DNA fragility in the parallel evolution of pelvic reduction in stickleback fish

Abstract

Evolution generates a remarkable breadth of living forms, but many traits evolve repeatedly, by still poorly understood mechanisms. A classic example of repeated evolution is the loss of pelvic hindfins in stickleback fish (Gasterosteus aculeatus). Repeated pelvic loss maps to recurrent deletions of a pelvic enhancer of the Pitx1 gene. Here, we identify molecular features contributing to these recurrent deletions. Pitx1 enhancer sequences form alternative DNA structures in vitro, and increase double-strand breaks and deletions in vivo. Enhancer mutability depends on DNA replication direction and is caused by (TG)-dinucleotide repeats. Modeling shows that elevated mutation rates can influence evolution under demographic conditions relevant for sticklebacks and humans. DNA fragility may thus help explain why the same loci are often used repeatedly during parallel adaptive evolution.

A silent orchestra: convergent song loss in Hawaiian crickets is repeated, morphologically varied, and widespread

“…Our observations are consistent with recent evidence for high evolvability of trait loss under negative selection (Xie et al. ), a phenomenon widely observed among costly sexually selected traits (Wiens ), and which may play an important role in rapid adaptation of populations to novel environments or selection pressures. The recurrent disappearance of song in T. oceanicus suggests evolutionary trait or signal loss could be a common means for hosts to evade their parasites, owing to the fitness advantages that arise from evading detection.…”

A phylogenomic perspective on diversity, hybridization and evolutionary affinities in the stickleback genusPungitius

“…Finally, it may be instructive to note that much of the long-standing and continued confusion in Pungitius systematics and taxonomy may be traced back to heavy emphasis on osteological and armour (e.g., pelvis structures, spine numbers, lateral plate numbers and presence or absence of keel) traits, as well coloration, as diagnostic characters of this group (Keivany & Nelson, 2000, 2004Mattern, 2006;Takahashi & Goto, 2001). These are all traits known to have a fairly simple genetic basis in stickleback fishes (Colosimo et al, 2005;Miller et al, 2007;Shapiro et al, 2009), and are subject to recurrent losses and gains in the course of evolution (e.g., Aldenhoven et al, 2010;Kitano et al, 2008;Klepaker et al, 2013;Wang et al, 2015;Xie et al, 2019). Hence, this together with our findings suggests that the praxis of designating species in this genus solely on the basis of phenotypic variability (e.g., Shedko et al, 2005) is not biologically sound.…”

Fast sequence-based microsatellite genotyping development workflow

“…The ability of SSRseq to characterize SNP and indel present along the sequences, in addition to the targeted microsatellite, represents a new opportunity to produce empirical data to apply existing theoretical and statistical frameworks that integrate linked polymorphism with different mutation characteristics (Payseur and Cutter 2006). Finally, the ease and cost effectiveness of parallel development for multiple species make these approach convenient to develop powerful multilocus datasets for comparative population and community genetics studies (Crutsinger 2016), and to further investigate the functional implications (Bagshaw 2017) and adaptive potential of microsatellite variation among natural populations (Xie et al 2019).…”

“…Secondly, variation in the number of repeated oligonucleotide motif is a unique kind of polymorphism with specific mutation mechanism and rate which in itself provides a complementary picture of genetic variation to nucleotide substitutions across populations (Haasl and Payseur 2011) and genomes (Willems et al 2014). Thirdly, it becomes more and more obvious that microsatellite polymorphism is involved in numerous biological processes such as gene expression regulation and epigenetic mechanisms (Bagshaw 2017;Sadd et al 2018), and more generally in phenotypic variation (Xie et al 2019) including human diseases (Gymrek 2017;Hannan 2018). Thus, while marker preference evolves through time with specific markers dominating the genotyping field over a period of time following technological advances (Schlötterer 2004;Seeb et al 2011), maintaining our capability to interrogate any kind of polymorphism in the context of rapid HTS technological advances is paramount and should be prioritized.…”