The Genetic Architecture of Skeletal Convergence and Sex Determination in Ninespine Sticklebacks

Abstract

SUMMARY The history of life offers plentiful examples of convergent evolution, the independent derivation of similar phenotypes in distinct lineages [1]. Convergent phenotypes among closely related lineages (frequently termed “parallel” evolution) are often assumed to result from changes in similar genes or developmental pathways [2], but the genetic origins of convergence remains poorly understood. Ninespine (Pungitius pungitius) and threespine (Gasterosteus aculeatus) stickleback fish provide many examples of convergent evolution of adaptive phenotypes, both within and between genera. The genetic architecture of several important traits is now known for threespine sticklebacks [3–10]; thus, ninespine sticklebacks thus provide a unique opportunity to critically test whether similar or different chromosome regions control similar phenotypes in these lineages. We have generated the first genome-wide linkage map for the ninespine stickleback and used quantitative trait locus (QTL) mapping to identify chromosome regions controlling several skeletal traits and sex determination. In ninespine sticklebacks, these traits mapped to chromosome regions not previously known to control the corresponding traits in threespine sticklebacks. Therefore, convergent morphological evolution in these related, but independent, vertebrate lineages may have different genetic origins. Comparative genetics in sticklebacks provides an exciting opportunity to study the mechanisms controlling similar phenotypic changes in different groups of animals.

Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila

“…In some of these cases, similar morphologies have evolved independently via changes in the same genes or genetic pathways (Chan et al, 2010;Protas et al, 2006;Prud'homme et al, 2006;Sucena et al, 2003;Zhang et al, 2012). However, in other cases convergent evolution of similar traits arises through different developmental or genetic mechanisms (Moczek et al, 2006;Shapiro et al, 2009;Steiner et al, 2009;Tanaka et al, 2009;Wittkopp et al, 2003;Zwaan et al, 2000).…”

The genetic and molecular architecture of phenotypic diversity in sticklebacks

“…Interestingly, both mechanisms can be involved when the same trait evolves. For example, the Pitx1 gene is responsible for the independent loss of pelvic structures in both threespine and ninespine stickleback populations; however, there are also threespine and ninespine populations with pelvic loss that is unlinked to mutations in Pitx1 [25,49,51,68,69]. Remarkably, it has also been suggested that variation in the Pitx1 gene contributes to loss of hindlimbs in manatees [69], and variation in other genes and pathways important for phenotypic evolution in sticklebacks (Kitlg, Gdf6, Eda) has also been implicated in phenotypic evolution in humans [28,70,74,75].…”

“…To date, there have been 28 QTL studies published in threespine stickleback [10,18,23 -48] and four in ninespine stickleback [49][50][51][52] (electronic supplementary material, tables S1 and S2). Most of these studies (19 in threespine, 3 in ninespine) have focused on divergence between the marine and freshwater ecotypes, with a smaller number of studies investigating divergence between freshwater ecotypes (benthic-limnetic, lake-stream) or between two marine species in Japan (G. aculeatus, G. nipponicus).…”

Confusion and dependence in uses of history

“…These kinds of nonhistorical data and analyses include work in quantitative genetics, genomics, population genetics, molecular evolution, field studies, and developmental biology. The nonhistorical data collected with this work and analyzed by Kingsley, members of his lab, colleagues, and Kingsley's former students with their own labs provide insights into how changes occur in evolution generally and in micro versus macroevolution in particular (Colosimo et al 2004(Colosimo et al , 2005Shapiro et al 2006;Shapiro et al 2009;Kingsley and Peichel 2007;Miller et al 2007;Hendry et al 2009;Kitano et al 2009;Chan et al 2010;Schluter et al 2010). We will elaborate on this approach in Sect.…”

“…3.2, one of the leading approaches to providing such explanations uses nonhistorical methods and nonhistorical properties involving hybrid mating and genomic tools/analysis to learn about the genetic architecture of evolutionary changes in courtship behavior, including the mechanisms underlying evolutionary changes in neural circuitry. This work follows the steps of Kingsley's lab in using stickleback genetic and genomic studies to learn about the molecular basis of vertebrate evolution more generally (Colosimo et al 2004(Colosimo et al , 2005Shapiro et al 2006;Shapiro et al 2009;Kingsley and Peichel 2007;Miller et al 2007;Kitano et al 2009;Schluter et al 2010). Enc's (1995) version of the indispensability argument: a brief case study Enc (1995) argues for a paradigm shift in how we understand certain classes of behavior.…”