The Genetic Architecture of Parallel Armor Plate Reduction in Threespine Sticklebacks

Department of Developmental Biology , Stanford University, Stanford, California, United States
PLoS Biology (Impact Factor: 9.34). 06/2004; 2(5):E109. DOI: 10.1371/journal.pbio.0020109
Source: PubMed


How many genetic changes control the evolution of new traits in natural populations? Are the same genetic changes seen in cases of parallel evolution? Despite long-standing interest in these questions, they have been difficult to address, particularly in vertebrates. We have analyzed the genetic basis of natural variation in three different aspects of the skeletal armor of threespine sticklebacks (Gasterosteus aculeatus): the pattern, number, and size of the bony lateral plates. A few chromosomal regions can account for variation in all three aspects of the lateral plates, with one major locus contributing to most of the variation in lateral plate pattern and number. Genetic mapping and allelic complementation experiments show that the same major locus is responsible for the parallel evolution of armor plate reduction in two widely separated populations. These results suggest that a small number of genetic changes can produce major skeletal alterations in natural populations and that the same major locus is used repeatedly when similar traits evolve in different locations.

Download full-text


Available from: Dolph Schluter
    • "Freshwater fish have typically evolved both fewer and smaller plates, which may contribute to neutral buoyant density in freshwater, reduced metabolic demand for calcium and phosphate, or increased body flexibility and higher burst swimming speed (Giles, 1983; Bergstrom, 2002; Myhre and Klepaker, 2009). Previous mapping studies show that distinct loci control the number and the size of armor plates in a cross between heavily armored marine and armor-reduced freshwater sticklebacks (Colosimo et al., 2004). To further study the QTL with the largest effect on plate size, we separately measured both armor-plate height and width in additional F2 progeny from the same marine 3 benthic cross and typed fish with a dense set of microsatellite markers (Table S1) designed in the region surrounding previous peak marker on chromosome XX. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Changes in bone size and shape are defining features of many vertebrates. Here we use genetic crosses and comparative genomics to identify specific regulatory DNA alterations controlling skeletal evolution. Armor bone-size differences in sticklebacks map to a major effect locus overlapping BMP family member GDF6. Freshwater fish express more GDF6 due in part to a transposon insertion, and transgenic overexpression of GDF6 phenocopies evolutionary changes in armor-plate size. The human GDF6 locus also has undergone distinctive regulatory evolution, including complete loss of an enhancer that is otherwise highly conserved between chimps and other mammals. Functional tests show that the ancestral enhancer drives expression in hindlimbs but not forelimbs, in locations that have been specifically modified during the human transition to bipedalism. Both gain and loss of regulatory elements can localize BMP changes to specific anatomical locations, providing a flexible regulatory basis for evolving species-specific changes in skeletal form. The bone morphogenetic protein gene GDF6 has evolved species-specific regulatory changes in both sticklebacks and humans, with gain and loss of particular enhancers providing a likely regulatory mechanism for changing bony armor in fish and modifying hindlimb-specific digit morphology during the transition to bipedalism in humans.
    No preview · Article · Jan 2016 · Cell
  • Source
    • "For example, GWAS successfully identified genes associated with hypoxia tolerance in Tibetan people and thermal regulation in naked mole rat (Simonson et al. 2010; Kim et al. 2011). Quantitative trait loci (QTL) analysis is a traditional approach to identify genes that contribute to the evolved traits of organisms, for example, the genes involved in the pelvic loss of stickleback and in the albino skin of cave fish (Colosimo et al. 2004; Borowsky and Wilkens 2002). Although these approaches have provided great insights for studying environmental adaptation, it is still unclear how the combination of multiple genes contributes to the fitness in an environment and how the adaptive genes are selected during the course of evolution (Barton and Keightley 2002; Barrett and Hoekstra 2011). "

    Preview · Article · Dec 2015 · G3-Genes Genomes Genetics
    • "Notable examples include floral traits involved in pollinator preference in Mimulus spp. (Bradshaw et al. 1995; Bradshaw et al. 1998; Schemske and Bradshaw 1999; Bradshaw and Schemske 2003), flowering and reproductive architecture in Arabidopsis (Alonso-Blanco et al. 1998; Johanson et al. 2000; Juenger et al. 2000; El-Assal et al. 2001; Ungerer et al. 2002, 2003), sensory bristle number in Drosophila (Mackay and Langley 1990; Lai et al. 1994; Long et al. 1998; Lyman and Mackay 1998), and morphological traits in sticklebacks (Colosimo et al. 2004; Shapiro et al. 2004). Large-effect polymorphisms were seen as explaining a substantial proportion, but not all, of the genetic variance for a typical trait (Orr and Coyne 1992; Mackay 2001a). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Perspectives on the role of large-effect quantitative trait loci (QTL) in the evolution of complex traits have shifted back and forth over the past few decades. Different sets of studies have produced contradictory insights on the evolution of genetic architecture. I argue that much of the confusion results from a failure to distinguish mutational and allelic effects, a limitation of using the Fisherian model of adaptive evolution as the lens through which the evolution of adaptive variation is examined. A molecular-based perspective reveals that allelic differences can involve the cumulative effects of many mutations plus intragenic recombination, a model that is supported by extensive empirical evidence. I discuss how different selection regimes could produce very different architectures of allelic effects under a molecular-based model, which may explain conflicting insights on genetic architecture from studies of variation within populations vs. between divergently-selected populations. I address shortcomings of genome-wide association study (GWAS) practices in light of more suitable models of allelic evolution, and suggest alternate GWAS strategies to generate more valid inferences about genetic architecture. Finally, I discuss how adopting more suitable models of allelic evolution could help redirect research on complex trait evolution toward addressing more meaningful questions in evolutionary biology.This article is protected by copyright. All rights reserved
    No preview · Article · Sep 2015 · Evolution
Show more