroundConvergent evolution, the repeated evolution of similar phenotypes in independent lineages, provides natural replicates to study mechanisms of evolution. Cases of convergent evolution might have the same underlying developmental and genetic bases, implying that some evolutionary trajectories might be predictable. In a classic example of convergent evolution, most freshwater populations of threespine stickleback fish have independently evolved a reduction of gill raker number to adapt to novel diets. Gill rakers are a segmentally reiterated set of dermal bones important for fish feeding. A previous large quantitative trait locus (QTL) mapping study using a marine × freshwater F2 cross identified QTL on chromosomes 4 and 20 with large effects on evolved gill raker reduction.ResultsBy examining skeletal morphology in adult and developing sticklebacks, we find heritable marine/freshwater differences in gill raker number and spacing that are specified early in development. Using the expression of the Ectodysplasin receptor (Edar) gene as a marker of raker primordia, we find that the differences are present before the budding of gill rakers occurs, suggesting an early change to a lateral inhibition process controlling raker primordia spacing. Through linkage mapping in F2 fish from crosses with three independently derived freshwater populations, we find in all three crosses QTL overlapping both previously identified QTL on chromosomes 4 and 20 that control raker number. These two QTL affect the early spacing of gill raker buds.ConclusionsCollectively, these data demonstrate that parallel developmental genetic features underlie the convergent evolution of gill raker reduction in freshwater sticklebacks, suggesting that even highly polygenic adaptive traits can have a predictable developmental genetic basis.

Highlights

Convergent evolution, the repeated evolution of similar phenotypes in independent lineages, provides natural replicates to study mechanisms of evolution
Heritable evolution of differences in gill raker pattern in three freshwater populations To test whether multiple freshwater populations have evolved a heritable change in gill raker number and spacing, we compared skeletal morphology in marine and freshwater wild and lab-reared fish
Across the lab-reared and wild datasets ventral row 1 raker number and spacing were generally moderately anti-correlated (Additional file 5: Figure S4). These data show that relative to ancestral marine fish, fish from these three derived freshwater populations have convergently evolved a heritable decrease in adult gill raker number and increase in gill raker spacing

Summary

Introduction

Convergent evolution, the repeated evolution of similar phenotypes in independent lineages, provides natural replicates to study mechanisms of evolution. One striking conclusion from these studies is that convergent evolution often occurs via parallel genetic mechanisms, with the same genomic regions, genes, and sometimes even alleles used for evolutionary change This genetic parallelism of convergent evolution has been observed in naturally [18,19,20,21,22,23] and artificially [24,25,26] selected populations of animals, as well as in plants [27,28,29,30], and experimentally evolved microbes [31,32,33]. These common phenomena of convergent and parallel evolution suggest that some evolutionary trajectories are constrained and perhaps even predictable

Methods

Results

Discussion

Conclusion