title: Distinct developmental 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 low-toothed 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.
authors.affiliation: Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
authors.forename: Nicholas A
authors.initials: NA
authors.lastname: Ellis
authors.affiliation: Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
authors.forename: Andrew M
authors.initials: AM
authors.lastname: Glazer
authors.affiliation: Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
authors.forename: Nikunj N
authors.initials: NN
authors.lastname: Donde
authors.affiliation: Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
authors.forename: Phillip A
authors.initials: PA
authors.lastname: Cleves
authors.affiliation: Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
authors.forename: Rachel M
authors.initials: RM
authors.lastname: Agoglia
authors.affiliation: Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA ctmiller@berkeley.edu.
authors.forename: Craig T
authors.initials: CT
authors.lastname: Miller
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002874:Chromosome Mapping; D005618:Fresh Water; D018507:Gene Expression Regulation, Developmental; D008040:Genetic Linkage; D016678:Genome; D055106:Genome-Wide Association Study; D005838:Genotype; D008957:Models, Genetic; D010641:Phenotype; D040641:Quantitative Trait Loci; D023701:Smegmamorpha / Q000196:embryology* / Q000502:physiology*; D014070:Tooth / Q000196:embryology* / Q000502:physiology
keywords: Convergent evolution; Odontogenesis; Polyphyodonty; Stickleback; Tooth replacement