Research Article: The Genetic Architecture of Parallel Armor Plate Reduction in Threespine Sticklebacks

Date Published: May 30, 2004

Publisher: Public Library of Science

Author(s): Pamela F Colosimo, Catherine L Peichel, Kirsten Nereng, Benjamin K Blackman, Michael D Shapiro, Dolph Schluter, David M Kingsley

Abstract: 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.

Partial Text: The number and type of genetic changes that control morphological and physiological changes during vertebrate evolution are not yet known. The evolutionary history of threespine sticklebacks (Gasterosteus aculeatus) provides an unusual opportunity to directly study the genetic architecture of adaptive divergence in natural populations. At the end of the last ice age, marine sticklebacks colonized newly formed freshwater environments throughout the Northern Hemisphere. Over the last 10,000 to 15,000 years, these fish have adapted to a wide range of new ecological conditions, giving rise to diverse populations with striking differences in morphology, physiology, and behavior (Bell and Foster 1994). Major changes in the bony armor have evolved repeatedly in different locations, and several hypotheses have been proposed to explain this morphological transformation, including response to changes in calcium availability (Giles 1983), stream gradients (Baumgartner and Bell 1984), or temperature, salinity, or other factors that may vary in parallel with climate (Heuts 1947; Hagen and Moodie 1982); or exposure to different types of predators (Hagen and Gilbertson 1973a; Moodie et al. 1973; Reimchen 1992; Reimchen 1995).

To directly analyze the number and location of genetic loci that control plate phenotypes, we crossed a completely plated marine fish with a low-plated benthic fish from Paxton Lake, British Columbia. Three hundred sixty progeny from a single F2 family (Cross 1) were examined in detail for the pattern, number, and size of lateral plates and then genotyped for the inheritance of different alleles at 160 polymorphic loci distributed across all linkage groups. The segregation of plate phenotypes was compared to the segregation of all genetic markers using quantitative trait loci (QTL) analysis (MapQTL; van Ooijen et al. 2002). Significance thresholds for detecting linkage were chosen using conservative criteria for genomewide linkage mapping in noninbred populations (log likelihood ratio [LOD] score ≥ 4.5; van Ooijen 1999).

The GenBank accession numbers for the Bmp6 gene is AY547294 and for the 12 additional new microsatellites Stn 210–219, 222–223 are BV102488–BV102499.



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