Academic journal article Genetics

Evolution of Schooling Behavior in Threespine Sticklebacks Is Shaped by the Eda Gene

Academic journal article Genetics

Evolution of Schooling Behavior in Threespine Sticklebacks Is Shaped by the Eda Gene

Article excerpt

BIOLOGISTS have long recognized that there must be genetic contributions to the evolution of behavioral differences among animals. Although genes that are necessary to perform specific behaviors have been identified through laboratory studies of inbred animals, these may not be the genes that underlie differences in behavior between individuals or species in nature (Boake et al. 2002; Hoekstra 2010). Because many behaviors arise from a complex interaction between multiple genes and the environment, it has been difficult to identify mutations that cause natural variation in behavior. Consequently, little is known about the genetic changes that enable behavior patterns to change in response to evolutionary forces, particularly in vertebrates (Bendesky and Bargmann 2011; Martin and Orgogozo 2013). To overcome these challenges, we used a combination of forward genetic mapping and transgenesis to identify Ectodysplasin (Eda) as a gene that contributes to the evolution of schooling behavior in threespine stickleback fish (Gasterosteus aculeatus).

Schooling is a fascinating behavior known to vary widely amongfishspecies,dueto evolutionarytrade-offsbetweenthe costs and benefits of group living (Krause and Ruxton 2002). To understand the proximate mechanisms that underlie the evolution of schooling behavior, we previously developed an assay to elicit naturalistic schooling in response to a controlled stimulus, a robotic school of model sticklebacks (Wark et al. 2011). This assay permits quantification of the two critical features of schooling behavior: motivation to school and ability to maintain an efficient body position within the school (Pitcher 1983). Marine sticklebacks from open-water, pelagic habitats school extensively both in the wild and in response to the model school (Wark et al. 2011; Di-Poi et al. 2014). They follow the school for extended durations and displayparallelbodypositionwiththemodelswhenschooling (Figure 1). In contrast, sticklebacks from benthic lake habitats spend significantly less time with the model school (Wark et al. 2011). When benthic fish attempt to school, they are less capable of performing this complex behavior, exhibiting an inefficient body position characterized by a significantly less parallel angle with the model fish (Figure 1). Thus, this assay recapitulates the reduced schooling behavior observed in wild benthic sticklebacks, which is likely an adaptation to the abundant shelter in their highly vegetated lake environment (Larson 1976; Vamosi 2002; Wark et al. 2011).

Our previous genome-wide linkage mapping of schooling behavior in a benthic 3 marine F2 intercross demonstrated that the ability to school and the motivation to school map to distinct genomic regions. Schooling ability, as measured by body position when schooling with the models, shows significant linkage to a region on chromosome 4 (Greenwood et al. 2013). Interestingly, this genomic region is also genetically linked to the presence of bony armor and the patterning of the sensory neuromasts of the lateral line (Wark et al. 2012). Both of these phenotypes are controlled by the Eda gene, which is contained within the schooling locus on chromosome 4 (Colosimo et al. 2005; Mills et al. 2014).

Here, we tested whether variation in Eda might also contribute to differences in schooling ability between marine and benthic sticklebacks by manipulating Eda expression in benthic sticklebacks. Benthics have significantly lower expression of Eda than marine sticklebacks in the developing flank (Mills et al. 2014; O'Brown et al. 2015) and in the brain (Supplemental Material, Figure S1). We had previously generated transgenic benthic sticklebacks that express the marine allele of the Eda complementary DNA (cDNA) under the control of a cytomegalovirus (CMV) promoter, which should drive constitutive expression of Eda throughout the fish (Mills et al. 2014). Here, we bred six CMV:Eda founder individuals to wild-type benthics to establish six independent stable benthic CMV:Eda transgenic lines. …

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