Parallel Evolution of Pitx1 Underlies Pelvic Reduction in Scottish Threespine Stickleback (Gasterosteus aculeatus)

Abstract

Little is known about the genetic and molecular mechanisms that underlie adaptive phenotypic variation in natural populations or whether similar genetic and molecular mechanisms are utilized when similar adaptive phenotypes arise in independent populations. The threespine stickleback (Gasterosteus aculeatus) is a good model system to investigate these questions because these fish display a large amount of adaptive phenotypic variation, and similar adaptive phenotypes have arisen in multiple, independent stickleback populations. A particularly striking pattern of parallel evolution in sticklebacks is reduction of skeletal armor, which has occurred in numerous freshwater locations around the world. New genetic and genomic tools for the threespine stickleback have made it possible to identify genes that underlie loss of different elements of the skeletal armor. Previous work has shown that regulatory mutations at the Pitx1 locus are likely responsible for loss of the pelvic structures in independent stickleback populations from North America and Iceland. Here we show that the Pitx1 locus is also likely to underlie pelvic reduction in a Scottish population of threespine stickleback, which has apparently evolved pelvic reduction under a different selection regime than the North American populations.

Identification of Major and Minor QTL for Ecologically Important Morphological Traits in Three-Spined Sticklebacks (Gasterosteus aculeatus)

“…, Wright et al 2004; McGuigan et al 2011; Karhunen et al 2013). During the last decade, studies have started to uncover the genetic bases underlying these traits, especially the armor traits such as the lateral plates and the pelvic structure (Peichel et al 2001; Colosimo et al 2004; Cresko et al 2004; Shapiro et al 2004; Coyle et al 2007). In particular, two major genes— Ectodysplasin ( Eda ) and Pituitary homebox transcription factor 1 ( Pitx1 )—have been identified to account for plate and pelvic reduction in three-spined sticklebacks, respectively (Shapiro et al 2004; Colosimo et al 2005; Coyle et al 2007; Chan et al 2010).…”

“…In addition, almost all of the previous investigations have used mapping crosses of Pacific origin ( i.e. , Canada, United States, or Japan; Supporting Information, Table S1), whereas few QTL studies have used populations of Atlantic origin (but see Shapiro et al 2004; Coyle et al 2007). Because QTL can be lineage- and even population-specific (Symonds et al 2005; Chen and Ritland 2013), a comparative approach is necessary to distinguish ancestral adaptive variation ( i.e.…”

Modular Skeletal Evolution in Sticklebacks Is Controlled by Additive and Clustered Quantitative Trait Loci

“…Instead the same major loci Cresko et al 2004;Coyle et al 2007), the same underlying genes (Chan et al 2010), and sometimes even the same freshwater alleles ) are used repeatedly in other populations that have evolved similar phenotypes (Jones et al 2012a). All of these well-studied examples involve QTL that control half or more of the variance in the corresponding trait, and it remains unclear whether QTL with smaller effects, like many of those identified here, will also be used in parallel in other populations.…”

Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators

“…Ancestral plasticity is thought to provide the developmental mechanism for shifts between ecotypes, explaining the rapid and recurrent emergence of particular forms (6,9). This hypothesis contrasts with studies that demonstrate parallel evolution based on co-option of ancestral alleles in genes of major effect (27) or change in cis-regulatory elements of developmental control genes not involved in ancestral plasticity (28)(29)(30). In this case, we provide evidence that ancestral plastic up-regulation of Ddc has been repeatedly co-opted to produce rapid adaptation in melanin, in concert with evolution of expression in the interacting gene ebony.…”