Distinct developmental and genetic mechanisms underlie convergently evolved tooth gain in sticklebacks

Abstract

Teeth are a classic model system of organogenesis, as repeated and reciprocal epithelial and mesenchymal interactions pattern placode formation and outgrowth. Less is known about the developmental and genetic bases of tooth formation and replacement in polyphyodonts, which are vertebrates with continual tooth replacement. Here, we leverage natural variation in the threespine stickleback fish Gasterosteus aculeatus to investigate the genetic basis of tooth development and replacement. We find that two derived freshwater stickleback populations have both convergently evolved more ventral pharyngeal teeth through heritable genetic changes. In both populations, evolved tooth gain manifests late in development. Using pulse-chase vital dye labeling to mark newly forming teeth in adult fish, we find that both high-toothed freshwater populations have accelerated tooth replacement rates relative to lowtoothed ancestral marine fish. Despite the similar evolved phenotype of more teeth and an accelerated adult replacement rate, the timing of tooth number divergence and the spatial patterns of newly formed adult teeth are different in the two populations, suggesting distinct developmental mechanisms. Using genome-wide linkage mapping in marine-freshwater F2 genetic crosses, we find that the genetic basis of evolved tooth gain in the two freshwater populations is largely distinct. Together, our results support a model whereby increased tooth number and an accelerated tooth replacement rate have evolved convergently in two independently derived freshwater stickleback populations using largely distinct developmental and genetic mechanisms.

Microinjection for Transgenesis and Genome Editing in Threespine Sticklebacks

“…Genetic mapping experiments have identified genomic regions underlying evolved phenotypes 4–6 , and in a few cases, the functional roles of specific candidate genes have been tested 7,8 . A number of genomic regions underlying morphological changes have been identified with promising candidate genes, but these candidates have not yet been functionally tested 9–12 . In addition, sticklebacks are common models for studies of population genetics/genomics 13,14 , speciation 15 , behavior 1 , endocrinology 16 , ecotoxicology 17 , immunology 18 and parasitology 19 .…”

Regulatory architecture of gene expression variation in the threespine stickleback, Gasterosteus aculeatus

“…However, only one of the trans-eQTL hotspots n (continued) found in this study (Chr12a) overlapped with genomic regions repeatedly found to be associated with marine/freshwater divergence by Hohenlohe et al (2010), Jones et al (2012), or Terekhanova et al (2014. Nevertheless, several studies indicate that adaptation to novel aquatic environments may also involve parts of the genome outside these large target regions (DeFaveri et al 2011;Leinonen et al 2012;Ellis et al 2015;Erickson et al 2016;Ferchaud and Hansen 2016). The QTL underlying physiological adaptations to different aquatic environments in sticklebacks have not been well characterized.…”

“…Successful colonization of these diverse habitats necessitates behavioral, morphological, and physiological adaptation to novel environmental conditions including changed temperature, salinity, oxygen, light, parasite and predator regimens, a process that can occur rapidly (Kitano et al 2010;Barrett et al 2011;Terekhanova et al 2014;Lescak et al 2015;Huang et al 2016, Rennison et al 2016. Parallel adaptations between independently founded freshwater populations frequently involve the same regions of the genome and arise from preexisting genetic variation in the marine population (Colosimo et al 2005;Hohenlohe et al 2010;Jones et al 2012;Liu et al 2014;Conte et al 2015, but see DeFaveri et al 2011Leinonen et al 2012;Ellis et al 2015;Ferchaud and Hansen 2016). Local adaptation in environmentally heterogeneous habitats such as the Baltic Sea (Guo et al 2015) and lake-stream complexes (Roesti et al 2015) has been shown to involve the same genomic regions.…”

Dissection and Flat-mounting of the Threespine Stickleback Branchial Skeleton

“…In cichlids, lower pharyngeal jaw morphology varies dramatically 32,33 and has been shown to be adaptive and correlated with trophic niche 34 . Multiple freshwater stickleback populations have evolved dramatic increases in ventral pharyngeal tooth number 23,35,36 . Recent work has demonstrated that the developmental genetic basis of this evolved tooth gain is largely distinct in two independently derived populations of freshwater sticklebacks 36 .…”

“…Multiple freshwater stickleback populations have evolved dramatic increases in ventral pharyngeal tooth number 23,35,36 . Recent work has demonstrated that the developmental genetic basis of this evolved tooth gain is largely distinct in two independently derived populations of freshwater sticklebacks 36 . Unlike mammalian teeth, fish regenerate their teeth continuously throughout adult life 37 .…”